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Bibliography on: Evolution of Multicelluarity

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Robert J. Robbins is a biologist, an educator, a science administrator, a publisher, an information technologist, and an IT leader and manager who specializes in advancing biomedical knowledge and supporting education through the application of information technology. More About:  RJR | OUR TEAM | OUR SERVICES | THIS WEBSITE

RJR: Recommended Bibliography 18 Aug 2019 at 01:33 Created: 

Evolution of Multicelluarity

Created with PubMed® Query: (evolution OR origin) AND (multicellularity OR multicellular) NOT pmcbook NOT ispreviousversion

Citations The Papers (from PubMed®)

RevDate: 2019-08-15

Miller WB, Torday JS, F Baluška (2019)

The N-Space Episenome Unifies Cellular Information Space-Time within Cognition-Based Evolution.

Progress in biophysics and molecular biology pii:S0079-6107(19)30148-8 [Epub ahead of print].

Self-referential cellular homeostasis is maintained by the measured assessment of both internal status and external conditions based within an integrated cellular information field. This cellular field attachment to biologic information space-time coordinates environmental inputs by connecting the cellular senome, as the sum of the sensory experiences of the cell, with its genome and epigenome. In multicellular organisms, individual cellular information fields aggregate into a collective information architectural matrix, termed a N-space Episenome, that enables mutualized organism-wide information management. It is hypothesized that biological organization represents a dual heritable system constituted by both its biological materiality and a conjoining N-space Episenome. It is further proposed that morphogenesis derives from reciprocations between these inter-related facets to yield coordinated multicellular growth and development. The N-space Episenome is conceived as a whole cell informational projection that is heritable, transferable via cell division and essential for the synchronous integration of the diverse self-referential cells that constitute holobionts.

RevDate: 2019-08-15

Fields C, M Levin (2019)

Somatic multicellularity as a satisficing solution to the prediction-error minimization problem.

Communicative & integrative biology, 12(1):119-132 pii:1643666.

Adaptive success in the biosphere requires the dynamic ability to adjust physiological, transcriptional, and behavioral responses to environmental conditions. From chemical networks to organisms to whole communities, biological entities at all levels of organization seek to optimize their predictive power. Here, we argue that this fundamental drive provides a novel perspective on the origin of multicellularity. One way for unicellular organisms to minimize surprise with respect to external inputs is to be surrounded by reproductively-disabled, i.e. somatic copies of themselves - highly predictable agents which in effect reduce uncertainty in their microenvironments. We show that the transition to multicellularity can be modeled as a phase transition driven by environmental threats. We present modeling results showing how multicellular bodies can arise if non-reproductive somatic cells protect their reproductive parents from environmental lethality. We discuss how a somatic body can be interpreted as a Markov blanket around one or more reproductive cells, and how the transition to somatic multicellularity can be represented as a transition from exposure of reproductive cells to a high-uncertainty environment to their protection from environmental uncertainty by this Markov blanket. This is, effectively, a transition by the Markov blanket from transparency to opacity for the variational free energy of the environment. We suggest that the ability to arrest the cell cycle of daughter cells and redirect their resource utilization from division to environmental threat amelioration is the key innovation of obligate multicellular eukaryotes, that the nervous system evolved to exercise this control over long distances, and that cancer is an escape by somatic cells from the control of reproductive cells. Our quantitative model illustrates the evolutionary dynamics of this system, provides a novel hypothesis for the origin of multicellular animal bodies, and suggests a fundamental link between the architectures of complex organisms and information processing in proto-cognitive cellular agents.

RevDate: 2019-08-15
CmpDate: 2019-08-15

Almeida LV, Coqueiro-Dos-Santos A, Rodriguez-Luiz GF, et al (2018)

Chromosomal copy number variation analysis by next generation sequencing confirms ploidy stability in Trypanosoma brucei subspecies.

Microbial genomics, 4(10):.

Although aneuploidy usually results in severe abnormalities in multicellular eukaryotes, recent data suggest that it could be beneficial for unicellular eukaryotes, such as yeast and trypanosomatid parasites, providing increased survival under stressful conditions. Among characterized trypanosomatids, Trypanosoma cruzi, Trypanosoma brucei and species from the genus Leishmania stand out due to their importance in public health, infecting around 20 million people worldwide. The presence of aneuploidies in T. cruzi and Leishmania was recently confirmed by analysis based on next generation sequencing (NGS) and fluorescence in situ hybridization, where they have been associated with adaptation during transmission between their insect vectors and mammalian hosts and in promoting drug resistance. Although chromosomal copy number variations (CCNVs) are present in the aforementioned species, PFGE and fluorescence cytophotometry analyses suggest that aneuploidies are absent from T. brucei. A re-evaluation of CCNV in T. b gambiense based on NGS reads confirmed the absence of aneuploidies in this subspecies. However, the presence of aneuploidies in the other two T. brucei subspecies, T. b. brucei and T. b. rhodesiense, has not been evaluated using NGS approaches. In the present work, we tested for aneuploidies in 26 T. brucei isolates, including samples from the three T. brucei subspecies, by both allele frequency and read depth coverage analyses. These analyses showed that none of the T. brucei subspecies presents aneuploidies, which could be related to differences in the mechanisms of DNA replication and recombination in these parasites when compared with Leishmania.

RevDate: 2019-08-14

Kuzdzal-Fick JJ, Chen L, G Balázsi (2019)

Disadvantages and benefits of evolved unicellularity versus multicellularity in budding yeast.

Ecology and evolution, 9(15):8509-8523 pii:ECE35322.

Multicellular organisms appeared on Earth through several independent major evolutionary transitions. Are such transitions reversible? Addressing this fundamental question entails understanding the benefits and costs of multicellularity versus unicellularity. For example, some wild yeast strains form multicellular clumps, which might be beneficial in stressful conditions, but this has been untested. Here, we show that unicellular yeast evolve from clump-forming ancestors by propagating samples from suspension after larger clumps have settled. Unicellular yeast strains differed from their clumping ancestors mainly by mutations in the AMN1 (Antagonist of Mitotic exit Network) gene. Ancestral yeast clumps were more resistant to freeze/thaw, hydrogen peroxide, and ethanol stressors than their unicellular counterparts, but they grew slower without stress. These findings suggest disadvantages and benefits to multicellularity and unicellularity that may have impacted the emergence of multicellular life forms.

RevDate: 2019-08-14

Small CM, Currey M, Beck EA, et al (2019)

Highly Reproducible 16S Sequencing Facilitates Measurement of Host Genetic Influences on the Stickleback Gut Microbiome.

mSystems, 4(4): pii:4/4/e00331-19.

Multicellular organisms interact with resident microbes in important ways, and a better understanding of host-microbe interactions is aided by tools such as high-throughput 16S sequencing. However, rigorous evaluation of the veracity of these tools in a different context from which they were developed has often lagged behind. Our goal was to perform one such critical test by examining how variation in tissue preparation and DNA isolation could affect inferences about gut microbiome variation between two genetically divergent lines of threespine stickleback fish maintained in the same laboratory environment. Using careful experimental design and intensive sampling of individuals, we addressed technical and biological sources of variation in 16S-based estimates of microbial diversity. After employing a two-tiered bead beating approach that comprised tissue homogenization followed by microbial lysis in subsamples, we found an extremely minor effect of DNA isolation protocol relative to among-host microbial diversity differences. Abundance estimates for rare operational taxonomic units (OTUs), however, showed much lower reproducibility. Gut microbiome composition was highly variable across fish-even among cohoused siblings-relative to technical replicates, but a subtle effect of host genotype (stickleback line) was nevertheless detected for some microbial taxa.IMPORTANCE Our findings demonstrate the importance of appropriately quantifying biological and technical variance components when attempting to understand major influences on high-throughput microbiome data. Our focus was on understanding among-host (biological) variance in community metrics and its magnitude in relation to within-host (technical) variance, because meaningful comparisons among individuals are necessary in addressing major questions in host-microbe ecology and evolution, such as heritability of the microbiome. Our study design and insights should provide a useful example for others desiring to quantify microbiome variation at biological levels in the face of various technical factors in a variety of systems.

RevDate: 2019-08-13
CmpDate: 2019-08-13

Tejos R, Rodriguez-Furlán C, Adamowski M, et al (2018)

PATELLINS are regulators of auxin-mediated PIN1 relocation and plant development in Arabidopsis thaliana.

Journal of cell science, 131(2): pii:jcs.204198.

Coordinated cell polarization in developing tissues is a recurrent theme in multicellular organisms. In plants, a directional distribution of the plant hormone auxin is at the core of many developmental programs. A feedback regulation of auxin on the polarized localization of PIN auxin transporters in individual cells has been proposed as a self-organizing mechanism for coordinated tissue polarization, but the molecular mechanisms linking auxin signalling to PIN-dependent auxin transport remain unknown. We used a microarray-based approach to find regulators of the auxin-induced PIN relocation in Arabidopsis thaliana root, and identified a subset of a family of phosphatidylinositol transfer proteins (PITPs), the PATELLINs (PATLs). Here, we show that PATLs are expressed in partially overlapping cell types in different tissues going through mitosis or initiating differentiation programs. PATLs are plasma membrane-associated proteins accumulated in Arabidopsis embryos, primary roots, lateral root primordia and developing stomata. Higher order patl mutants display reduced PIN1 repolarization in response to auxin, shorter root apical meristem, and drastic defects in embryo and seedling development. This suggests that PATLs play a redundant and crucial role in polarity and patterning in Arabidopsis.

RevDate: 2019-08-09
CmpDate: 2019-08-09

Aripovsky AV, VN Titov (2019)

[Biologocally active peptides in metabolism regulation. Peptons, peptides, amino acids, fatty acids, lipoproteins, lipids, and the effect of nutriceuticals.].

Klinicheskaia laboratornaia diagnostika, 64(1):14-23.

According to phylogenetic theory of general pathology, formation of multicellular organisms started when each cell (a unicellular organism) reached the first level of relative biological perfection. By that time the stimuli for perfection of the unicellular exhausted, and formation of the multicellular became a biological necessity. All cells, being associated, formed the second level of relative biological perfection within the principle of biological succession. The association included highly organized unicellular organisms with their specific autocrine biological functions and reactions. At the second level of relative biological perfection all humoral mediators in paracrine regulated cell communities (PC) and organs were predominantly hydrophilic and short living. They had a small molecular weight and were probably biologically active peptides (BAP). We believe that functional difference of PC and later of organs is based on differentiation of lysosomal function and production of various enzymes involved in proteolysis of dietary proteins. This allowed various PC and organs to form chemically and functionally different BAP pools from one protein upon proteolysis. Individual peptide pools in PC created the basis for morphologically and functionally different cells and organs. Cell that produces peptides can modify their concentration, chemical parameters and ratios by varying the selectivity of its proteases. In vivo regulation of metabolism by BAP has a common root in bacteria, plants and vertebrates, including Homo sapiens. The third level of relative biological perfection in the organism has formed in close association with cognitive biological function.

RevDate: 2019-08-06

Blum P, S Payne (2019)

Evidence of an Epigenetics System in Archaea.

Epigenetics insights, 12:2516865719865280 pii:10.1177_2516865719865280.

Changes in the phenotype of a cell or organism that are heritable but do not involve changes in DNA sequence are referred to as epigenetic. They occur primarily through the gain or loss of chemical modification of chromatin protein or DNA. Epigenetics is therefore a non-Mendelian process. The study of epigenetics in eukaryotes is expanding with advances in knowledge about the relationship between mechanism and phenotype and as a requirement for multicellularity and cancer. However, life also includes other groups or domains, notably the bacteria and archaea. The occurrence of epigenetics in these deep lineages is an emerging topic accompanied by controversy. In these non-eukaryotic organisms, epigenetics is critically important because it stimulates new evolutionary theory and refines perspective about biological action.

RevDate: 2019-08-05

Newman SA (2019)

Inherent forms and the evolution of evolution.

Journal of experimental zoology. Part B, Molecular and developmental evolution [Epub ahead of print].

John Bonner presented a provocative conjecture that the means by which organisms evolve has itself evolved. The elements of his postulated nonuniformitarianism in the essay under discussion-the emergence of sex, the enhanced selection pressures on larger multicellular forms-center on a presumed close mapping of genotypic to phenotypic change. A different view emerges from delving into earlier work of Bonner's in which he proposed the concept of "neutral phenotypes" and "neutral morphologies" allied to D'Arcy Thompson's analysis of physical determinants of form and studied the conditional elicitation of intrinsic organizational properties of cell aggregates in social amoebae. By comparing the shared and disparate mechanistic bases of morphogenesis and developmental outcomes in the embryos of metazoans (animals), closely related nonmetazoan holozoans, more distantly related dictyostelids, and very distantly related volvocine algae, I conclude, in agreement with Bonner's earlier proposals, that understanding the evolution of multicellular evolution requires knowledge of the inherent forms of diversifying lineages, and that the relevant causative factors extend beyond genes and adaptation to the physics of materials.

RevDate: 2019-08-02

Yeoh LM, Goodman CD, Mollard V, et al (2019)

Alternative splicing is required for stage differentiation in malaria parasites.

Genome biology, 20(1):151 pii:10.1186/s13059-019-1756-6.

BACKGROUND: In multicellular organisms, alternative splicing is central to tissue differentiation and identity. Unicellular protists lack multicellular tissue but differentiate into variable cell types during their life cycles. The role of alternative splicing in transitions between cell types and establishing cellular identity is currently unknown in any unicellular organism.

RESULTS: To test whether alternative splicing in unicellular protists plays a role in cellular differentiation, we conduct RNA-seq to compare splicing in female and male sexual stages to asexual intraerythrocytic stages in the rodent malaria parasite Plasmodium berghei. We find extensive changes in alternative splicing between stages and a role for alternative splicing in sexual differentiation. Previously, general gametocyte differentiation was shown to be modulated by specific transcription factors. Here, we show that alternative splicing establishes a subsequent layer of regulation, controlling genes relating to consequent sex-specific differentiation of gametocytes.

CONCLUSIONS: We demonstrate that alternative splicing is reprogrammed during cellular differentiation of a unicellular protist. Disruption of an alternative splicing factor, PbSR-MG, perturbs sex-specific alternative splicing and decreases the ability of the parasites to differentiate into male gametes and oocysts, thereby reducing transmission between vertebrate and insect hosts. Our results reveal alternative splicing as an integral, stage-specific phenomenon in these protists and as a regulator of cellular differentiation that arose early in eukaryotic evolution.

RevDate: 2019-08-01

Olin-Sandoval V, Yu JSL, Miller-Fleming L, et al (2019)

Lysine harvesting is an antioxidant strategy and triggers underground polyamine metabolism.

Nature pii:10.1038/s41586-019-1442-6 [Epub ahead of print].

Both single and multicellular organisms depend on anti-stress mechanisms that enable them to deal with sudden changes in the environment, including exposure to heat and oxidants. Central to the stress response are dynamic changes in metabolism, such as the transition from the glycolysis to the pentose phosphate pathway-a conserved first-line response to oxidative insults1,2. Here we report a second metabolic adaptation that protects microbial cells in stress situations. The role of the yeast polyamine transporter Tpo1p3-5 in maintaining oxidant resistance is unknown6. However, a proteomic time-course experiment suggests a link to lysine metabolism. We reveal a connection between polyamine and lysine metabolism during stress situations, in the form of a promiscuous enzymatic reaction in which the first enzyme of the polyamine pathway, Spe1p, decarboxylates lysine and forms an alternative polyamine, cadaverine. The reaction proceeds in the presence of extracellular lysine, which is taken up by cells to reach concentrations up to one hundred times higher than those required for growth. Such extensive harvest is not observed for the other amino acids, is dependent on the polyamine pathway and triggers a reprogramming of redox metabolism. As a result, NADPH-which would otherwise be required for lysine biosynthesis-is channelled into glutathione metabolism, leading to a large increase in glutathione concentrations, lower levels of reactive oxygen species and increased oxidant tolerance. Our results show that nutrient uptake occurs not only to enable cell growth, but when the nutrient availability is favourable it also enables cells to reconfigure their metabolism to preventatively mount stress protection.

RevDate: 2019-07-29

Herron MD, Ghimire S, Vinikoor CR, et al (2014)

Fitness trade-offs and developmental constraints in the evolution of soma: an experimental study in a volvocine alga.

Evolutionary ecology research, 16(3):203-221.

Background: The evolution of mortal somatic cells was a critical step in the evolution of complex body plans and the major radiations of multicellular life. In the volvocine green algae, somatic cells are hypothesized to mitigate an increasing cost of reproduction as colony size increases, primarily by providing motility to the colony during reproduction.

Questions: Does selection on colony size cause an evolutionary response in proportion of somatic cells? Does the effect of selection on colony size differ in environments that differ in the importance of motility?

Methods: We subjected an outcrossed population of the volvocine alga Pleodorina starrii to selection on colony size in still and mixed environments. After approximately 40 generations with periodic selection, we estimated the relationship between colony size and proportion of soma in evolved colonies from both environments.

Results: In the largest size category, colonies selected in the still environment (in which motility is hypothesized to be more important) had a higher proportion of soma than those from the mixed environment. Within-strain variation in cell number was surprisingly large: up to 16-fold for some genotypes. The positive among-species relationship between colony size and proportion of soma was paralleled within the larger (16- to 64-celled) colonies of P. starrii, but not within the smaller (4- and 8-celled) colonies, which had the highest proportions of soma, suggesting the existence of an evolutionary constraint preventing optimization of soma in the smallest size classes.

RevDate: 2019-07-26

Lu TM, Kanda M, Furuya H, et al (2019)

Dicyemid mesozoans: a unique parasitic lifestyle with reduced genome.

Genome biology and evolution pii:5536717 [Epub ahead of print].

Dicyemids, previously called "mesozoans" (intermediates between unicellular protozoans and multicellular metazoans), are an enigmatic animal group. They have a highly simplified adult body, comprising only ∼30 cells, and they have a unique parasitic lifestyle. Recently, dicyemids were shown to be spiralians, with affinities to the Platyhelminthes. In order to understand molecular mechanisms involved in evolution of this odd animal, we sequenced the genome of Dicyema japonicum and a reference transcriptome assembly using mixed-stage samples. The D. japonicum genome features a high proportion of repetitive sequences that account for 49% of the genome. The dicyemid genome is reduced to approximately 67.5 Mb with 5,012 protein-coding genes. Only four Hox genes exist in the genome, with no clustering. Gene distribution in KEGG pathways shows that D. japonicum has fewer genes in most pathways. Instead of eliminating entire critical metabolic pathways, parasitic lineages likely simplify pathways by eliminating pathway-specific genes, while genes with fundamental functions may be retained in multiple pathways. In principle, parasites can stand to lose genes that are unnecessary, in order to conserve energy. However, whether retained genes in incomplete pathways serve intermediate functions and how parasites overcome the physiological needs served by lost genes, remain to be investigated in future studies.

RevDate: 2019-07-23
CmpDate: 2019-07-23

Zannier F, Portero LR, Ordoñez OF, et al (2019)

Polyextremophilic Bacteria from High Altitude Andean Lakes: Arsenic Resistance Profiles and Biofilm Production.

BioMed research international, 2019:1231975.

High levels of arsenic present in the High Altitude Andean Lakes (HAALs) ecosystems selected arsenic-resistant microbial communities which are of novel interest to study adaptations mechanisms potentially useful in bioremediation processes. We herein performed a detailed characterization of the arsenic tolerance profiles and the biofilm production of two HAAL polyextremophiles, Acinetobacter sp. Ver3 (Ver3) and Exiguobacterium sp. S17 (S17). Cellular adherence over glass and polypropylene surfaces were evaluated together with the effect of increasing doses and oxidative states of arsenic over the quality and quantity of their biofilm production. The arsenic tolerance outcomes showed that HAAL strains could tolerate higher arsenic concentrations than phylogenetic related strains belonging to the German collection of microorganisms and cell cultures (Deutsche Sammlung von Mikroorganismen und Zellkulturen, DSMZ), which suggest adaptations of HAAL strains to their original environment. On the other hand, the crystal violet method (CV) and SEM analysis showed that Ver3 and S17 were able to attach to solid surfaces and to form the biofilm. The quantification of biofilms production in 48 hours' cultures through CV shows that Ver3 yielded higher production in the treatment without arsenic cultured on a glass support, while S17 yield higher biofilm production under intermediate arsenic concentration on glass supports. Polypropylene supports had negative effects on the biofilm production of Ver3 and S17. SEM analysis shows that the highest biofilm yields could be associated with a larger number of attached cells as well as the development of more complex 3D multicellular structures.

RevDate: 2019-07-23
CmpDate: 2019-07-23

Yu YN, Cooper E, GJ Velicer (2017)

A conserved stem of the Myxococcus xanthus sRNA Pxr controls sRNA accumulation and multicellular development.

Scientific reports, 7(1):15411.

The small RNA (sRNA) Pxr negatively controls multicellular fruiting body formation in the bacterium Myxococcus xanthus, inhibiting the transition from growth to development when nutrients are abundant. Like many other prokaryotic sRNAs, Pxr is predicted to fold into three stem loops (SL1-SL3). SL1 and SL2 are highly conserved across the myxobacteria, whereas SL3 is much more variable. SL1 is necessary for the regulatory function of Pxr but the importance of SL3 in this regard is unknown. To test for cis genetic elements required for Pxr function, we deleted the entire pxr gene from a developmentally defective strain that fails to remove Pxr-mediated blockage of development and reintroduced variably truncated fragments of the pxr region to test for their ability to block development. These truncations demonstrated that SL3 is necessary for Pxr function in the defective strain. We further show that a highly conserved eight-base-pair segment of SL3 is not only necessary for Pxr to block development in the defective strain under starvation conditions, but is also required for Pxr to prevent fruiting body development by a developmentally proficient wild-type strain under high-nutrient conditions. This conserved segment of SL3 is also necessary for detectable levels of Pxr to accumulate, suggesting that this segment either stabilizes Pxr against premature degradation during vegetative growth or positively regulates its transcription.

RevDate: 2019-07-20

Perez-Lamarque B, H Morlon (2019)

Characterizing symbiont inheritance during host-microbiota evolution: application to the great apes gut microbiota.

Molecular ecology resources [Epub ahead of print].

Microbiota play a central role in the functioning of multicellular life, yet understanding their inheritance during host evolutionary history remains an important challenge. Symbiotic microorganisms are either acquired from the environment during the life of the host (i.e. environmental acquisition), transmitted across generations with a faithful association with their hosts (i.e. strict vertical transmission), or transmitted with occasional host-switches (i.e. vertical transmission with horizontal switches). These different modes of inheritance affect microbes' diversification, which at the two extremes can be independent from that of their associated host or follow host diversification. The few existing quantitative tools for investigating the inheritance of symbiotic organisms rely on cophylogenetic approaches, which require knowledge of both host and symbiont phylogenies, and are therefore often not well adapted to DNA metabarcoding microbial data. Here, we develop a model-based framework for identifying vertically transmitted microbial taxa. We consider a model for the evolution of microbial sequences on a fixed host phylogeny that includes vertical transmission and horizontal host-switches. This model allows estimating the number of host-switches and testing for strict vertical transmission and independent evolution. We test our approach using simulations. Finally, we illustrate our framework on gut microbiota high-throughput sequencing data of the family Hominidae and identify several microbial taxonomic units, including fibrolytic bacteria involved in carbohydrate digestion, that tend to be vertically transmitted. This article is protected by copyright. All rights reserved.

RevDate: 2019-07-17

Boscaro V, Husnik F, Vannini C, et al (2019)

Symbionts of the ciliate Euplotes: diversity, patterns and potential as models for bacteria-eukaryote endosymbioses.

Proceedings. Biological sciences, 286(1907):20190693.

Endosymbioses between bacteria and eukaryotes are enormously important in ecology and evolution, and as such are intensely studied. Despite this, the range of investigated hosts is narrow in the context of the whole eukaryotic tree of life: most of the information pertains to animal hosts, while most of the diversity is found in unicellular protists. A prominent case study is the ciliate Euplotes, which has repeatedly taken up the bacterium Polynucleobacter from the environment, triggering its transformation into obligate endosymbiont. This multiple origin makes the relationship an excellent model to understand recent symbioses, but Euplotes may host bacteria other than Polynucleobacter, and a more detailed knowledge of these additional interactions is needed in order to correctly interpret the system. Here, we present the first systematic survey of Euplotes endosymbionts, adopting a classical as well as a metagenomic approach, and review the state of knowledge. The emerging picture is indeed quite complex, with some Euplotes harbouring rich, stable prokaryotic communities not unlike those of multicellular animals. We provide insights into the distribution, evolution and diversity of these symbionts (including the establishment of six novel bacterial taxa), and outline differences and similarities with the most well-understood group of eukaryotic hosts: insects.

RevDate: 2019-07-17
CmpDate: 2019-07-17

Gavish M, L Veenman (2018)

Regulation of Mitochondrial, Cellular, and Organismal Functions by TSPO.

Advances in pharmacology (San Diego, Calif.), 82:103-136.

In 1999, the enigma of the 18kDa mitochondrial translocator protein (TSPO), also known as the peripheral-type benzodiazepine receptor, was the seeming disparity of the many functions attributed to TSPO, ranging from the potential of TSPO acting as a housekeeping gene at molecular biological levels to adaptations to stress, and even involvement in higher emotional and cognitive functioning, such as anxiety and depression. In the years since then, knowledge regarding the many functions modulated by TSPO has expanded, and understanding has deepened. In addition, new functions could be firmly associated with TSPO, such as regulation of programmed cell death and modulation of gene expression. Interestingly, control by the mitochondrial TSPO over both of these life and death functions appears to include Ca++ homeostasis, generation of reactive oxygen species (ROS), and ATP production. Other mitochondrial functions under TSPO control are considered to be steroidogenesis and tetrapyrrole metabolism. As TSPO effects on gene expression and on programmed cell death can be related to the wide range of functions that can be associated with TSPO, several of these five elements of Ca++, ROS, ATP, steroids, and tetrapyrroles may indeed form the basis of TSPO's capability to operate as a multifunctional housekeeping gene to maintain homeostasis of the cell and of the whole multicellular organism.

RevDate: 2019-07-17
CmpDate: 2019-07-17

McGrath C (2018)

Highlight: Origins of Multicellularity Revealed by Single-Celled Amoebae.

Genome biology and evolution, 10(2):705-706.

RevDate: 2019-07-14

Newman SA (2019)

Inherency and homomorphy in the evolution of development.

Current opinion in genetics & development, 57:1-8 pii:S0959-437X(18)30148-5 [Epub ahead of print].

Organismal development occurs when expression of certain genes leads to the mobilization of physical forces and effects that shape and pattern multicellular clusters. All materials exhibit preferred forms, but the inherent morphological motifs of some, such as liquids and crystalline solids are well-characterized. Recent work has shown that the origin of the animals (Metazoa) was accompanied by the acquisition by their developing tissues of liquid-like and liquid-crystalline properties. This and the novel capacity to produce stiff internal substrata (basal laminae) set these organisms apart from their closest relatives by the propensity (predictable from their material nature) to form complex bodies and organs. Once functional forms became established, however, they were susceptible to further genetic change as well as partial or full supplanting of original physical determinants by different ones. This results in the increasingly recognized phenomenon of homomorphy, the presence of the same structure in descendent organisms, brought about by transformed developmental mechanisms.

RevDate: 2019-07-12

Joukov V, A De Nicolo (2019)

The Centrosome and the Primary Cilium: The Yin and Yang of a Hybrid Organelle.

Cells, 8(7): pii:cells8070701.

Centrosomes and primary cilia are usually considered as distinct organelles, although both are assembled with the same evolutionary conserved, microtubule-based templates, the centrioles. Centrosomes serve as major microtubule- and actin cytoskeleton-organizing centers and are involved in a variety of intracellular processes, whereas primary cilia receive and transduce environmental signals to elicit cellular and organismal responses. Understanding the functional relationship between centrosomes and primary cilia is important because defects in both structures have been implicated in various diseases, including cancer. Here, we discuss evidence that the animal centrosome evolved, with the transition to complex multicellularity, as a hybrid organelle comprised of the two distinct, but intertwined, structural-functional modules: the centriole/primary cilium module and the pericentriolar material/centrosome module. The evolution of the former module may have been caused by the expanding cellular diversification and intercommunication, whereas that of the latter module may have been driven by the increasing complexity of mitosis and the requirement for maintaining cell polarity, individuation, and adhesion. Through its unique ability to serve both as a plasma membrane-associated primary cilium organizer and a juxtanuclear microtubule-organizing center, the animal centrosome has become an ideal integrator of extracellular and intracellular signals with the cytoskeleton and a switch between the non-cell autonomous and the cell-autonomous signaling modes. In light of this hypothesis, we discuss centrosome dynamics during cell proliferation, migration, and differentiation and propose a model of centrosome-driven microtubule assembly in mitotic and interphase cells. In addition, we outline the evolutionary benefits of the animal centrosome and highlight the hierarchy and modularity of the centrosome biogenesis networks.

RevDate: 2019-07-11

Yang YJ, Singh RP, Lan X, et al (2019)

Whole transcriptome analysis and gene deletion to understand the chloramphenicol resistance mechanism and develop a screening method for homologous recombination in Myxococcus xanthus.

Microbial cell factories, 18(1):123 pii:10.1186/s12934-019-1172-3.

BACKGROUND: Myxococcus xanthus DK1622 is a model system for studying multicellular development, predation, cellular differentiation, and evolution. Furthermore, it is a rich source of novel secondary metabolites and is widely used as heterologous expression host of exogenous biosynthetic gene clusters. For decades, genetic modification of M. xanthus DK1622 has mainly relied on kanamycin and tetracycline selection systems.

RESULTS: Here, we introduce an alternative selection system based on chloramphenicol (Cm) to broaden the spectrum of available molecular tools. A chloramphenicol-resistant growth phase and a chloramphenicol-susceptible growth phase before and after chloramphenicol-induction were prepared, and later sequenced to identify specific genes related to chloramphenicol-repercussion and drug-resistance. A total of 481 differentially expressed genes were revealed in chloramphenicol-resistant Cm5_36h and 1920 differentially expressed genes in chloramphenicol-dormant Cm_8h. Moreover, the gene expression profile in the chloramphenicol-dormant strain Cm_8h was quite different from that of Cm5_36 which had completely adapted to Cm, and 1513 differentially expression genes were identified between these two phenotypes. Besides upregulated acetyltransferases, several transporter encoding genes, including ABC transporters, major facilitator superfamily transporters (MFS), resistance-nodulation-cell division (RND) super family transporters and multidrug and toxic compound extrusion family transporters (MATE) were found to be involved in Cm resistance. After the knockout of the most highly upregulated MXAN_2566 MFS family gene, mutant strain DK-2566 was proved to be sensitive to Cm by measuring the growth curve in the Cm-added condition. A plasmid with a Cm resistance marker was constructed and integrated into chromosomes via homologous recombination and Cm screening. The integration efficiency was about 20% at different concentrations of Cm.

CONCLUSIONS: This study provides a new antibiotic-based selection system, and will help to understand antibiotic resistance mechanisms in M. xanthus DK1622.

RevDate: 2019-07-09

Rezaei-Lotfi S, Hunter N, RM Farahani (2019)

Coupled cycling programs multicellular self-organization of neural progenitors.

Cell cycle (Georgetown, Tex.) [Epub ahead of print].

Self-organization is central to the morphogenesis of multicellular organisms. However, the molecular platform that coordinates the robust emergence of complex morphological patterns from local interactions between cells remains unresolved. Here we demonstrate that neural self- organization is driven by coupled cycling of progenitor cells. In a coupled cycling mode, intercellular contacts relay extrinsic cues to override the intrinsic cycling rhythm of an individual cell and synchronize the population. The stringency of coupling and hence the synchronicity of the population is programmed by recruitment of a key coupler, β-catenin, into junctional complexes. As such, multicellular self-organization is driven by the same basic mathematical principle that governs synchronized behavior of macro-scale biological systems as diverse as the synchronized chirping of crickets, flashing of fireflies and schooling of fish; that is synchronization by coupling. It is proposed that coupled cycling foreshadows a fundamental adaptive change that facilitated evolution and diversification of multicellular life forms.

RevDate: 2019-07-09

Staps M, van Gestel J, CE Tarnita (2019)

Emergence of diverse life cycles and life histories at the origin of multicellularity.

Nature ecology & evolution pii:10.1038/s41559-019-0940-0 [Epub ahead of print].

The evolution of multicellularity has given rise to a remarkable diversity of multicellular life cycles and life histories. Whereas some multicellular organisms are long-lived, grow through cell division, and repeatedly release single-celled propagules (for example, animals), others are short-lived, form by aggregation, and propagate only once, by generating large numbers of solitary cells (for example, cellular slime moulds). There are no systematic studies that explore how diverse multicellular life cycles can come about. Here, we focus on the origin of multicellularity and develop a mechanistic model to examine the primitive life cycles that emerge from a unicellular ancestor when an ancestral gene is co-opted for cell adhesion. Diverse life cycles readily emerge, depending on ecological conditions, group-forming mechanism, and ancestral constraints. Among these life cycles, we recapitulate both extremes of long-lived groups that propagate continuously and short-lived groups that propagate only once, with the latter type of life cycle being particularly favoured when groups can form by aggregation. Our results show how diverse life cycles and life histories can easily emerge at the origin of multicellularity, shaped by ancestral constraints and ecological conditions. Beyond multicellularity, this finding has similar implications for other major transitions, such as the evolution of sociality.

RevDate: 2019-07-03

Etxebeste O, Otamendi A, Garzia A, et al (2019)

Rewiring of transcriptional networks as a major event leading to the diversity of asexual multicellularity in fungi.

Critical reviews in microbiology [Epub ahead of print].

Complex multicellularity (CM) is characterized by the generation of three-dimensional structures that follow a genetically controlled program. CM emerged at least five times in evolution, one of them in fungi. There are two types of CM programs in fungi, leading, respectively, to the formation of sexual or asexual spores. Asexual spores foment the spread of mycoses, as they are the main vehicle for dispersion. In spite of this key dependence, there is great morphological diversity of asexual multicellular structures in fungi. To advance the understanding of the mechanisms that control initiation and progression of asexual CM and how they can lead to such a remarkable morphological diversification, we studied 503 fungal proteomes, representing all phyla and subphyla, and most known classes. Conservation analyses of 33 regulators of asexual development suggest stepwise emergence of transcription factors. While velvet proteins constitute one of the most ancient systems, the central regulator BrlA emerged late in evolution (with the class Eurotiomycetes). Some factors, such as MoConX4, seem to be species-specific. These observations suggest that the emergence and evolution of transcriptional regulators rewire transcriptional networks. This process could reach the species level, resulting in a vast diversity of morphologies.

RevDate: 2019-06-29

Falz AL, SJ Müller-Schüssele (2019)

Physcomitrella as a model system for plant cell biology and organelle-organelle communication.

Current opinion in plant biology, 52:7-13 pii:S1369-5266(18)30178-X [Epub ahead of print].

In multicellular eukaryotic cells, metabolism and growth are sustained by the cooperative functioning of organelles in combination with cell-to-cell communication at the organism level. In land plants, multiple strategies have evolved to adapt to life outside water. As basal land plant, the moss Physcomitrella patens is used for comparative genomics, allowing to study lineage-specific features, as well as to track the evolution of fundamental parameters of plant cell organisation and physiology. P. patens is a versatile model for cell biology research, especially to investigate adaptive growth, stress biology as well as organelle dynamics and interactions. Recent advances include the use of genetically encoded biosensors for in vivo imaging of physiological parameters.

RevDate: 2019-06-27

Aufrecht JA, Fowlkes JD, Bible AN, et al (2019)

Pore-scale hydrodynamics influence the spatial evolution of bacterial biofilms in a microfluidic porous network.

PloS one, 14(6):e0218316 pii:PONE-D-18-34329.

Bacteria occupy heterogeneous environments, attaching and growing within pores in materials, living hosts, and matrices like soil. Systems that permit high-resolution visualization of dynamic bacterial processes within the physical confines of a realistic and tractable porous media environment are rare. Here we use microfluidics to replicate the grain shape and packing density of natural sands in a 2D platform to study the flow-induced spatial evolution of bacterial biofilms underground. We discover that initial bacterial dispersal and grain attachment is influenced by bacterial transport across pore space velocity gradients, a phenomenon otherwise known as rheotaxis. We find that gravity-driven flow conditions activate different bacterial cell-clustering phenotypes depending on the strain's ability to product extracellular polymeric substances (EPS). A wildtype, biofilm-producing bacteria formed compact, multicellular patches while an EPS-defective mutant displayed a linked-cell phenotype in the presence of flow. These phenotypes subsequently influenced the overall spatial distribution of cells across the porous media network as colonies grew and altered the fluid dynamics of their microenvironment.

RevDate: 2019-06-26

Ågren JA, Davies NG, KR Foster (2019)

Enforcement is central to the evolution of cooperation.

Nature ecology & evolution pii:10.1038/s41559-019-0907-1 [Epub ahead of print].

Cooperation occurs at all levels of life, from genomes, complex cells and multicellular organisms to societies and mutualisms between species. A major question for evolutionary biology is what these diverse systems have in common. Here, we review the full breadth of cooperative systems and find that they frequently rely on enforcement mechanisms that suppress selfish behaviour. We discuss many examples, including the suppression of transposable elements, uniparental inheritance of mitochondria and plastids, anti-cancer mechanisms, reciprocation and punishment in humans and other vertebrates, policing in eusocial insects and partner choice in mutualisms between species. To address a lack of accompanying theory, we develop a series of evolutionary models that show that the enforcement of cooperation is widely predicted. We argue that enforcement is an underappreciated, and often critical, ingredient for cooperation across all scales of biological organization.

RevDate: 2019-06-25

Robu A, Mironov V, A Neagu (2019)

Using Sacrificial Cell Spheroids for the Bioprinting of Perfusable 3D Tissue and Organ Constructs: A Computational Study.

Computational and mathematical methods in medicine, 2019:7853586.

A long-standing problem in tissue engineering is the biofabrication of perfusable tissue constructs that can be readily connected to the patient's vasculature. It was partially solved by three-dimensional (3D) printing of sacrificial material (e.g., hydrogel) strands: upon incorporation in another cell-laden hydrogel, the strands were removed, leaving behind perfusable channels. Their complexity, however, did not match that of the native vasculature. Here, we propose to use multicellular spheroids as a sacrificial material and investigate their potential benefits in the context of 3D bioprinting of cell aggregates and/or cell-laden hydrogels. Our study is based on computer simulations of postprinting cellular rearrangements. The computational model of the biological system is built on a cubic lattice, whereas its evolution is simulated using the Metropolis Monte Carlo algorithm. The simulations describe structural changes in three types of tissue constructs: a tube made of a single cell type, a tube made of two cell types, and a cell-laden hydrogel slab that incorporates a branching tube. In all three constructs, the lumen is obtained after the elimination of the sacrificial cell population. Our study suggests that sacrificial cell spheroids (sacrospheres) enable one to print tissue constructs outfitted with a finer and more complex network of channels than the ones obtained so far. Moreover, cellular interactions might give rise to a tissue microarchitecture that lies beyond the bioprinter's resolution. Although more expensive than inert materials, sacrificial cells have the potential to bring further progress towards the biofabrication of fully vascularized tissue substitutes.

RevDate: 2019-06-22

Tian L, Zhang B, Zhang J, et al (2019)

A magnetic compass guides the direction of foraging in a bat.

Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology pii:10.1007/s00359-019-01353-1 [Epub ahead of print].

Previously, two studies have provided evidence that bats can use magnetic field cues for homing or roosting. For insectivorous bats, it is well established that foraging represents one of the most fundamental behaviors in animals relies on their ability to echolocate. Whether echolocating bats can also use magnetic cues during foraging remains unknown, however. Here, we tested the orientation behavior of Chinese noctules (Nyctalus plancyi) during foraging in a plus-shaped, 4-channel apparatus under different magnetic field conditions. To minimize the effects of spatial memory on orientation from repeated experiments, naïve bats were tested only once in each experimental condition. As expected, under geomagnetic field and a food resource offered conditions, the bats significantly preferred to enter the channel containing food, indicating that they primarily relied on direct sensory signals unrelated to magnetic cues. In contrast, when we offered food simultaneously in all four channels and minimized any differences in all other sensory signals available, the bats exhibited a clear directional preference to forage along the magnetic field direction under either geomagnetic field or a magnetic field in which the horizontal component was rotated by 90°. Our study offers a novel evidence for the importance of a geomagnetic field during foraging.

RevDate: 2019-06-19

Muras V, Toulouse C, Fritz G, et al (2019)

Respiratory Membrane Protein Complexes Convert Chemical Energy.

Sub-cellular biochemistry, 92:301-335.

The invention of a biological membrane which is used as energy storage system to drive the metabolism of a primordial, unicellular organism represents a key event in the evolution of life. The innovative, underlying principle of this key event is respiration. In respiration, a lipid bilayer with insulating properties is chosen as the site for catalysis of an exergonic redox reaction converting substrates offered from the environment, using the liberated Gibbs free energy (ΔG) for the build-up of an electrochemical H+ (proton motive force, PMF) or Na+ gradient (sodium motive force, SMF) across the lipid bilayer. Very frequently , several redox reactions are performed in a consecutive manner, with the first reaction delivering a product which is used as substrate for the second redox reaction, resulting in a respiratory chain. From today's perspective, the (mostly) unicellular bacteria and archaea seem to be much simpler and less evolved when compared to multicellular eukaryotes. However, they are overwhelmingly complex with regard to the various respiratory chains which permit survival in very different habitats of our planet, utilizing a plethora of substances to drive metabolism. This includes nitrogen, sulfur and carbon compounds which are oxidized or reduced by specialized, respiratory enzymes of bacteria and archaea which lie at the heart of the geochemical N, S and C-cycles. This chapter gives an overview of general principles of microbial respiration considering thermodynamic aspects, chemical reactions and kinetic restraints. The respiratory chains of Escherichia coli and Vibrio cholerae are discussed as models for PMF- versus SMF-generating processes, respectively. We introduce main redox cofactors of microbial respiratory enzymes, and the concept of intra-and interelectron transfer. Since oxygen is an electron acceptor used by many respiratory chains, the formation and removal of toxic oxygen radicals is described. Promising directions of future research are respiratory enzymes as novel bacterial targets, and biotechnological applications relying on respiratory complexes.

RevDate: 2019-06-18

Bonner JT (2019)

The evolution of evolution.

Journal of experimental zoology. Part B, Molecular and developmental evolution [Epub ahead of print].

In the past, most biologists, myself included, did not think of evolution as changing over time. The wonders of natural selection were always at hand and went into operation once there was life. However, with a little reflection it becomes obvious that evolution has changed-there has been an evolution of evolution. Evolution can be separated into four phases, or eras, that may or may not overlap. The first era starts with the evolution of life on earth, which led to single cells that multiply asexually. The second era takes advantage of the invention of sexual reproduction as evolution could now gallop forward because of a richer fare of diverse offspring for natural selection. The third era begins with the introduction of multicellularity. In the fourth era there is a radical innovation: the nervous system that arises animals by standard Darwinian selection. This has allowed major rapid changes to proceed, such as language that led to all the rapid progress we call civilization; a true revolution, and one that does not depend on the slow genetic changes of all other standard gene-controlled evolutionary steps.

RevDate: 2019-06-18
CmpDate: 2019-06-18

Belato FA, Schrago CG, Coates CJ, et al (2019)

Newly Discovered Occurrences and Gene Tree of the Extracellular Globins and Linker Chains from the Giant Hexagonal Bilayer Hemoglobin in Metazoans.

Genome biology and evolution, 11(3):597-612.

Multicellular organisms depend on oxygen-carrying proteins to transport oxygen throughout the body; therefore, proteins such as hemoglobins (Hbs), hemocyanins, and hemerythrins are essential for maintenance of tissues and cellular respiration. Vertebrate Hbs are among the most extensively studied proteins; however, much less is known about invertebrate Hbs. Recent studies of hemocyanins and hemerythrins have demonstrated that they have much wider distributions than previously thought, suggesting that oxygen-binding protein diversity is underestimated across metazoans. Hexagonal bilayer hemoglobin (HBL-Hb), a blood pigment found exclusively in annelids, is a polymer comprised up to 144 extracellular globins and 36 linker chains. To further understand the evolutionary history of this protein complex, we explored the diversity of linkers and extracellular globins from HBL-Hbs using in silico approaches on 319 metazoan and one choanoflagellate transcriptomes. We found 559 extracellular globin and 414 linker genes transcribed in 171 species from ten animal phyla with new records in Echinodermata, Hemichordata, Brachiopoda, Mollusca, Nemertea, Bryozoa, Phoronida, Platyhelminthes, and Priapulida. Contrary to previous suggestions that linkers and extracellular globins emerged in the annelid ancestor, our findings indicate that they have putatively emerged before the protostome-deuterostome split. For the first time, we unveiled the comprehensive evolutionary history of metazoan HBL-Hb components, which consists of multiple episodes of gene gains and losses. Moreover, because our study design surveyed linkers and extracellular globins independently, we were able to cross-validate our results, significantly reducing the rate of false positives. We confirmed that the distribution of HBL-Hb components has until now been underestimated among animals.

RevDate: 2019-06-14

Pirkmajer S, AV Chibalin (2019)

Hormonal regulation of Na+-K+-ATPase from the evolutionary perspective.

Current topics in membranes, 83:315-351.

Na+-K+-ATPase, an α/β heterodimer, is an ancient enzyme that maintains Na+ and K+ gradients, thus preserving cellular ion homeostasis. In multicellular organisms, this basic housekeeping function is integrated to fulfill the needs of specialized organs and preserve whole-body homeostasis. In vertebrates, Na+-K+-ATPase is essential for many fundamental physiological processes, such as nerve conduction, muscle contraction, nutrient absorption, and urine excretion. During vertebrate evolution, three key developments contributed to diversification and integration of Na+-K+-ATPase functions. Generation of novel α- and β-subunits led to formation of multiple Na+-K+-ATPase isoenyzmes with distinct functional characteristics. Development of a complex endocrine system enabled efficient coordination of diverse Na+-K+-ATPase functions. Emergence of FXYDs, small transmembrane proteins that regulate Na+-K+-ATPase, opened new ways to modulate its function. FXYDs are a vertebrate innovation and an important site of hormonal action, suggesting they played an especially prominent role in evolving interaction between Na+-K+-ATPase and the endocrine system in vertebrates.

RevDate: 2019-06-13

Sogabe S, Hatleberg WL, Kocot KM, et al (2019)

Pluripotency and the origin of animal multicellularity.

Nature pii:10.1038/s41586-019-1290-4 [Epub ahead of print].

A widely held-but rarely tested-hypothesis for the origin of animals is that they evolved from a unicellular ancestor, with an apical cilium surrounded by a microvillar collar, that structurally resembled modern sponge choanocytes and choanoflagellates1-4. Here we test this view of animal origins by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types-choanocytes, pluripotent mesenchymal archaeocytes and epithelial pinacocytes-with choanoflagellates and other unicellular holozoans. Unexpectedly, we find that the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or sponges alone. By contrast, pluripotent archaeocytes upregulate genes that control cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two unicellular holozoans, including a colonial choanoflagellate. Choanocytes in the sponge Amphimedon queenslandica exist in a transient metastable state and readily transdifferentiate into archaeocytes, which can differentiate into a range of other cell types. These sponge cell-type conversions are similar to the temporal cell-state changes that occur in unicellular holozoans5. Together, these analyses argue against homology of sponge choanocytes and choanoflagellates, and the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells.

RevDate: 2019-06-12

Qian XX, Santini CL, Kosta A, et al (2019)

Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes.

Environmental microbiology [Epub ahead of print].

Multicellular magnetotactic prokaryotes (MMPs) exhibit peculiar coordination of swimming along geomagnetic field lines. Approximate 40-80 cells assemble, with a helical geometry or axisymmetry, into spherical or ellipsoidal MMPs, respectively. To contribute to a comprehensive understanding of bacterial multicellularity here we took multiple microscopic approaches to study the diversity, assembly, reproduction and motility of ellipsoidal MMPs. Using correlative fluorescence in situ hybridization and scanning electron microscopy analysis, we found an unexpected diversity in populations of ellipsoidal MMPs in the Mediterranean Sea. The high-pressure freezing/freeze substitution fixation technique allowed us to show, for the first time, that cells adhere via juxtaposed membranes and are held together by a rimming lattice. Fluorescence confocal microscopy and ultra-thin section images revealed not only the one-layer hollow three-dimensional architecture, but also periphery-core unilateral constriction of constituent cells and unidirectional binary fission of the ellipsoidal MMPs. This finding suggests the evolution toward MMPs multicellularity via the mechanism of incomplete separation of offspring. Remarkably, thousands of flagellar at the periphery surface of cells underpin the coordinated swimming of MMPs in response to mechanical, chemical, magnetic and optical stimuli, including a magnetotactic photokinesis behavior. Together these results unveil the unique structure and function property of ellipsoidal MMPs. This article is protected by copyright. All rights reserved.

RevDate: 2019-06-12

Yamashita S, H Nozaki (2019)

Embryogenesis of flattened colonies implies the innovation required for the evolution of spheroidal colonies in volvocine green algae.

BMC evolutionary biology, 19(1):120 pii:10.1186/s12862-019-1452-x.

BACKGROUND: Volvocine algae provide a suitable model for investigation of the evolution of multicellular organisms. Within this group, evolution of the body plan from flattened to spheroidal colonies is thought to have occurred independently in two different lineages, Volvocaceae and Astrephomene. Volvocacean species undergo inversion to form a spheroidal cell layer following successive cell divisions during embryogenesis. During inversion, the daughter protoplasts change their shape and develop acute chloroplast ends (opposite to basal bodies). By contrast, Astrephomene does not undergo inversion; rather, its daughter protoplasts rotate during successive cell divisions to form a spheroidal colony. However, the evolutionary pathways of these cellular events involved in the two tactics for formation of spheroidal colony are unclear, since the embryogenesis of extant volvocine genera with ancestral flattened colonies, such as Gonium and Tetrabaena, has not previously been investigated in detail.

RESULTS: We conducted time-lapse imaging by light microscopy and indirect immunofluorescence microscopy with staining of basal bodies, nuclei, and microtubules to observe embryogenesis in G. pectorale and T. socialis, which form 16-celled or 4-celled flattened colonies, respectively. In G. pectorale, a cup-shaped cell layer of the 16-celled embryo underwent gradual expansion after successive cell divisions, with the apical ends (position of basal bodies) of the square embryo's peripheral protoplasts separated from each other. In T. socialis, on the other hand, there was no apparent expansion of the daughter protoplasts in 4-celled embryos after successive cell divisions, however the two pairs of diagonally opposed daughter protoplasts shifted slightly and flattened after hatching. Neither of these two species exhibited rotation of daughter protoplasts during successive cell divisions as in Astrephomene or the formation of acute chloroplast ends of daughter protoplasts as in volvocacean inversion.

CONCLUSIONS: The present results indicate that the ancestor of Astrephomene might have newly acquired the rotation of daughter protoplasts after it diverged from the ancestor of Gonium, while the ancestor of Volvocaceae might have newly acquired the formation of acute chloroplast ends to complete inversion after divergence from the ancestor of Goniaceae (Gonium and Astrephomene).

RevDate: 2019-06-11

Roy M, SD Finley (2019)

Metabolic reprogramming dynamics in tumor spheroids: Insights from a multicellular, multiscale model.

PLoS computational biology, 15(6):e1007053 pii:PCOMPBIOL-D-18-01871 [Epub ahead of print].

Mathematical modeling provides the predictive ability to understand the metabolic reprogramming and complex pathways that mediate cancer cells' proliferation. We present a mathematical model using a multiscale, multicellular approach to simulate avascular tumor growth, applied to pancreatic cancer. The model spans three distinct spatial and temporal scales. At the extracellular level, reaction diffusion equations describe nutrient concentrations over a span of seconds. At the cellular level, a lattice-based energy driven stochastic approach describes cellular phenomena including adhesion, proliferation, viability and cell state transitions, occurring on the timescale of hours. At the sub-cellular level, we incorporate a detailed kinetic model of intracellular metabolite dynamics on the timescale of minutes, which enables the cells to uptake and excrete metabolites and use the metabolites to generate energy and building blocks for cell growth. This is a particularly novel aspect of the model. Certain defined criteria for the concentrations of intracellular metabolites lead to cancer cell growth, proliferation or death. Overall, we model the evolution of the tumor in both time and space. Starting with a cluster of tumor cells, the model produces an avascular tumor that quantitatively and qualitatively mimics experimental measurements of multicellular tumor spheroids. Through our model simulations, we can investigate the response of individual intracellular species under a metabolic perturbation and investigate how that response contributes to the response of the tumor as a whole. The predicted response of intracellular metabolites under various targeted strategies are difficult to resolve with experimental techniques. Thus, the model can give novel predictions as to the response of the tumor as a whole, identifies potential therapies to impede tumor growth, and predicts the effects of those therapeutic strategies. In particular, the model provides quantitative insight into the dynamic reprogramming of tumor cells at the intracellular level in response to specific metabolic perturbations. Overall, the model is a useful framework to study targeted metabolic strategies for inhibiting tumor growth.

RevDate: 2019-06-11

Chaplain MAJ, Lorenzi T, FR Macfarlane (2019)

Bridging the gap between individual-based and continuum models of growing cell populations.

Journal of mathematical biology pii:10.1007/s00285-019-01391-y [Epub ahead of print].

Continuum models for the spatial dynamics of growing cell populations have been widely used to investigate the mechanisms underpinning tissue development and tumour invasion. These models consist of nonlinear partial differential equations that describe the evolution of cellular densities in response to pressure gradients generated by population growth. Little prior work has explored the relation between such continuum models and related single-cell-based models. We present here a simple stochastic individual-based model for the spatial dynamics of multicellular systems whereby cells undergo pressure-driven movement and pressure-dependent proliferation. We show that nonlinear partial differential equations commonly used to model the spatial dynamics of growing cell populations can be formally derived from the branching random walk that underlies our discrete model. Moreover, we carry out a systematic comparison between the individual-based model and its continuum counterparts, both in the case of one single cell population and in the case of multiple cell populations with different biophysical properties. The outcomes of our comparative study demonstrate that the results of computational simulations of the individual-based model faithfully mirror the qualitative and quantitative properties of the solutions to the corresponding nonlinear partial differential equations. Ultimately, these results illustrate how the simple rules governing the dynamics of single cells in our individual-based model can lead to the emergence of complex spatial patterns of population growth observed in continuum models.

RevDate: 2019-06-08

Kees ED, Pendleton AR, Paquete CM, et al (2019)

On the Cost and Role of Secreted Flavin Cofactors for Anaerobic Respiration of Fumarate and Urocanate by Shewanella oneidensis.

Applied and environmental microbiology pii:AEM.00852-19 [Epub ahead of print].

Shewanella oneidensis strain MR-1, a facultative anaerobe and model organism for dissimilatory metal reduction, uses a periplasmic flavocytochrome, FccA, as both a terminal fumarate reductase and as a periplasmic electron transfer hub for extracellular respiration of a variety of substrates. It is currently unclear how maturation of FccA and other periplasmic flavoproteins is achieved, specifically in the context of flavin cofactor loading nor has the fitness cost of flavin secretion been quantified. We demonstrate that deletion of the inner membrane flavin adenine dinucleotide (FAD) exporter Bfe results in a 23% slower growth rate than wild-type during fumarate respiration, and an 80-90% loss in fumarate reductase activity. Exogenous flavin supplementation does not restore FccA activity in a Δbfe mutant unless the gene encoding the periplasmic FAD hydrolase UshA is also deleted. We demonstrate that the small Bfe-independent pool of FccA is sufficient for anaerobic growth with fumarate. Strains lacking Bfe were unable to grow using urocanate as the sole electron acceptor, which relies on the periplasmic flavoprotein UrdA. We show that periplasmic flavoprotein maturation occurs in careful balance with periplasmic FAD hydrolysis, and that the current model for periplasmic flavin cofactor loading must account for a Bfe-independent mechanism for flavin transport. Finally, we determine that the metabolic burden of flavin secretion is not significant during growth with flavin-independent anaerobic electron acceptors. Our work helps frame the physiological motivations that drove evolution of flavin secretion by ShewanellaImportanceShewanella species are prevalent in marine and aquatic environments, throughout stratified water columns, mineral rich sediments and in association with multicellular marine and aquatic organisms. The diversity of niches Shewanellae can occupy are due largely to their respiratory versatility. Shewanella oneidensis is a model organism for dissimilatory metal reduction and can respire a diverse array of organic and inorganic compounds including dissolved and solid metal oxides. The fumarate reductase FccA is a highly abundant multifunctional periplasmic protein that acts to bridge the periplasm and temporarily store electrons in a variety of respiratory nodes including metal, nitrate and dimethyl sulfoxide respiration. However, maturation of this central protein, particularly flavin cofactor acquisition, is poorly understood. Here we quantify the fitness cost of flavin secretion and describe how free flavins are acquired by FccA and a homologous periplasmic flavoprotein UrdA.

RevDate: 2019-06-07

St-Georges-Robillard A, Cahuzac M, Péant B, et al (2019)

Long-term fluorescence hyperspectral imaging of on-chip treated co-culture tumour spheroids to follow clonal evolution.

Integrative biology : quantitative biosciences from nano to macro pii:5512163 [Epub ahead of print].

Multicellular tumour spheroids are an ideal in vitro tumour model to study clonal heterogeneity and drug resistance in cancer research because different cell types can be mixed at will. However, measuring the individual response of each cell population over time is challenging: current methods are either destructive, such as flow cytometry, or cannot image throughout a spheroid, such as confocal microscopy. Our group previously developed a wide-field fluorescence hyperspectral imaging system to study spheroids formed and cultured in microfluidic chips. In the present study, two subclones of a single parental ovarian cancer cell line transfected to express different fluorophores were produced and co-culture spheroids were formed on-chip using ratios forming highly asymmetric subpopulations. We performed a 3D proliferation assay on each cell population forming the spheroids that matched the 2D growth behaviour. Response assays to PARP inhibitors and platinum-based drugs were also performed to follow the clonal evolution of mixed populations. Our experiments show that hyperspectral imaging can detect spheroid response before observing a decrease in spheroid diameter. Hyperspectral imaging and microfluidic-based spheroid assays provide a versatile solution to study clonal heterogeneity, able to measure response in subpopulations presenting as little as 10% of the initial spheroid.

RevDate: 2019-06-11

Rossy T, Nadell CD, A Persat (2019)

Cellular advective-diffusion drives the emergence of bacterial surface colonization patterns and heterogeneity.

Nature communications, 10(1):2471 pii:10.1038/s41467-019-10469-6.

Microorganisms navigate and divide on surfaces to form multicellular structures called biofilms, the most widespread survival strategy found in the bacterial world. One common assumption is that cellular components guide the spatial architecture and arrangement of multiple species in a biofilm. However, bacteria must contend with mechanical forces generated through contact with surfaces and under fluid flow, whose contributions to colonization patterns are poorly understood. Here, we show how the balance between motility and flow promotes the emergence of morphological patterns in Caulobacter crescentus biofilms. By modeling transport of single cells by flow and Brownian-like swimming, we show that the emergence of these patterns is guided by an effective Péclet number. By analogy with transport phenomena we show that, counter-intuitively, fluid flow represses mixing of distinct clonal lineages, thereby affecting the interaction landscapes between biofilm-dwelling bacteria. This demonstrates that hydrodynamics influence species interaction and evolution within surface-associated communities.

RevDate: 2019-06-06

Edgar JA (2019)

L-Ascorbic Acid and the Evolution of Multicellular Eukaryotes.

Journal of theoretical biology pii:S0022-5193(19)30228-0 [Epub ahead of print].

The lifeless earth was formed around 4.5 billion years ago and the first anaerobic unicellular "organisms" may have appeared half a billion years later. Despite subsequent prokaryotes (bacteria and archaea) evolving quite complex biochemistry and some eukaryote characteristics, the transition from unicellular prokaryotes to multicellular, aerobic eukaryotes took a further 2.5 billion years to begin. The key factor or factors that eventually caused this long-delayed transition is a question that has been a focus of considerable research and a topic of discussion over many years. On the basis of the extensive literature available and consideration of some of the characteristics that distinguish multicellular eukaryotes from prokaryotes, it is proposed that, as well as the development of oxygenic photosynthesis producing high levels of environmental oxygen and the formation of vital organelles such as aerobic adenosine triphosphate-generating mitochondria, the concurrent evolution of the L-ascorbic acid redox system should be considered as a key factor that led to the evolution of multicellular eukaryotes and it remains vitally involved in the maintenance of multicellularity and many other eukaryote characteristics.

RevDate: 2019-06-06

Thomas F, Madsen T, Giraudeau M, et al (2019)

Transmissible cancer and the evolution of sex.

PLoS biology, 17(6):e3000275 pii:PBIOLOGY-D-19-00513.

The origin and subsequent maintenance of sex and recombination are among the most elusive and controversial problems in evolutionary biology. Here, we propose a novel hypothesis, suggesting that sexual reproduction not only evolved to reduce the negative effects of the accumulation of deleterious mutations and processes associated with pathogen and/or parasite resistance but also to prevent invasion by transmissible selfish neoplastic cheater cells, henceforth referred to as transmissible cancer cells. Sexual reproduction permits systematic change of the multicellular organism's genotype and hence an enhanced detection of transmissible cancer cells by immune system. Given the omnipresence of oncogenic processes in multicellular organisms, together with the fact that transmissible cancer cells can have dramatic effects on their host fitness, our scenario suggests that the benefits of sex and concomitant recombination will be large and permanent, explaining why sexual reproduction is, despite its costs, the dominant mode of reproduction among eukaryotes.

RevDate: 2019-06-06

Siddiqui S, Singh A, Faizi N, et al (2019)

Cell cannibalism in oral cancer: A sign of aggressiveness, de-evolution, and retroversion of multicellularity.

Journal of cancer research and therapeutics, 15(3):631-637.

Background: According to Darwin's theory of evolution, complex creatures evolve from more simplistic ancestors. Dollo's law of irreversibility states that evolution is irreversible. However, cancer cells tend to follow anti-Dollo's law. Unfavorable conditions such as hypoxia, acidic pH and low nutrients cause the cancer cells to switch their lifestyle atavistically in order to survive. They start behaving like a unicellular organism. There is a switch from normal metabolism to Warburg effect and finally cannibalism. Cannibalism is a cell eating cell phenomenon. It is defined as a large cell enclosing a smaller one within its cytoplasm and is known by odd names such as "bird's eye cells" or "signet ring cells." Smaller tumor cells are found in the cytoplasm of larger tumor cells with crescent-shaped nucleus. Cannibalistic cells (CCs) are a feature of aggressive tumors. These cell types are vulnerable to metastasis.

Aim: The aim of this study is to identify CCs in various histological grades of oral squamous cell carcinoma (OSCC) and to relate them with the pattern of invasion, lymphocytic response (LR), and mitotic figures (Mfs). The purpose of the article is to establish it as a marker of aggressiveness and metastasis and as an evidence of de-evolution and retroversion of multicellularity.

Materials and Methods: Sixty-five histologically confirmed cases of OSCC were studied. Pattern of invasion, LR, number of CCs, and Mfs were recorded on 5 μ hematoxylin and eosin-stained tissue sections. ANOVA and t-test were applied; P < 0.05 was considered statistically significant.

Results: CCs were more in sections with patchy LR, increased Mfs, and grade IV pattern of invasion.

Conclusion: With increase in dedifferentiation, tumor cells start behaving like unicellular organisms with cell eating cell characteristics.

RevDate: 2019-06-04

Ostrowski EA (2019)

Enforcing Cooperation in the Social Amoebae.

Current biology : CB, 29(11):R474-R484.

Cooperation has been essential to the evolution of biological complexity, but many societies struggle to overcome internal conflicts and divisions. Dictyostelium discoideum, or the social amoeba, has been a useful model system for exploring these conflicts and how they can be resolved. When starved, these cells communicate, gather into groups, and build themselves into a multicellular fruiting body. Some cells altruistically die to form the rigid stalk, while the remainder sit atop the stalk, become spores, and disperse. Evolutionary theory predicts that conflict will arise over which cells die to form the stalk and which cells become spores and survive. The power of the social amoeba lies in the ability to explore how cooperation and conflict work across multiple levels, ranging from proximate mechanisms (how does it work?) to ultimate evolutionary answers (why does it work?). Recent studies point to solutions to the problem of ensuring fairness, such as the ability to suppress selfishness and to recognize and avoid unrelated individuals. This work confirms a central role for kin selection, but also suggests new explanations for how social amoebae might enforce cooperation. New approaches based on genomics are also enabling researchers to decipher for the first time the evolutionary history of cooperation and conflict and to determine its role in shaping the biology of multicellular organisms.

RevDate: 2019-06-04

Smith P, M Schuster (2019)

Public goods and cheating in microbes.

Current biology : CB, 29(11):R442-R447.

Communication and cooperation are not restricted to complex, higher organisms. Microbes, too, perform a variety of collective, multicellular behaviors, including biofilm formation, quorum sensing, nutrient acquisition, and dispersal. The products of these microbial cooperative behaviors are generally referred to as public goods. Here we describe the nature of microbial public goods, the associated problem of cheating, and ways in which microbes maintain public goods in the face of cheating. We highlight work in a growing field at the interface of microbiology, evolution, and ecology that combines multiple approaches in experimental evolution, genetics, and mathematical modeling.

RevDate: 2019-06-03

Russell SL, Chappell L, W Sullivan (2019)

A symbiont's guide to the germline.

Current topics in developmental biology, 135:315-351.

Microbial symbioses exhibit astounding adaptations, yet all symbionts face the problem of how to reliably associate with host offspring every generation. A common strategy is vertical transmission, in which symbionts are directly transmitted from the female to her offspring. The diversity of symbionts and vertical transmission mechanisms is as expansive as the diversity of eukaryotic host taxa that house them. However, there are several common themes among these mechanisms based on the degree to which symbionts associate with the host germline during transmission. In this review, we detail three distinct vertical transmission strategies, starting with associations that are transmitted from host somatic cells to offspring somatic cells, either due to lacking a germline or avoiding it. A second strategy involves somatically-localized symbionts that migrate into the germline during host development. The third strategy we discuss is one in which the symbiont maintains continuous association with the germline throughout development. Unexpectedly, the vast majority of documented vertically inherited symbionts rely on the second strategy: soma-to-germline migration. Given that not all eukaryotes contain a sequestered germline and instead produce offspring from somatic stem cell lineages, this soma-to-germline migration is discussed in the context of multicellular evolution. Lastly, as recent genomics data have revealed an abundance of horizontal gene transfer events from symbiotic and non-symbiotic bacteria to host genomes, we discuss their impact on eukaryotic host evolution.

RevDate: 2019-05-31

Moreno MA, C Ofria (2019)

Toward Open-Ended Fraternal Transitions in Individuality.

Artificial life, 25(2):117-133.

The emergence of new replicating entities from the union of simpler entities characterizes some of the most profound events in natural evolutionary history. Such transitions in individuality are essential to the evolution of the most complex forms of life. Thus, understanding these transitions is critical to building artificial systems capable of open-ended evolution. Alas, these transitions are challenging to induce or detect, even with computational organisms. Here, we introduce the DISHTINY (Distributed Hierarchical Transitions in Individuality) platform, which provides simple cell-like organisms with the ability and incentive to unite into new individuals in a manner that can continue to scale to subsequent transitions. The system is designed to encourage these transitions so that they can be studied: Organisms that coordinate spatiotemporally can maximize the rate of resource harvest, which is closely linked to their reproductive ability. We demonstrate the hierarchical emergence of multiple levels of individuality among simple cell-like organisms that evolve parameters for manually designed strategies. During evolution, we observe reproductive division of labor and close cooperation among cells, including resource-sharing, aggregation of resource endowments for propagules, and emergence of an apoptosis response to somatic mutation. Many replicate populations evolved to direct their resources toward low-level groups (behaving like multicellular individuals), and many others evolved to direct their resources toward high-level groups (acting as larger-scale multicellular individuals).

RevDate: 2019-05-30

Sweeney EG, Nishida A, Weston A, et al (2019)

Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture.

mSphere, 4(3): pii:4/3/e00285-19.

Bacteria are often found living in aggregated multicellular communities known as biofilms. Biofilms are three-dimensional structures that confer distinct physical and biological properties to the collective of cells living within them. We used agent-based modeling to explore whether local cellular interactions were sufficient to give rise to global structural features of biofilms. Specifically, we asked whether chemorepulsion from a self-produced quorum-sensing molecule, autoinducer-2 (AI-2), was sufficient to recapitulate biofilm growth and cellular organization observed for biofilms of Helicobacter pylori, a common bacterial resident of human stomachs. To carry out this modeling, we modified an existing platform, Individual-based Dynamics of Microbial Communities Simulator (iDynoMiCS), to incorporate three-dimensional chemotaxis, planktonic cells that could join or leave the biofilm structure, and cellular production of AI-2. We simulated biofilm growth of previously characterized H. pylori strains with various AI-2 production and sensing capacities. Using biologically plausible parameters, we were able to recapitulate both the variation in biofilm mass and cellular distributions observed with these strains. Specifically, the strains that were competent to chemotax away from AI-2 produced smaller and more heterogeneously spaced biofilms, whereas the AI-2 chemotaxis-defective strains produced larger and more homogeneously spaced biofilms. The model also provided new insights into the cellular demographics contributing to the biofilm patterning of each strain. Our analysis supports the idea that cellular interactions at small spatial and temporal scales are sufficient to give rise to larger-scale emergent properties of biofilms.IMPORTANCE Most bacteria exist in aggregated, three-dimensional structures called biofilms. Although biofilms play important ecological roles in natural and engineered settings, they can also pose societal problems, for example, when they grow in plumbing systems or on medical implants. Understanding the processes that promote the growth and disassembly of biofilms could lead to better strategies to manage these structures. We had previously shown that Helicobacter pylori bacteria are repulsed by high concentrations of a self-produced molecule, AI-2, and that H. pylori mutants deficient in AI-2 sensing form larger and more homogeneously spaced biofilms. Here, we used computer simulations of biofilm formation to show that local H. pylori behavior of repulsion from high AI-2 could explain the overall architecture of H. pylori biofilms. Our findings demonstrate that it is possible to change global biofilm organization by manipulating local cell behaviors, which suggests that simple strategies targeting cells at local scales could be useful for controlling biofilms in industrial and medical settings.

RevDate: 2019-06-10

Liu T, Wang X, Wang G, et al (2019)

Evolution of Complex Thallus Alga: Genome Sequencing of Saccharina japonica.

Frontiers in genetics, 10:378.

Saccharina, as one of the most important brown algae (Phaeophyceae) with multicellular thallus, has a very remarkable evolutionary history, and globally accounts for most of the economic marine aquaculture production worldwide. Here, we present the 580.5 million base pairs of genome sequence of Saccharina japonica, whose current assembly contains 35,725 protein-coding genes. In a comparative analysis with Ectocarpus siliculosus, the integrated virus sequence suggested the genome evolutionary footprints, which derived from their co-ancestry and experienced genomic arrangements. Furthermore, the gene expansion was found to be an important strategy for functional evolution, especially with regard to extracelluar components, stress-related genes, and vanadium-dependent haloperoxidases, and we proposed a hypothesis that gene duplication events were the main driving force for the evolution history from multicellular filamentous algae to thallus algae. The sequenced Saccharina genome paves the way for further molecular studies and is useful for genome-assisted breeding of S. japonica and other related algae species.

RevDate: 2019-05-23

Loron CC, François C, Rainbird RH, et al (2019)

Early fungi from the Proterozoic era in Arctic Canada.

Nature pii:10.1038/s41586-019-1217-0 [Epub ahead of print].

Fungi are crucial components of modern ecosystems. They may have had an important role in the colonization of land by eukaryotes, and in the appearance and success of land plants and metazoans1-3. Nevertheless, fossils that can unambiguously be identified as fungi are absent from the fossil record until the middle of the Palaeozoic era4,5. Here we show, using morphological, ultrastructural and spectroscopic analyses, that multicellular organic-walled microfossils preserved in shale of the Grassy Bay Formation (Shaler Supergroup, Arctic Canada), which dates to approximately 1,010-890 million years ago, have a fungal affinity. These microfossils are more than half a billion years older than previously reported unambiguous occurrences of fungi, a date which is consistent with data from molecular clocks for the emergence of this clade6,7. In extending the fossil record of the fungi, this finding also pushes back the minimum date for the appearance of eukaryotic crown group Opisthokonta, which comprises metazoans, fungi and their protist relatives8,9.

RevDate: 2019-05-22

Ballinger MJ, SJ Perlman (2019)

The defensive Spiroplasma.

Current opinion in insect science, 32:36-41.

Defensive microbes are of great interest for their roles in arthropod health, disease transmission, and biocontrol efforts. Obligate bacterial passengers of arthropods, such as Spiroplasma, confer protection against the natural enemies of their hosts to improve their own fitness. Although known for less than a decade, Spiroplasma's defensive reach extends to diverse parasites, both microbial and multicellular. We provide an overview of known defensive phenotypes against nematodes, parasitoid wasps, and fungi, and highlight recent studies supporting the role of Spiroplasma-encoded ribosome-inactivating proteins in protection. With cellular features well-suited for life in the hemolymph, broad distribution among invertebrate hosts, and the capacity to repeatedly evolve vertical transmission, Spiroplasma may be uniquely equipped to form intimate, defensive associations to combat extracellular parasites. Along with insights into defensive mechanisms, recent significant advances have been made in male-killing - a phenotype with interesting evolutionary ties to defense. Finally, we look forward to an exciting decade using the genetic tools of Drosophila, and the rapidly-advancing tractability of Spiroplasma itself, to better understand mechanisms and evolution in defensive symbiosis.

RevDate: 2019-06-10

Khan MAW, Stephens WZ, Mohammed AD, et al (2019)

Does MHC heterozygosity influence microbiota form and function?.

PloS one, 14(5):e0215946 pii:PONE-D-18-12229.

MHC molecules are essential for the adaptive immune response, and they are the most polymorphic genetic loci in vertebrates. Extreme genetic variation at these loci is paradoxical given their central importance to host health. Classic models of MHC gene evolution center on antagonistic host-pathogen interactions to promote gene diversification and allelic diversity in host populations. However, all multicellular organisms are persistently colonized by their microbiota that perform essential metabolic functions for their host and protect from infection. Here, we provide data to support the hypothesis that MHC heterozygote advantage (a main force of selection thought to drive MHC gene evolution), may operate by enhancing fitness advantages conferred by the host's microbiome. We utilized fecal 16S rRNA gene sequences and their predicted metagenome datasets collected from multiple MHC congenic homozygote and heterozygote mouse strains to describe the influence of MHC heterozygosity on microbiome form and function. We find that in contrast to homozygosity at MHC loci, MHC heterozygosity promotes functional diversification of the microbiome, enhances microbial network connectivity, and results in enrichment for a variety of microbial functions that are positively associated with host fitness. We demonstrate that taxonomic and functional diversity of the microbiome is positively correlated in MHC heterozygote but not homozygote animals, suggesting that heterozygote microbiomes are more functionally adaptive under similar environmental conditions than homozygote microbiomes. Our data complement previous observations on the role of MHC polymorphism in sculpting microbiota composition, but also provide functional insights into how MHC heterozygosity may enhance host health by modulating microbiome form and function. We also provide evidence to support that MHC heterozygosity limits functional redundancy among commensal microbes and may enhance the metabolic versatility of their microbiome. Results from our analyses yield multiple testable predictions regarding the role of MHC heterozygosity on the microbiome that will help guide future research in the area of MHC-microbiome interactions.

RevDate: 2019-05-15

Pichugin Y, Park HJ, A Traulsen (2019)

Evolution of simple multicellular life cycles in dynamic environments.

Journal of the Royal Society, Interface, 16(154):20190054.

The mode of reproduction is a critical characteristic of any species, as it has a strong effect on its evolution. As any other trait, the reproduction mode is subject to natural selection and may adapt to the environment. When the environment varies over time, different reproduction modes could be optimal at different times. The natural response to a dynamic environment seems to be bet hedging, where multiple reproductive strategies are stochastically executed. Here, we develop a framework for the evolution of simple multicellular life cycles in a dynamic environment. We use a matrix population model of undifferentiated multicellular groups undergoing fragmentation and ask which mode maximizes the population growth rate. Counterintuitively, we find that natural selection in dynamic environments generally tends to promote deterministic, not stochastic, reproduction modes.

RevDate: 2019-06-10

Gao Y, Traulsen A, Y Pichugin (2019)

Interacting cells driving the evolution of multicellular life cycles.

PLoS computational biology, 15(5):e1006987 pii:PCOMPBIOL-D-19-00097.

Evolution of complex multicellular life began from the emergence of a life cycle involving the formation of cell clusters. The opportunity for cells to interact within clusters provided them with an advantage over unicellular life forms. However, what kind of interactions may lead to the evolution of multicellular life cycles? Here, we combine evolutionary game theory with a model for the emergence of multicellular groups to investigate how cell interactions can influence reproduction modes during the early stages of the evolution of multicellularity. In our model, the presence of both cell types is maintained by stochastic phenotype switching during cell division. We identify evolutionary optimal life cycles as those which maximize the population growth rate. Among all interactions captured by two-player games, the vast majority promotes two classes of life cycles: (i) splitting into unicellular propagules or (ii) fragmentation into two offspring clusters of equal (or almost equal) size. Our findings indicate that the three most important characteristics, determining whether multicellular life cycles will evolve, are the average performance of homogeneous groups, heterogeneous groups, and solitary cells.

RevDate: 2019-05-20

Vinogradov AE, OV Anatskaya (2019)

Evolutionary framework of the human interactome: Unicellular and multicellular giant clusters.

Bio Systems, 181:82-87 pii:S0303-2647(19)30010-3 [Epub ahead of print].

The main contradiction of multicellularity (MCM) is between the unicellular (UC) and multicellular (MC) levels. In human interactome we revealed two giant clusters with MC and UC medians (and several smaller ones with MC medians). The enrichment of these clusters by phylostrata and by functions support the MC versus UC division. The total interactome and the giant clusters show a core-periphery evolutionary growth. From viewpoint of the MCM, the most important is the placement of genes, appearing at UC evolutionary stage, in the MC clusters. Thus, genes involved in vesicle-mediated transport, cell cycle, cellular responses to stress, post-translational modifications and many diseases appeared at UC evolutionary stage but are placed mostly in MC clusters. Genes downregulated with age are enriched in UC cluster, whereas the upregulated genes are preferentially placed in MC giant cluster. The tumor suppressor and pluripotency regulating pathways are also enriched in MC giant cluster. Therefore, this cluster probably operates as 'internal manager' constraining runaway unicellularity. The clusters have denser interactions within than between them, therefore they can serve as attractors (stable states of dynamic systems) of cellular programs. Importantly, the UC cluster have a higher inside/outside connection ratio compared with MC clusters, which suggests a stronger attractor effect and may explain why cells of MC organisms are prone to oncogenesis. The evolutionary clustering of human interactome elucidates the MC control over functions appearing at UC evolutionary stage and can build a framework for biosystems studies focusing on the interplay between UC and MC levels.

RevDate: 2019-05-12

Erkenbrack EM, JR Thompson (2019)

Cell type phylogenetics informs the evolutionary origin of echinoderm larval skeletogenic cell identity.

Communications biology, 2:160 pii:417.

The multiplicity of cell types comprising multicellular organisms begs the question as to how cell type identities evolve over time. Cell type phylogenetics informs this question by comparing gene expression of homologous cell types in distantly related taxa. We employ this approach to inform the identity of larval skeletogenic cells of echinoderms, a clade for which there are phylogenetically diverse datasets of spatial gene expression patterns. We determined ancestral spatial expression patterns of alx1, ets1, tbr, erg, and vegfr, key components of the skeletogenic gene regulatory network driving identity of the larval skeletogenic cell. Here we show ancestral state reconstructions of spatial gene expression of extant eleutherozoan echinoderms support homology and common ancestry of echinoderm larval skeletogenic cells. We propose larval skeletogenic cells arose in the stem lineage of eleutherozoans during a cell type duplication event that heterochronically activated adult skeletogenic cells in a topographically distinct tissue in early development.

RevDate: 2019-05-12

Wang P, Liang J, Shi LZ, et al (2018)

Visualizing Spatiotemporal Dynamics of Intercellular Mechanotransmission upon Wounding.

ACS photonics, 5(9):3565-3574.

During cell-to-cell communications, the interplay between physical and biochemical cues is essential for informational exchange and functional coordination, especially in multicellular organisms. However, it remains a challenge to visualize intercellular signaling dynamics in single live cells. Here, we report a photonic approach, based on laser microscissors and Förster resonance energy transfer (FRET) microscopy, to study intercellular signaling transmission. First, using our high-throughput screening platform, we developed a highly sensitive FRET-based biosensor (SCAGE) for Src kinase, a key regulator of intercellular interactions and signaling cascades. Notably, SCAGE showed a more than 40-fold sensitivity enhancement than the original biosensor in live mammalian cells. Next, upon local severance of physical intercellular connections by femtosecond laser pulses, SCAGE enabled the visualization of a transient Src activation across neighboring cells. Lastly, we found that this observed transient Src activation following the loss of cell-cell contacts depends on the passive structural support of cytoskeleton but not on the active actomyosin contractility. Hence, by precisely introducing local physical perturbations and directly visualizing spatiotemporal transmission of ensuing signaling events, our integrated approach could be broadly applied to mimic and investigate the wounding process at single-cell resolutions. This integrated approach with highly sensitive FRET-based biosensors provides a unique system to advance our in-depth understanding of molecular mechanisms underlying the physical-biochemical basis of intercellular coupling and wounding processes.

RevDate: 2019-05-07

Turan ZG, Parvizi P, Dönertaş HM, et al (2019)

Molecular footprint of Medawar's mutation accumulation process in mammalian aging.

Aging cell [Epub ahead of print].

Medawar's mutation accumulation hypothesis explains aging by the declining force of natural selection with age: Slightly deleterious germline mutations expressed in old age can drift to fixation and thereby lead to aging-related phenotypes. Although widely cited, empirical evidence for this hypothesis has remained limited. Here, we test one of its predictions that genes relatively highly expressed in old adults should be under weaker purifying selection than genes relatively highly expressed in young adults. Combining 66 transcriptome datasets (including 16 tissues from five mammalian species) with sequence conservation estimates across mammals, here we report that the overall conservation level of expressed genes is lower at old age compared to young adulthood. This age-related decrease in transcriptome conservation (ADICT) is systematically observed in diverse mammalian tissues, including the brain, liver, lung, and artery, but not in others, most notably in the muscle and heart. Where observed, ADICT is driven partly by poorly conserved genes being up-regulated during aging. In general, the more often a gene is found up-regulated with age among tissues and species, the lower its evolutionary conservation. Poorly conserved and up-regulated genes have overlapping functional properties that include responses to age-associated tissue damage, such as apoptosis and inflammation. Meanwhile, these genes do not appear to be under positive selection. Hence, genes contributing to old age phenotypes are found to harbor an excess of slightly deleterious alleles, at least in certain tissues. This supports the notion that genetic drift shapes aging in multicellular organisms, consistent with Medawar's mutation accumulation hypothesis.

RevDate: 2019-05-05

Singer D, Mitchell EAD, Payne RJ, et al (2019)

Dispersal limitations and historical factors determine the biogeography of specialized terrestrial protists.

Molecular ecology [Epub ahead of print].

Recent studies show that soil eukaryotic diversity is immense and dominated by microorganisms. However, it is unclear to what extent the processes that shape the distribution of diversity in plants and animals also apply to microorganisms. Major diversification events in multicellular organisms have often been attributed to long-term climatic and geological processes, but the impact of such processes on protist diversity has received much less attention as their distribution has often been believed to be largely cosmopolitan. Here, we quantified phylogeographic patterns in Hyalosphenia papilio, a large testate amoeba restricted to Holarctic Sphagnum-dominated peatlands, to test if the current distribution of its genetic diversity can be explained by historical factors or by the current distribution of suitable habitat. Phylogenetic diversity was higher in Western North America, corresponding to the inferred geographical origin of the H. papilio complex, and was lower in Eurasia despite extensive suitable habitat. These results suggest that patterns of phylogenetic diversity and distribution can be explained by the history of Holarctic Sphagnum peatland range expansions and contractions in response to Quaternary glaciations that promoted cladogenetic range evolution, rather than the contemporary distribution of suitable habitats. Species distributions were positively correlated with climatic niche breadth, suggesting that climatic tolerance is key to dispersal ability in H. papilio. This implies that, at least for large and specialized terrestrial microorganisms, propagule dispersal is slow enough that historical processes may contribute to their diversification and phylogeographic patterns and may partly explain their very high overall diversity. This article is protected by copyright. All rights reserved.

RevDate: 2019-05-04

Li J, Zhang H, Liu P, et al (2019)

Phylogenetic and structural identification of a novel magnetotactic Deltaproteobacterium strain WYHR-1 from a freshwater lake.

Applied and environmental microbiology pii:AEM.00731-19 [Epub ahead of print].

Magnetotactic bacteria (MTB) are phylogenetically diverse prokaryotes that are able to biomineralize intracellular, magnetic chains of magnetite or greigite nanocrystals called magnetosomes. Simultaneous characterization of MTB phylogeny and biomineralization is crucial but challenging because most MTB are extremely difficult to culture. We identify a large rod, bean-like MTB (tentatively named WYHR-1) from freshwater sediments of Weiyang Lake, Xi'an, China, using a coupled fluorescence and scanning electron microscopy approach at the single-cell scale. Phylogenetic analysis of 16S rRNA gene sequences indicates that WYHR-1 is a novel genus from the Deltaproteobacteria class. Transmission electron microscope observations reveal that WYHR-1 cells contain tens of magnetite magnetosomes that are organized into a single chain bundle along the cell long axis. Mature WYHR-1 magnetosomes are bullet-shaped, straight and elongated along the (001) direction, with a large flat end terminated by a {100} face at the base and a conical top. This crystal morphology is distinctively different from bullet-shaped magnetosomes produced by other MTB in the Deltaproteobacteria class and the Nitrospirae phylum. This indicates that WYHR-1 may have a different crystal growth process and mechanism from other species, which results from species-specific magnetosome biomineralization in MTB.IMPORTANCE Magnetotactic bacteria (MTB) are a model system for understanding biomineralization, and are also studied intensively in biogeomagnetic and paleomagnetic research. However, many uncultured MTB strains have not been identified phylogenetically or investigated structurally at the single-cell level, which limits comprehensive understanding of MTB diversity and their role in biomineralization. We have identified a novel MTB strain WYHR-1 from a freshwater lake using a coupled fluorescence and scanning electron microscopy approach at the single-cell scale. Our analyses further indicate that strain WYHR-1 represents a novel genus from the Deltaproteobacteria class. In contrast to bullet-shaped magnetosomes produced by other MTB in the Deltaproteobacteria class and the Nitrospirae phylum, WYHR-1 magnetosomes are bullet-shaped, straight, and highly elongated along the (001) direction, and are terminated by a large {100} face at their base and have a conical top. Our findings imply that, consistent with phylogenetic diversity of MTB, bullet-shaped magnetosomes have diverse crystal habits and growth patterns.

RevDate: 2019-05-02

Biscotti MA, Barucca M, Carducci F, et al (2019)

The p53 gene family in vertebrates: Evolutionary considerations.

Journal of experimental zoology. Part B, Molecular and developmental evolution [Epub ahead of print].

The origin of the p53 gene family predates multicellular life since TP53 members of this gene family have been found in unicellular eukaryotes. In invertebrates one or two genes attributable to a TP53-like or TP63/73-like gene are present. The radiation into three genes, TP53, TP63, and TP73, has been reported as a vertebrate invention. TP53 is considered the "guardian of the genome" given its role in protecting cells against the DNA damage and cellular stressors. TP63 and TP73 play a role in epithelial development and neurogenesis, respectively. The evolution of the p53 gene family has been the subject of considerable analyses even if several questions remain still open. In this study we addressed the evolutionary history of the p53 gene family in vertebrates performing an extended microsyntenic investigation coupled with a phylogenetic analysis, together with protein domain organization and structure assessment. On the basis of our results we discussed a possible evolutionary scenario according to which a TP53/63/73 ancestor form gave rise to the current TP53 and a TP63/73 form, which in turn independently duplicated into two genes in agnathe and gnathostome lineages.

RevDate: 2019-05-19

Salvi M, Morbiducci U, Amadeo F, et al (2019)

Automated Segmentation of Fluorescence Microscopy Images for 3D Cell Detection in human-derived Cardiospheres.

Scientific reports, 9(1):6644 pii:10.1038/s41598-019-43137-2.

The 'cardiosphere' is a 3D cluster of cardiac progenitor cells recapitulating a stem cell niche-like microenvironment with a potential for disease and regeneration modelling of the failing human myocardium. In this multicellular 3D context, it is extremely important to decrypt the spatial distribution of cell markers for dissecting the evolution of cellular phenotypes by direct quantification of fluorescent signals in confocal microscopy. In this study, we present a fully automated method, named CARE ('CARdiosphere Evaluation'), for the segmentation of membranes and cell nuclei in human-derived cardiospheres. The proposed method is tested on twenty 3D-stacks of cardiospheres, for a total of 1160 images. Automatic results are compared with manual annotations and two open-source software designed for fluorescence microscopy. CARE performance was excellent in cardiospheres membrane segmentation and, in cell nuclei detection, the algorithm achieved the same performance as two expert operators. To the best of our knowledge, CARE is the first fully automated algorithm for segmentation inside in vitro 3D cell spheroids, including cardiospheres. The proposed approach will provide, in the future, automated quantitative analysis of markers distribution within the cardiac niche-like environment, enabling predictive associations between cell mechanical stresses and dynamic phenotypic changes.

RevDate: 2019-04-30

Borisenko I, Podgornaya OI, AV Ereskovsky (2019)

From traveler to homebody: Which signaling mechanisms sponge larvae use to become adult sponges?.

Advances in protein chemistry and structural biology, 116:421-449.

Cell-to-cell signaling is responsible for regulation of many developmental processes such as proliferation, cell migration, survival, cell fate specification and axis patterning. In this article we discussed the role of signaling in the metamorphosis of sponges with a focus on epithelial-mesenchymal transition (EMT) accompanying this event. Sponges (Porifera) are an ancient lineage of morphologically simple animals occupying a basal position on the tree of life. The study of these animals is necessary for understanding the origin of multicellularity and the evolution of developmental processes. Development of sponges is quite diverse. It finishes with the metamorphosis of a free-swimming larva into a young settled sponge. The outer surface of sponge larvae consists of a ciliated epithelial sheath, which ensures locomotion, while their internal structure varies from genus to genus. The fate of larval ciliated cells is the most intriguing aspect of metamorphosis. In this review we discuss the fate of larval ciliated cells, the processes going on in cells during metamorphosis at the molecular level and the regulation of this process. The review is based on information about several sponge species with a focus on Halisarca dujardini, Sycon ciliatum and Amphimedon queenslandica. In our model sponge, H. dujardini, ciliated cells leave the larval epithelium during metamorphosis and migrate to the internal cell mass as amoeboid cells to be differentiated into choanocytes of the juvenile sponge. Ciliated cells undergo EMT and internalize within minutes. As EMT involves the disappearance of adherens junctions and as cadherin, the main adherens junction protein, was identified in the transcriptome of several sponges, we suppose that EMT is regulated through cadherin-containing adherens junctions between ciliated cells. We failed to identify the master genes of EMT in the H. dujardini transcriptome, possibly because transcription was absent in the sequenced stages. They may be revealed by a search in the genome. The master genes themselves are controlled by various signaling pathways. Sponges have all the six signaling pathways conserved in Metazoa: Wnt, TGF-beta, Hedgehog, Notch, FGF and NO-dependent pathways. Summarizing the new data about intercellular communication in sponges, we can put forward two main questions regarding metamorphosis: (1) Which of the signaling pathways and in what hierarchical order are involved in metamorphosis? (2) How is the organization of a young sponge related to that of the larva or, in other words, is there a heredity of axes between the larva and the adult sponge?

RevDate: 2019-05-01

Rivera-Yoshida N, Arzola AV, Arias Del Angel JA, et al (2019)

Plastic multicellular development of Myxococcus xanthus: genotype-environment interactions in a physical gradient.

Royal Society open science, 6(3):181730 pii:rsos181730.

In order to investigate the contribution of the physical environment to variation in multicellular development of Myxococcus xanthus, phenotypes developed by different genotypes in a gradient of substrate stiffness conditions were quantitatively characterized. Statistical analysis showed that plastic phenotypes result from the genotype, the substrate conditions and the interaction between them. Also, phenotypes were expressed in two distinguishable scales, the individual and the population levels, and the interaction with the environment showed scale and trait specificity. Overall, our results highlight the constructive role of the physical context in the development of microbial multicellularity, with both ecological and evolutionary implications.

RevDate: 2019-05-01

Hajheidari M, Koncz C, M Bucher (2019)

Chromatin Evolution-Key Innovations Underpinning Morphological Complexity.

Frontiers in plant science, 10:454.

The history of life consists of a series of major evolutionary transitions, including emergence and radiation of complex multicellular eukaryotes from unicellular ancestors. The cells of multicellular organisms, with few exceptions, contain the same genome, however, their organs are composed of a variety of cell types that differ in both structure and function. This variation is largely due to the transcriptional activity of different sets of genes in different cell types. This indicates that complex transcriptional regulation played a key role in the evolution of complexity in eukaryotes. In this review, we summarize how gene duplication and subsequent evolutionary innovations, including the structural evolution of nucleosomes and chromatin-related factors, contributed to the complexity of the transcriptional system and provided a basis for morphological diversity.

RevDate: 2019-05-09

Krishnan A, Degnan BM, SM Degnan (2019)

The first identification of complete Eph-ephrin signalling in ctenophores and sponges reveals a role for neofunctionalization in the emergence of signalling domains.

BMC evolutionary biology, 19(1):96 pii:10.1186/s12862-019-1418-z.

BACKGROUND: Animals have a greater diversity of signalling pathways than their unicellular relatives, consistent with the evolution and expansion of these pathways occurring in parallel with the origin of animal multicellularity. However, the genomes of sponges and ctenophores - non-bilaterian basal animals - typically encode no, or far fewer, recognisable signalling ligands compared to bilaterians and cnidarians. For instance, the largest subclass of receptor tyrosine kinases (RTKs) in bilaterians, the Eph receptors (Ephs), are present in sponges and ctenophores, but their cognate ligands, the ephrins, have not yet been detected.

RESULTS: Here, we use an iterative HMM analysis to identify for the first time membrane-bound ephrins in sponges and ctenophores. We also expand the number of Eph-receptor subtypes identified in these animals and in cnidarians. Both sequence and structural analyses are consistent with the Eph ligand binding domain (LBD) and the ephrin receptor binding domain (RBD) having evolved via the co-option of ancient galactose-binding (discoidin-domain)-like and monodomain cupredoxin domains, respectively. Although we did not detect a complete Eph-ephrin signalling pathway in closely-related unicellular holozoans or in other non-metazoan eukaryotes, truncated proteins with Eph receptor LBDs and ephrin RBDs are present in some choanoflagellates. Together, these results indicate that Eph-ephrin signalling was present in the last common ancestor of extant metazoans, and perhaps even in the last common ancestor of animals and choanoflagellates. Either scenario pushes the origin of Eph-ephrin signalling back much earlier than previously reported.

CONCLUSIONS: We propose that the Eph-LBD and ephrin-RBD, which were ancestrally localised in the cytosol, became linked to the extracellular parts of two cell surface proteins before the divergence of sponges and ctenophores from the rest of the animal kingdom. The ephrin-RBD lost the ancestral capacity to bind copper, and the Eph-LBD became linked to an ancient RTK. The identification of divergent ephrin ligands in sponges and ctenophores suggests that these ligands evolve faster than their cognate receptors. As this may be a general phenomena, we propose that the sequence-structure approach used in this study may be usefully applied to other signalling systems where no, or a small number of, ligands have been identified.

RevDate: 2019-04-23

Gunaratne PH, Pan Y, Rao AK, et al (2019)

Activating p53 family member TAp63: A novel therapeutic strategy for targeting p53-altered tumors.

Cancer [Epub ahead of print].

BACKGROUND: Over 96% of high-grade ovarian carcinomas and 50% of all cancers are characterized by alterations in the p53 gene. Therapeutic strategies to restore and/or reactivate the p53 pathway have been challenging. By contrast, p63, which shares many of the downstream targets and functions of p53, is rarely mutated in cancer.

METHODS: A novel strategy is presented for circumventing alterations in p53 by inducing the tumor-suppressor isoform TAp63 (transactivation domain of tumor protein p63) through its direct downstream target, microRNA-130b (miR-130b), which is epigenetically silenced and/or downregulated in chemoresistant ovarian cancer.

RESULTS: Treatment with miR-130b resulted in: 1) decreased migration/invasion in HEYA8 cells (p53 wild-type) and disruption of multicellular spheroids in OVCAR8 cells (p53-mutant) in vitro, 2) sensitization of HEYA8 and OVCAR8 cells to cisplatin (CDDP) in vitro and in vivo, and 3) transcriptional activation of TAp63 and the B-cell lymphoma (Bcl)-inhibitor B-cell lymphoma 2-like protein 11 (BIM). Overexpression of TAp63 was sufficient to decrease cell viability, suggesting that it is a critical downstream effector of miR-130b. In vivo, combined miR-130b plus CDDP exhibited greater therapeutic efficacy than miR-130b or CDDP alone. Mice that carried OVCAR8 xenograft tumors and were injected with miR-130b in 1,2-dioleoyl-sn-glycero-3-phosphatidylcholine (DOPC) liposomes had a significant decrease in tumor burden at rates similar to those observed in CDDP-treated mice, and 20% of DOPC-miR-130b plus CDDP-treated mice were living tumor free. Systemic injections of scL-miR-130b plus CDDP in a clinically tested, tumor-targeted nanocomplex (scL) improved survival in 60% and complete remissions in 40% of mice that carried HEYA8 xenografts.

CONCLUSIONS: The miR-130b/TAp63 axis is proposed as a new druggable pathway that has the potential to uncover broad-spectrum therapeutic options for the majority of p53-altered cancers.

RevDate: 2019-06-06

Sudianto E (2019)

Digest: Banding together to battle adversaries has its consequences.

Evolution; international journal of organic evolution, 73(6):1320-1321.

Why did life evolve from single-celled to multicellular organisms? Could there be advantages to this transition? What about associated fitness costs? Kapsetaki and West found that although multicellularity allows Chlorella sorokiniana to avoid predation from similarly-sized predators, it also reduces their competitiveness when resources are limited.

RevDate: 2019-04-19

Lehtonen J, GA Parker (2019)

Evolution of the Two Sexes under Internal Fertilization and Alternative Evolutionary Pathways.

The American naturalist, 193(5):702-716.

Transition from isogamy to anisogamy, hence males and females, leads to sexual selection, sexual conflict, sexual dimorphism, and sex roles. Gamete dynamics theory links biophysics of gamete limitation, gamete competition, and resource requirements for zygote survival and assumes broadcast spawning. It makes testable predictions, but most comparative tests use volvocine algae, which feature internal fertilization. We broaden this theory by comparing broadcast-spawning predictions with two plausible internal-fertilization scenarios: gamete casting/brooding (one mating type retains gametes internally, the other broadcasts them) and packet casting/brooding (one type retains gametes internally, the other broadcasts packets containing gametes, which are released for fertilization). Models show that predictions are remarkably robust to these radical changes, yielding (1) isogamy under low gamete limitation, low gamete competition, and similar required resources for gametes and zygotes, (2) anisogamy when gamete competition and/or limitation are higher and when zygotes require more resources than gametes, as is likely as multicellularity develops, (3) a positive correlation between multicellular complexity and anisogamy ratio, and (4) under gamete competition, only brooders becoming female. Thus, gamete dynamics theory represents a potent rationale for isogamy/anisogamy and makes similar testable predictions for broadcast spawners and internal fertilizers, regardless of whether anisogamy or internal fertilization evolved first.

RevDate: 2019-04-19

Olito C, T Connallon (2019)

Sexually Antagonistic Variation and the Evolution of Dimorphic Sexual Systems.

The American naturalist, 193(5):688-701.

Multicellular Eukaryotes use a broad spectrum of sexual reproduction strategies, ranging from simultaneous hermaphroditism to complete dioecy (separate sexes). The evolutionary pathway from hermaphroditism to dioecy involves the spread of sterility alleles that eliminate female or male reproductive functions, producing unisexual individuals. Classical theory predicts that evolutionary transitions to dioecy are feasible when female and male sex functions genetically trade off with one another (allocation to sex functions is sexually antagonistic) and rates of self-fertilization and inbreeding depression are high within the ancestral hermaphrodite population. We show that genetic linkage between sterility alleles and loci under sexually antagonistic selection significantly alters these classical predictions. We identify three specific consequences of linkage for the evolution of dimorphic sexual systems. First, linkage broadens conditions for the invasion of unisexual sterility alleles, facilitating transitions to sexual systems that are intermediate between hermaphroditism and dioecy (androdioecy and gynodioecy). Second, linkage elevates the equilibrium frequencies of unisexual individuals within androdioecious and gynodioecious populations, which promotes subsequent transitions to full dioecy. Third, linkage dampens the role of inbreeding during transitions to androdioecy and gynodioecy, making these transitions feasible in outbred populations. We discuss implications of these results for the evolution of dimorphic reproductive systems and sex chromosomes.

RevDate: 2019-04-16

Pérez P, Soto T, Gómez-Gil E, et al (2019)

Functional interaction between Cdc42 and the stress MAPK signaling pathway during the regulation of fission yeast polarized growth.

International microbiology : the official journal of the Spanish Society for Microbiology pii:10.1007/s10123-019-00072-6 [Epub ahead of print].

Cell polarization can be defined as the generation and maintenance of directional cellular organization. The spatial distribution and protein or lipid composition of the cell are not symmetric but organized in specialized domains which allow cells to grow and acquire a certain shape that is closely linked to their physiological function. The establishment and maintenance of polarized growth requires the coordination of diverse processes including cytoskeletal dynamics, membrane trafficking, and signaling cascade regulation. Some of the major players involved in the selection and maintenance of sites for polarized growth are Rho GTPases, which recognize the polarization site and transmit the signal to regulatory proteins of the cytoskeleton. Additionally, cytoskeletal organization, polarized secretion, and endocytosis are controlled by signaling pathways including those mediated by mitogen-activated protein kinases (MAPKs). Rho GTPases and the MAPK signaling pathways are strongly conserved from yeast to mammals, suggesting that the basic mechanisms of polarized growth have been maintained throughout evolution. For this reason, the study of how polarized growth is established and regulated in simple organisms such as the fission yeast Schizosaccharomyces pombe has contributed to broaden our knowledge about these processes in multicellular organisms. We review here the function of the Cdc42 GTPase and the stress activated MAPK (SAPK) signaling pathways during fission yeast polarized growth, and discuss the relevance of the crosstalk between both pathways.

RevDate: 2019-05-16

Qian XX, Liu J, Menguy N, et al (2019)

Identification of novel species of marine magnetotactic bacteria affiliated with Nitrospirae phylum.

Environmental microbiology reports, 11(3):330-337.

Magnetotactic bacteria (MTB) are a group of Gram-negative bacteria characterized by synthesizing magnetosomes and swimming along geomagnetic field lines. Phylogenetically, they belong to different taxonomic lineages including Proteobacteria, Nitrospirae, Omnitrophica, Latescibacteria and Planctomycetes phyla on the phylogenetic tree. To date, six Nitrospirae MTB phylotypes have been identified from freshwater or low-salinity environments and described in the literature. Here, we report the identification of two Nitrospirae MTB phylotypes collected, for the first time, from the marine environment. Both have a spherical morphology with a cell size of ~ 5 μM and similar motility but are different colours (black-brown and ivory-white) under the optic microscope. They synthesized bullet-shaped iron-oxide magnetosomes that were arranged in multiple bundles of chains. Moreover, the cytoplasm of the black-brown Nitrospirae MTB contained sulphur inclusions that conferred on cells a rough, granular appearance. Phylogenetic analysis based on their 16S rRNA gene sequences revealed that they are two novel species and cluster with the previously reported MTB affiliated with the phylum Nitrospirae, thus extending the distribution of Nitrospirae MTB from freshwater to the marine environment.

RevDate: 2019-05-08

Laundon D, Larson BT, McDonald K, et al (2019)

The architecture of cell differentiation in choanoflagellates and sponge choanocytes.

PLoS biology, 17(4):e3000226 pii:PBIOLOGY-D-18-01101.

Although collar cells are conserved across animals and their closest relatives, the choanoflagellates, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta expresses genes necessary for animal development and can alternate between unicellular and multicellular states, making it a powerful model for investigating the origin of animal multicellularity and mechanisms underlying cell differentiation. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular 'rosette' colonies and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with higher levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell-cell contact networks, and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type, pointing toward spatial cell differentiation. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some but not all neighbouring cells. Reconstruction of sponge choanocytes revealed ultrastructural commonalities but also differences in major organelle composition in comparison to choanoflagellates. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of animals.

RevDate: 2019-05-02

Rêgo A, Messina FJ, Z Gompert (2019)

Dynamics of genomic change during evolutionary rescue in the seed beetle Callosobruchus maculatus.

Molecular ecology [Epub ahead of print].

Rapid adaptation can prevent extinction when populations are exposed to extremely marginal or stressful environments. Factors that affect the likelihood of evolutionary rescue from extinction have been identified, but much less is known about the evolutionary dynamics (e.g., rates and patterns of allele frequency change) and genomic basis of successful rescue, particularly in multicellular organisms. We conducted an evolve-and-resequence experiment to investigate the dynamics of evolutionary rescue at the genetic level in the cowpea seed beetle, Callosobruchus maculatus, when it is experimentally shifted to a stressful host plant, lentil. Low survival (~1%) at the onset of the experiment caused population decline. But adaptive evolution quickly rescued the population, with survival rates climbing to 69% by the F5 generation and 90% by the F10 generation. Population genomic data showed that rescue likely was caused by rapid evolutionary change at multiple loci, with many alleles fixing or nearly fixing within five generations of selection on lentil. Selection on these loci was only moderately consistent in time, but parallel evolutionary changes were evident in sublines formed after the lentil line had passed through a bottleneck. By comparing estimates of selection and genomic change on lentil across five independent C. maculatus lines (the new lentil-adapted line, three long-established lines and one case of failed evolutionary rescue), we found that adaptation on lentil occurred via somewhat idiosyncratic evolutionary changes. Overall, our results suggest that evolutionary rescue in this system can be caused by very strong selection on multiple loci driving rapid and pronounced genomic change.

RevDate: 2019-04-10

Nguyen H, Koehl MAR, Oakes C, et al (2019)

Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates.

Journal of the Royal Society, Interface, 16(150):20180736.

Choanoflagellates, eukaryotes that are important predators on bacteria in aquatic ecosystems, are closely related to animals and are used as a model system to study the evolution of animals from protozoan ancestors. The choanoflagellate Salpingoeca rosetta has a complex life cycle with different morphotypes, some unicellular and some multicellular. Here we use computational fluid dynamics to study the hydrodynamics of swimming and feeding by different unicellular stages of S. rosetta: a swimming cell with a collar of prey-capturing microvilli surrounding a single flagellum, a thecate cell attached to a surface and a dispersal-stage cell with a slender body, long flagellum and short collar. We show that a longer flagellum increases swimming speed, longer microvilli reduce speed and cell shape only affects speed when the collar is very short. The flux of prey-carrying water into the collar capture zone is greater for swimming than sessile cells, but this advantage decreases with collar size. Stalk length has little effect on flux for sessile cells. We show that ignoring the collar, as earlier models have done, overestimates flux and greatly overestimates the benefit to feeding performance of swimming versus being attached, and of a longer stalk for attached cells.

RevDate: 2019-04-11

Baade T, Paone C, Baldrich A, et al (2019)

Clustering of integrin β cytoplasmic domains triggers nascent adhesion formation and reveals a protozoan origin of the integrin-talin interaction.

Scientific reports, 9(1):5728 pii:10.1038/s41598-019-42002-6.

Integrins and integrin-dependent cell-matrix adhesions are essential for a number of physiological processes. Integrin function is tightly regulated via binding of cytoplasmic proteins to integrin intracellular domains. Yet, the complexity of cell-matrix adhesions in mammals, with more than 150 core adhesome proteins, complicates the analysis of integrin-associated protein complexes. Interestingly, the evolutionary origin of integrins dates back before the transition from unicellular life to complex multicellular animals. Though unicellular relatives of metazoa have a less complex adhesome, nothing is known about the initial steps of integrin activation and adhesion complex assembly in protozoa. Therefore, we developed a minimal, microscope-based system using chimeric integrins to investigate receptor-proximal events during focal adhesion assembly. Clustering of the human integrin β1 tail led to recruitment of talin, kindlin, and paxillin and mutation of the known talin binding site abolished recruitment of this protein. Proteins indirectly linked to integrins, such as vinculin, migfilin, p130CAS, or zyxin were not enriched around the integrin β1 tail. With the exception of integrin β4 and integrin β8, the cytoplasmic domains of all human integrin β subunits supported talin binding. Likewise, the cytoplasmic domains of integrin β subunits expressed by the protozoan Capsaspora owczarzaki readily recruited talin and this interaction was based on an evolutionary conserved NPXY/F amino acid motif. The results we present here validate the use of our novel microscopic assay to uncover details of integrin-based protein-protein interactions in a cellular context and suggest that talin binding to integrin β cytoplasmic tails is an ancient feature of integrin regulation.

RevDate: 2019-04-07

Bohlin J, JH Pettersson (2019)

Evolution of Genomic Base Composition: From Single Cell Microbes to Multicellular Animals.

Computational and structural biotechnology journal, 17:362-370 pii:S2001-0370(18)30183-1.

Whole genome sequencing (WGS) of thousands of microbial genomes has provided considerable insight into evolutionary mechanisms in the microbial world. While substantially fewer eukaryotic genomes are available for analyses the number is rapidly increasing. This mini-review summarizes broadly evolutionary dynamics of base composition in the different domains of life from the perspective of prokaryotes. Common and different evolutionary mechanisms influencing genomic base composition in eukaryotes and prokaryotes are discussed. The conclusion from the data currently available suggests that while there are similarities there are also striking differences in how genomic base composition has evolved within prokaryotes and eukaryotes. For instance, homologous recombination appears to increase GC content locally in eukaryotes due to a non-selective process termed GC-biased gene conversion (gBGC). For prokaryotes on the other hand, increase in genomic GC content seems to be driven by the environment and selection. We find that similar phenomena observed for some organisms in each respective domain may be caused by very different mechanisms: while gBGC and recombination rates appear to explain the negative correlation between GC3 (GC content based on the third codon nucleotides) and genome size in some eukaryotes uptake of AT rich DNA sequences is the main reason for a similar negative correlation observed in prokaryotes. We provide further examples that indicate that base composition in prokaryotes and eukaryotes have evolved under very different constraints.

RevDate: 2019-05-07

Gulli JG, Herron MD, WC Ratcliff (2019)

Evolution of altruistic cooperation among nascent multicellular organisms.

Evolution; international journal of organic evolution, 73(5):1012-1024.

Cooperation is a classic solution to hostile environments that limit individual survival. In extreme cases this may lead to the evolution of new types of biological individuals (e.g., eusocial super-organisms). We examined the potential for interindividual cooperation to evolve via experimental evolution, challenging nascent multicellular "snowflake yeast" with an environment in which solitary multicellular clusters experienced low survival. In response, snowflake yeast evolved to form cooperative groups composed of thousands of multicellular clusters that typically survive selection. Group formation occurred through the creation of protein aggregates, only arising in strains with high (>2%) rates of cell death. Nonetheless, it was adaptive and repeatable, although ultimately evolutionarily unstable. Extracellular protein aggregates act as a common good, as they can be exploited by cheats that do not contribute to aggregate production. These results highlight the importance of group formation as a mechanism for surviving environmental stress, and underscore the remarkable ease with which even simple multicellular entities may evolve-and lose-novel social traits.

RevDate: 2019-06-10

Pedchenko V, Bauer R, Pokidysheva EN, et al (2019)

A chloride ring is an ancient evolutionary innovation mediating the assembly of the collagen IV scaffold of basement membranes.

The Journal of biological chemistry, 294(20):7968-7981.

Collagen IV scaffold is a principal component of the basement membrane (BM), a specialized extracellular matrix that is essential for animal multicellularity and tissue evolution. Scaffold assembly begins with the trimerization of α-chains into protomers inside the cell, which then are secreted and undergo oligomerization outside the cell. For the ubiquitous scaffold composed of α1- and α2-chains, both intracellular and extracellular stages are mediated by the noncollagenous domain (NC1). The association of protomers is chloride-dependent, whereby chloride ions induce interactions of the protomers' trimeric NC1 domains leading to NC1 hexamer formation. Here, we investigated the mechanisms, kinetics, and functionality of the chloride ion-mediated protomer assembly by using a single-chain technology to produce a stable NC1 trimer comprising α1, α2, and α1 NC1 monomers. We observed that in the presence of chloride, the single-chain NC1-trimer self-assembles into a hexamer, for which the crystal structure was determined. We discovered that a chloride ring, comprising 12 ions, induces the assembly of and stabilizes the NC1 hexamer. Furthermore, we found that the chloride ring is evolutionarily conserved across all animals, first appearing in cnidarians. These findings reveal a fundamental role for the chloride ring in the assembly of collagen IV scaffolds of BMs, a critical event enabling tissue evolution and development. Moreover, the single-chain technology is foundational for generating trimeric NC1 domains of other α-chain compositions to investigate the α121, α345, and α565 collagen IV scaffolds and to develop therapies for managing Alport syndrome, Goodpasture's disease, and cancerous tumor growth.

RevDate: 2019-05-07

Zhu SQ, Zhang YJ, Abbas MN, et al (2019)

Hedgehog promotes cell proliferation in the midgut of silkworm, Bombyx mori.

Insect science [Epub ahead of print].

The Hedgehog (Hh) signaling pathway is one of the major regulators of embryonic development and tissue homeostasis in multicellular organisms. However, the role of this pathway in the silkworm, especially in the silkworm midgut, remains poorly understood. Here, we report that Bombyx mori Hedgehog (BmHh) is expressed in most tissues of silkworm larvae and that its functions are well-conserved throughout evolution. We further demonstrate that the messenger RNA of four Hh signaling components, BmHh ligand, BmPtch receptor, signal transducer BmSmo and transcription factor BmCi, are all upregulated following Escherichia coli or Bacillus thuringiensis infection, indicating the activation of the Hh pathway. Simultaneously, midgut cell proliferation is strongly promoted. Conversely, the repression of Hh signal transduction with double-stranded RNA or cyclopamine inhibits the expression of BmHh and BmCi and reduces cell proliferation. Overall, these findings provide new insights into the Hh signaling pathway in the silkworm, B. mori.

RevDate: 2019-04-26

Arimoto A, Nishitsuji K, Higa Y, et al (2019)

A siphonous macroalgal genome suggests convergent functions of homeobox genes in algae and land plants.

DNA research : an international journal for rapid publication of reports on genes and genomes pii:5419551 [Epub ahead of print].

Genome evolution and development of unicellular, multinucleate macroalgae (siphonous algae) are poorly known, although various multicellular organisms have been studied extensively. To understand macroalgal developmental evolution, we assembled the ∼26 Mb genome of a siphonous green alga, Caulerpa lentillifera, with high contiguity, containing 9,311 protein-coding genes. Molecular phylogeny using 107 nuclear genes indicates that the diversification of the class Ulvophyceae, including C. lentillifera, occurred before the split of the Chlorophyceae and Trebouxiophyceae. Compared with other green algae, the TALE superclass of homeobox genes, which expanded in land plants, shows a series of lineage-specific duplications in this siphonous macroalga. Plant hormone signalling components were also expanded in a lineage-specific manner. Expanded transport regulators, which show spatially different expression, suggest that the structural patterning strategy of a multinucleate cell depends on diversification of nuclear pore proteins. These results not only imply functional convergence of duplicated genes among green plants, but also provide insight into evolutionary roots of green plants. Based on the present results, we propose cellular and molecular mechanisms involved in the structural differentiation in the siphonous alga.

RevDate: 2019-04-01

Stucky BJ, Balhoff JP, Barve N, et al (2019)

Developing a vocabulary and ontology for modeling insect natural history data: example data, use cases, and competency questions.

Biodiversity data journal, 7:e33303 pii:33303.

Insects are possibly the most taxonomically and ecologically diverse class of multicellular organisms on Earth. Consequently, they provide nearly unlimited opportunities to develop and test ecological and evolutionary hypotheses. Currently, however, large-scale studies of insect ecology, behavior, and trait evolution are impeded by the difficulty in obtaining and analyzing data derived from natural history observations of insects. These data are typically highly heterogeneous and widely scattered among many sources, which makes developing robust information systems to aggregate and disseminate them a significant challenge. As a step towards this goal, we report initial results of a new effort to develop a standardized vocabulary and ontology for insect natural history data. In particular, we describe a new database of representative insect natural history data derived from multiple sources (but focused on data from specimens in biological collections), an analysis of the abstract conceptual areas required for a comprehensive ontology of insect natural history data, and a database of use cases and competency questions to guide the development of data systems for insect natural history data. We also discuss data modeling and technology-related challenges that must be overcome to implement robust integration of insect natural history data.

RevDate: 2019-03-27

Kolasa M, Ścibior R, Mazur MA, et al (2019)

How Hosts Taxonomy, Trophy, and Endosymbionts Shape Microbiome Diversity in Beetles.

Microbial ecology pii:10.1007/s00248-019-01358-y [Epub ahead of print].

Bacterial communities play a crucial role in the biology, ecology, and evolution of multicellular organisms. In this research, the microbiome of 24 selected beetle species representing five families (Carabidae, Staphylinidae, Curculionidae, Chrysomelidae, Scarabaeidae) and three trophic guilds (carnivorous, herbivorous, detrivorous) was examined using 16S rDNA sequencing on the Illumina platform. The aim of the study was to compare diversity within and among species on various levels of organization, including evaluation of the impact of endosymbiotic bacteria. Collected data showed that beetles possess various bacterial communities and that microbiota of individuals of particular species hosts are intermixed. The most diverse microbiota were found in Carabidae and Scarabaeidae; the least diverse, in Staphylinidae. On higher organization levels, the diversity of bacteria was more dissimilar between families, while the most distinct with respect to their microbiomes were trophic guilds. Moreover, eight taxa of endosymbiotic bacteria were detected including common genera such as Wolbachia, Rickettsia, and Spiroplasma, as well as the rarely detected Cardinium, Arsenophonus, Buchnera, Sulcia, Regiella, and Serratia. There were no correlations among the abundance of the most common Wolbachia and Rickettsia; a finding that does not support the hypothesis that these bacteria occur interchangeably. The abundance of endosymbionts only weakly and negatively correlates with diversity of the whole microbiome in beetles. Overall, microbiome diversity was found to be more dependent on host phylogeny than on the abundance of endosymbionts. This is the first study in which bacteria diversity is compared between numerous species of beetles in a standardized manner.

RevDate: 2019-03-29

Bielska E, Birch PRJ, Buck AH, et al (2019)

Highlights of the mini-symposium on extracellular vesicles in inter-organismal communication, held in Munich, Germany, August 2018.

Journal of extracellular vesicles, 8(1):1590116 pii:1590116.

All living organisms secrete molecules for intercellular communication. Recent research has revealed that extracellular vesicles (EVs) play an important role in inter-organismal cell-to-cell communication by transporting diverse messenger molecules, including RNA, DNA, lipids and proteins. These discoveries have raised fundamental questions regarding EV biology. How are EVs biosynthesized and loaded with messenger/cargo molecules? How are EVs secreted into the extracellular matrix? What are the EV uptake mechanisms of recipient cells? As EVs are produced by all kind of organisms, from unicellular bacteria and protists, filamentous fungi and oomycetes, to complex multicellular life forms such as plants and animals, basic research in diverse model systems is urgently needed to shed light on the multifaceted biology of EVs and their role in inter-organismal communications. To help catalyse progress in this emerging field, a mini-symposium was held in Munich, Germany in August 2018. This report highlights recent progress and major questions being pursued across a very diverse group of model systems, all united by the question of how EVs contribute to inter-organismal communication.

RevDate: 2019-04-28

Moffitt L, Karimnia N, Stephens A, et al (2019)

Therapeutic Targeting of Collective Invasion in Ovarian Cancer.

International journal of molecular sciences, 20(6): pii:ijms20061466.

Ovarian cancer is the seventh most commonly diagnosed cancer amongst women and has the highest mortality rate of all gynaecological malignancies. It is a heterogeneous disease attributed to one of three cell types found within the reproductive milieu: epithelial, stromal, and germ cell. Each histotype differs in etiology, pathogenesis, molecular biology, risk factors, and prognosis. Furthermore, the origin of ovarian cancer remains unclear, with ovarian involvement secondary to the contribution of other gynaecological tissues. Despite these complexities, the disease is often treated as a single entity, resulting in minimal improvement to survival rates since the introduction of platinum-based chemotherapy over 30 years ago. Despite concerted research efforts, ovarian cancer remains one of the most difficult cancers to detect and treat, which is in part due to the unique mode of its dissemination. Ovarian cancers tend to invade locally to neighbouring tissues by direct extension from the primary tumour, and passively to pelvic and distal organs within the peritoneal fluid or ascites as multicellular spheroids. Once at their target tissue, ovarian cancers, like most epithelial cancers including colorectal, melanoma, and breast, tend to invade as a cohesive unit in a process termed collective invasion, driven by specialized cells termed "leader cells". Emerging evidence implicates leader cells as essential drivers of collective invasion and metastasis, identifying collective invasion and leader cells as a viable target for the management of metastatic disease. However, the development of targeted therapies specifically against this process and this subset of cells is lacking. Here, we review our understanding of metastasis, collective invasion, and the role of leader cells in ovarian cancer. We will discuss emerging research into the development of novel therapies targeting collective invasion and the leader cell population.

RevDate: 2019-05-22
CmpDate: 2019-05-22

Krizsán K, Almási É, Merényi Z, et al (2019)

Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi.

Proceedings of the National Academy of Sciences of the United States of America, 116(15):7409-7418.

The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including animals, embryophytes, red and brown algae, and fungi. Despite being a key step toward the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. The development of fungal fruiting bodies from a hyphal thallus represents a transition from simple to complex multicellularity that is inducible under laboratory conditions. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall remodeling, targeted protein degradation, signal transduction, adhesion, and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, many of which convergently expanded in multicellular plants and/or animals too, reflecting convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides an entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms.

RevDate: 2019-03-22

Wielgoss S, Wolfensberger R, Sun L, et al (2019)

Social genes are selection hotspots in kin groups of a soil microbe.

Science (New York, N.Y.), 363(6433):1342-1345.

The composition of cooperative systems, including animal societies, organismal bodies, and microbial groups, reflects their past and shapes their future evolution. However, genomic diversity within many multiunit systems remains uncharacterized, limiting our ability to understand and compare their evolutionary character. We have analyzed genomic and social-phenotype variation among 120 natural isolates of the cooperative bacterium Myxococcus xanthus derived from six multicellular fruiting bodies. Each fruiting body was composed of multiple lineages radiating from a unique recent ancestor. Genomic evolution was concentrated in selection hotspots associated with evolutionary change in social phenotypes. Synonymous mutations indicated that kin lineages within the same fruiting body often first diverged from a common ancestor more than 100 generations ago. Thus, selection appears to promote endemic diversification of kin lineages that remain together over long histories of local interaction, thereby potentiating social coevolution.

RevDate: 2019-04-17

Talbert PB, Meers MP, S Henikoff (2019)

Old cogs, new tricks: the evolution of gene expression in a chromatin context.

Nature reviews. Genetics, 20(5):283-297.

Sophisticated gene-regulatory mechanisms probably evolved in prokaryotes billions of years before the emergence of modern eukaryotes, which inherited the same basic enzymatic machineries. However, the epigenomic landscapes of eukaryotes are dominated by nucleosomes, which have acquired roles in genome packaging, mitotic condensation and silencing parasitic genomic elements. Although the molecular mechanisms by which nucleosomes are displaced and modified have been described, just how transcription factors, histone variants and modifications and chromatin regulators act on nucleosomes to regulate transcription is the subject of considerable ongoing study. We explore the extent to which these transcriptional regulatory components function in the context of the evolutionarily ancient role of chromatin as a barrier to processes acting on DNA and how chromatin proteins have diversified to carry out evolutionarily recent functions that accompanied the emergence of differentiation and development in multicellular eukaryotes.

RevDate: 2019-04-17
CmpDate: 2019-04-03

Xu S, Stapley J, Gablenz S, et al (2019)

Low genetic variation is associated with low mutation rate in the giant duckweed.

Nature communications, 10(1):1243 pii:10.1038/s41467-019-09235-5.

Mutation rate and effective population size (Ne) jointly determine intraspecific genetic diversity, but the role of mutation rate is often ignored. Here we investigate genetic diversity, spontaneous mutation rate and Ne in the giant duckweed (Spirodela polyrhiza). Despite its large census population size, whole-genome sequencing of 68 globally sampled individuals reveals extremely low intraspecific genetic diversity. Assessed under natural conditions, the genome-wide spontaneous mutation rate is at least seven times lower than estimates made for other multicellular eukaryotes, whereas Ne is large. These results demonstrate that low genetic diversity can be associated with large-Ne species, where selection can reduce mutation rates to very low levels. This study also highlights that accurate estimates of mutation rate can help to explain seemingly unexpected patterns of genome-wide variation.

RevDate: 2019-06-06

Kapsetaki SE, SA West (2019)

The costs and benefits of multicellular group formation in algae.

Evolution; international journal of organic evolution, 73(6):1296-1308.

The first step in the evolution of complex multicellular organisms involves single cells forming a cooperative group. Consequently, to understand multicellularity, we need to understand the costs and benefits associated with multicellular group formation. We found that in the facultatively multicellular algae Chlorella sorokiniana: (1) the presence of the flagellate Ochromonas danica or the crustacean Daphnia magna leads to the formation of multicellular groups; (2) the formation of multicellular groups reduces predation by O. danica, but not by the larger predator D. magna; (3) under conditions of relatively low light intensity, where competition for light is greater, multicellular groups grow slower than single cells; (4) in the absence of live predators, the proportion of cells in multicellular groups decreases at a rate that does not vary with light intensity. These results can explain why, in cases such as this algae species, multicellular group formation is facultative, in response to the presence of predators.

RevDate: 2019-04-21

Goh GH, Maloney SK, Mark PJ, et al (2019)

Episodic Ultradian Events-Ultradian Rhythms.

Biology, 8(1): pii:biology8010015.

In the fast lane of chronobiology, ultradian events are short-term rhythms that have been observed since the beginning of modern biology and were quantified about a century ago. They are ubiquitous in all biological systems and found in all organisms, from unicellular organisms to mammals, and from single cells to complex biological functions in multicellular animals. Since these events are aperiodic and last for a few minutes to a few hours, they are better classified as episodic ultradian events (EUEs). Their origin is unclear. However, they could have a molecular basis and could be controlled by hormonal inputs-in vertebrates, they originate from the activity of the central nervous system. EUEs are receiving increasing attention but their aperiodic nature requires specific sampling and analytic tools. While longer scale rhythms are adaptations to predictable changes in the environment, in theory, EUEs could contribute to adaptation by preparing organisms and biological functions for unpredictability.

RevDate: 2019-06-10

Shoemark DK, Ziegler B, Watanabe H, et al (2019)

Emergence of a Thrombospondin Superfamily at the Origin of Metazoans.

Molecular biology and evolution, 36(6):1220-1238.

Extracellular matrix (ECM) is considered central to the evolution of metazoan multicellularity; however, the repertoire of ECM proteins in nonbilaterians remains unclear. Thrombospondins (TSPs) are known to be well conserved from cnidarians to vertebrates, yet to date have been considered a unique family, principally studied for matricellular functions in vertebrates. Through searches utilizing the highly conserved C-terminal region of TSPs, we identify undisclosed new families of TSP-related proteins in metazoans, designated mega-TSP, sushi-TSP, and poriferan-TSP, each with a distinctive phylogenetic distribution. These proteins share the TSP C-terminal region domain architecture, as determined by domain composition and analysis of molecular models against known structures. Mega-TSPs, the only form identified in ctenophores, are typically >2,700 aa and are also characterized by N-terminal leucine-rich repeats and central cadherin/immunoglobulin domains. In cnidarians, which have a well-defined ECM, Mega-TSP was expressed throughout embryogenesis in Nematostella vectensis, with dynamic endodermal expression in larvae and primary polyps and widespread ectodermal expression in adult Nematostella vectensis and Hydra magnipapillata polyps. Hydra Mega-TSP was also expressed during regeneration and siRNA-silencing of Mega-TSP in Hydra caused specific blockade of head regeneration. Molecular phylogenetic analyses based on the conserved TSP C-terminal region identified each of the TSP-related groups to form clades distinct from the canonical TSPs. We discuss models for the evolution of the newly defined TSP superfamily by gene duplications, radiation, and gene losses from a debut in the last metazoan common ancestor. Together, the data provide new insight into the evolution of ECM and tissue organization in metazoans.

RevDate: 2019-06-10

Lenhart BA, Meeks B, HA Murphy (2019)

Variation in Filamentous Growth and Response to Quorum-Sensing Compounds in Environmental Isolates of Saccharomyces cerevisiae.

G3 (Bethesda, Md.), 9(5):1533-1544 pii:g3.119.400080.

In fungi, filamentous growth is a major developmental transition that occurs in response to environmental cues. In diploid Saccharomyces cerevisiae, it is known as pseudohyphal growth and presumed to be a foraging mechanism. Rather than unicellular growth, multicellular filaments composed of elongated, attached cells spread over and into surfaces. This morphogenetic switch can be induced through quorum sensing with the aromatic alcohols phenylethanol and tryptophol. Most research investigating pseudohyphal growth has been conducted in a single lab background, Σ1278b. To investigate the natural variation in this phenotype and its induction, we assayed the diverse 100-genomes collection of environmental isolates. Using computational image analysis, we quantified the production of pseudohyphae and observed a large amount of variation. Population origin was significantly associated with pseudohyphal growth, with the West African population having the most. Surprisingly, most strains showed little or no response to exogenous phenylethanol or tryptophol. We also investigated the amount of natural genetic variation in pseudohyphal growth using a mapping population derived from a highly-heterozygous clinical isolate that contained as much phenotypic variation as the environmental panel. A bulk-segregant analysis uncovered five major peaks with candidate loci that have been implicated in the Σ1278b background. Our results indicate that the filamentous growth response is a generalized, highly variable phenotype in natural populations, while response to quorum sensing molecules is surprisingly rare. These findings highlight the importance of coupling studies in tractable lab strains with natural isolates in order to understand the relevance and distribution of well-studied traits.

RevDate: 2019-03-29

Sicard A, Pirolles E, Gallet R, et al (2019)

A multicellular way of life for a multipartite virus.

eLife, 8: pii:43599.

A founding paradigm in virology is that the spatial unit of the viral replication cycle is an individual cell. Multipartite viruses have a segmented genome where each segment is encapsidated separately. In this situation the viral genome is not recapitulated in a single virus particle but in the viral population. How multipartite viruses manage to efficiently infect individual cells with all segments, thus with the whole genome information, is a long-standing but perhaps deceptive mystery. By localizing and quantifying the genome segments of a nanovirus in host plant tissues we show that they rarely co-occur within individual cells. We further demonstrate that distinct segments accumulate independently in different cells and that the viral system is functional through complementation across cells. Our observation deviates from the classical conceptual framework in virology and opens an alternative possibility (at least for nanoviruses) where the infection can operate at a level above the individual cell level, defining a viral multicellular way of life.

RevDate: 2019-03-21

Ruiz MC, Kljun J, Turel I, et al (2019)

Comparative antitumor studies of organoruthenium complexes with 8-hydroxyquinolines on 2D and 3D cell models of bone, lung and breast cancer.

Metallomics : integrated biometal science, 11(3):666-675.

The purpose of this work was to screen the antitumor actions of two metal organoruthenium-8-hydroxyquinolinato (Ru-hq) complexes to find a potential novel agent for bone, lung and breast chemotherapies. We showed that ruthenium compounds (1 and 2) impaired the cell viability of human bone (MG-63), lung (A549) and breast (MCF7) cancer cells with greater selectivity and specificity than cisplatin. Besides, complexes 1 and 2 decreased proliferation, migration and invasion on cell monolayers at lower concentrations (2.5-10 μM). In addition, both compounds induced genotoxicity revealed by the micronucleus test, which led to G2/M cell cycle arrest and induced the tumor cells to undergo apoptosis. On the other hand, in multicellular 3D models (multicellular spheroids; MCS), 1 and 2 overcame CDDP presenting lower IC50 values only in MCS of lung origin. Moreover, 1 outperformed 2 in MCS of bone and breast origin. Finally, our findings revealed that both compounds inhibited the cell invasion of multicellular spheroids, showing that complex 1 exhibited the most important antimetastatic action. Taken together, these results indicate that compound 1 is an interesting candidate to be tested on in vivo models as a novel strategy for anticancer therapy.

RevDate: 2019-03-30

Fillinger RJ, MZ Anderson (2019)

Seasons of change: Mechanisms of genome evolution in human fungal pathogens.

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases, 70:165-174.

Fungi are a diverse kingdom of organisms capable of thriving in various niches across the world including those in close association with multicellular eukaryotes. Fungal pathogens that contribute to human disease reside both within the host as commensal organisms of the microbiota and the environment. Their niche of origin dictates how infection initiates but also places specific selective pressures on the fungal pathogen that contributes to its genome organization and genetic repertoire. Recent efforts to catalogue genomic variation among major human fungal pathogens have unveiled evolutionary themes that shape the fungal genome. Mechanisms ranging from large scale changes such as aneuploidy and ploidy cycling as well as more targeted mutations like base substitutions and gene copy number variations contribute to the evolution of these species, which are often under multiple competing selective pressures with their host, environment, and other microbes. Here, we provide an overview of the major selective pressures and mechanisms acting to evolve the genome of clinically important fungal pathogens of humans.

RevDate: 2019-03-06

Kabir M, Wenlock S, Doig AJ, et al (2019)

The Essentiality Status of Mouse Duplicate Gene Pairs Correlates with Developmental Co-Expression Patterns.

Scientific reports, 9(1):3224 pii:10.1038/s41598-019-39894-9.

During the evolution of multicellular eukaryotes, gene duplication occurs frequently to generate new genes and/or functions. A duplicated gene may have a similar function to its ancestral gene. Therefore, it may be expected that duplicated genes are less likely to be critical for the survival of an organism, since there are multiple copies of the gene rendering each individual copy redundant. In this study, we explored the developmental expression patterns of duplicate gene pairs and the relationship between development co-expression and phenotypes resulting from the knockout of duplicate genes in the mouse. We define genes that generate lethal phenotypes in single gene knockout experiments as essential genes. We found that duplicate gene pairs comprised of two essential genes tend to be expressed at different stages of development, compared to duplicate gene pairs with at least one non-essential member, showing that the timing of developmental expression affects the ability of one paralogue to compensate for the loss of the other. Gene essentiality, developmental expression and gene duplication are thus closely linked.

RevDate: 2019-04-04
CmpDate: 2019-04-04

Lurgi M, Thomas T, Wemheuer B, et al (2019)

Modularity and predicted functions of the global sponge-microbiome network.

Nature communications, 10(1):992 pii:10.1038/s41467-019-08925-4.

Defining the organisation of species interaction networks and unveiling the processes behind their assembly is fundamental to understanding patterns of biodiversity, community stability and ecosystem functioning. Marine sponges host complex communities of microorganisms that contribute to their health and survival, yet the mechanisms behind microbiome assembly are largely unknown. We present the global marine sponge-microbiome network and reveal a modular organisation in both community structure and function. Modules are linked by a few sponge species that share microbes with other species around the world. Further, we provide evidence that abiotic factors influence the structuring of the sponge microbiome when considering all microbes present, but biotic interactions drive the assembly of more intimately associated 'core' microorganisms. These findings suggest that both ecological and evolutionary processes are at play in host-microbe network assembly. We expect mechanisms behind microbiome assembly to be consistent across multicellular hosts throughout the tree of life.

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RJR Experience and Expertise

Researcher

Robbins holds BS, MS, and PhD degrees in the life sciences. He served as a tenured faculty member in the Zoology and Biological Science departments at Michigan State University. He is currently exploring the intersection between genomics, microbial ecology, and biodiversity — an area that promises to transform our understanding of the biosphere.

Educator

Robbins has extensive experience in college-level education: At MSU he taught introductory biology, genetics, and population genetics. At JHU, he was an instructor for a special course on biological database design. At FHCRC, he team-taught a graduate-level course on the history of genetics. At Bellevue College he taught medical informatics.

Administrator

Robbins has been involved in science administration at both the federal and the institutional levels. At NSF he was a program officer for database activities in the life sciences, at DOE he was a program officer for information infrastructure in the human genome project. At the Fred Hutchinson Cancer Research Center, he served as a vice president for fifteen years.

Technologist

Robbins has been involved with information technology since writing his first Fortran program as a college student. At NSF he was the first program officer for database activities in the life sciences. At JHU he held an appointment in the CS department and served as director of the informatics core for the Genome Data Base. At the FHCRC he was VP for Information Technology.

Publisher

While still at Michigan State, Robbins started his first publishing venture, founding a small company that addressed the short-run publishing needs of instructors in very large undergraduate classes. For more than 20 years, Robbins has been operating The Electronic Scholarly Publishing Project, a web site dedicated to the digital publishing of critical works in science, especially classical genetics.

Speaker

Robbins is well-known for his speaking abilities and is often called upon to provide keynote or plenary addresses at international meetings. For example, in July, 2012, he gave a well-received keynote address at the Global Biodiversity Informatics Congress, sponsored by GBIF and held in Copenhagen. The slides from that talk can be seen HERE.

Facilitator

Robbins is a skilled meeting facilitator. He prefers a participatory approach, with part of the meeting involving dynamic breakout groups, created by the participants in real time: (1) individuals propose breakout groups; (2) everyone signs up for one (or more) groups; (3) the groups with the most interested parties then meet, with reports from each group presented and discussed in a subsequent plenary session.

Designer

Robbins has been engaged with photography and design since the 1960s, when he worked for a professional photography laboratory. He now prefers digital photography and tools for their precision and reproducibility. He designed his first web site more than 20 years ago and he personally designed and implemented this web site. He engages in graphic design as a hobby.

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Collection of publications by R J Robbins

Reprints and preprints of publications, slide presentations, instructional materials, and data compilations written or prepared by Robert Robbins. Most papers deal with computational biology, genome informatics, using information technology to support biomedical research, and related matters.

Research Gate page for R J Robbins

ResearchGate is a social networking site for scientists and researchers to share papers, ask and answer questions, and find collaborators. According to a study by Nature and an article in Times Higher Education , it is the largest academic social network in terms of active users.

Curriculum Vitae for R J Robbins

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Curriculum Vitae for R J Robbins

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