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19 Nov 2018 at 01:33
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Bibliography on: Origin of Eukaryotes


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RJR: Recommended Bibliography 19 Nov 2018 at 01:33 Created: 

Origin of Eukaryotes

The evolutionary origin of eukaryotes is a critically important, yet poorly understood event in the history of life on earth. The endosymbiotic origin of mitochondria allowed cells to become sufficiently large that they could begin to interact mechanically with their surrounding environment, thereby allowing evolution to create the visible biosphere of multicellular eukaryotes.

Created with PubMed® Query: ("origin of eukaryotes"[TIAB] OR "appearance of eukaryotes"[TIAB] OR "evolution of eukaryotes[TIAB]") NOT pmcbook NOT ispreviousversion

Citations The Papers (from PubMed®)

RevDate: 2018-10-25

Gabaldón T (2018)

Relative timing of mitochondrial endosymbiosis and the "pre-mitochondrial symbioses" hypothesis.

IUBMB life [Epub ahead of print].

The origin of eukaryotes stands as a major open question in biology. Central to this question is the nature and timing of the origin of the mitochondrion, an ubiquitous eukaryotic organelle originated by the endosymbiosis of an alphaproteobacterial ancestor. Different hypotheses disagree, among other aspects, on whether mitochondria were acquired early or late during eukaryogenesis. Similarly, the nature and complexity of the receiving host is debated, with models ranging from a simple prokaryotic host to an already complex proto-eukaryote. Here, I will discuss recent findings from phylogenomics analyses of extant genomes that are shedding light into the evolutionary origins of the eukaryotic ancestor, and which suggest a later acquisition of alpha-proteobacterial derived proteins as compared to those with different bacterial ancestries. I argue that simple eukaryogenesis models that assume a binary symbiosis between an archaeon host and an alpha-proteobacterial proto-mitochondrion cannot explain the complex chimeric nature that is inferred for the eukaryotic ancestor. To reconcile existing hypotheses with the new data, I propose the "pre-mitochondrial symbioses" hypothesis that provides a framework for eukaryogenesis scenarios involving alternative symbiotic interactions that predate the acquisition of mitochondria. © 2018 IUBMB Life, 2018.

RevDate: 2018-07-30

Bártulos CR, Rogers MB, Williams TA, et al (2018)

Mitochondrial glycolysis in a major lineage of eukaryotes.

Genome biology and evolution pii:5061552 [Epub ahead of print].

The establishment of the mitochondrion is seen as a transformational step in the origin of eukaryotes. With the mitochondrion came bioenergetic freedom to explore novel evolutionary space leading to the eukaryotic radiation known today. The tight integration of the bacterial endosymbiont with its archaeal host was accompanied by a massive endosymbiotic gene transfer resulting in a small mitochondrial genome which is just a ghost of the original incoming bacterial genome. This endosymbiotic gene transfer resulted in the loss of many genes, both from the bacterial symbiont as well the archaeal host. Loss of genes encoding redundant functions resulted in a replacement of the bulk of the host's metabolism for those originating from the endosymbiont. Glycolysis is one such metabolic pathway in which the original archaeal enzymes have been replaced by the bacterial enzymes from the endosymbiont. Glycolysis is a major catabolic pathway that provides cellular energy from the breakdown of glucose. The glycolytic pathway of eukaryotes appears to be bacterial in origin, and in well-studied model eukaryotes it takes place in the cytosol. In contrast, here we demonstrate that the latter stages of glycolysis take place in the mitochondria of stramenopiles, a diverse and ecologically important lineage of eukaryotes. Although our work is based on a limited sample of stramenopiles, it leaves open the possibility that the mitochondrial targeting of glycolytic enzymes in stramenopiles might represent the ancestral state for eukaryotes.

RevDate: 2018-05-10

Kauko A, K Lehto (2018)

Eukaryote specific folds: Part of the whole.

Proteins [Epub ahead of print].

The origin of eukaryotes is one of the central transitions in the history of life; without eukaryotes there would be no complex multicellular life. The most accepted scenarios suggest the endosymbiosis of a mitochondrial ancestor with a complex archaeon, even though the details regarding the host and the triggering factors are still being discussed. Accordingly, phylogenetic analyses have demonstrated archaeal affiliations with key informational systems, while metabolic genes are often related to bacteria, mostly to the mitochondrial ancestor. Despite of this, there exists a large number of protein families and folds found only in eukaryotes. In this study, we have analyzed structural superfamilies and folds that probably appeared during eukaryogenesis. These folds typically represent relatively small binding domains of larger multidomain proteins. They are commonly involved in biological processes that are particularly complex in eukaryotes, such as signaling, trafficking/cytoskeleton, ubiquitination, transcription and RNA processing, but according to recent studies, these processes also have prokaryotic roots. Thus the folds originating from an eukaryotic stem seem to represent accessory parts that have contributed in the expansion of several prokaryotic processes to a new level of complexity. This might have taken place as a co-evolutionary process where increasing complexity and fold innovations have supported each other.

RevDate: 2018-03-22

Méheust R, Bhattacharya D, Pathmanathan JS, et al (2018)

Formation of chimeric genes with essential functions at the origin of eukaryotes.

BMC biology, 16(1):30 pii:10.1186/s12915-018-0500-0.

BACKGROUND: Eukaryotes evolved from the symbiotic association of at least two prokaryotic partners, and a good deal is known about the timings, mechanisms, and dynamics of these evolutionary steps. Recently, it was shown that a new class of nuclear genes, symbiogenetic genes (S-genes), was formed concomitant with endosymbiosis and the subsequent evolution of eukaryotic photosynthetic lineages. Understanding their origins and contributions to eukaryogenesis would provide insights into the ways in which cellular complexity has evolved.

RESULTS: Here, we show that chimeric nuclear genes (S-genes), built from prokaryotic domains, are critical for explaining the leap forward in cellular complexity achieved during eukaryogenesis. A total of 282 S-gene families contributed solutions to many of the challenges faced by early eukaryotes, including enhancing the informational machinery, processing spliceosomal introns, tackling genotoxicity within the cell, and ensuring functional protein interactions in a larger, more compartmentalized cell. For hundreds of S-genes, we confirmed the origins of their components (bacterial, archaeal, or generally prokaryotic) by maximum likelihood phylogenies. Remarkably, Bacteria contributed nine-fold more S-genes than Archaea, including a two-fold greater contribution to informational functions. Therefore, there is an additional, large bacterial contribution to the evolution of eukaryotes, implying that fundamental eukaryotic properties do not strictly follow the traditional informational/operational divide for archaeal/bacterial contributions to eukaryogenesis.

CONCLUSION: This study demonstrates the extent and process through which prokaryotic fragments from bacterial and archaeal genes inherited during eukaryogenesis underly the creation of novel chimeric genes with important functions.

RevDate: 2018-01-19

Eme L, Spang A, Lombard J, et al (2018)

Archaea and the origin of eukaryotes.

Nature reviews. Microbiology, 16(2):120.

This corrects the article DOI: 10.1038/nrmicro.2017.133.

RevDate: 2017-12-05

Janouškovec J, Tikhonenkov DV, Burki F, et al (2017)

A New Lineage of Eukaryotes Illuminates Early Mitochondrial Genome Reduction.

Current biology : CB, 27(23):3717-3724.e5.

The origin of eukaryotic cells represents a key transition in cellular evolution and is closely tied to outstanding questions about mitochondrial endosymbiosis [1, 2]. For example, gene-rich mitochondrial genomes are thought to be indicative of an ancient divergence, but this relies on unexamined assumptions about endosymbiont-to-host gene transfer [3-5]. Here, we characterize Ancoracysta twista, a new predatory flagellate that is not closely related to any known lineage in 201-protein phylogenomic trees and has a unique morphology, including a novel type of extrusome (ancoracyst). The Ancoracysta mitochondrion has a gene-rich genome with a coding capacity exceeding that of all other eukaryotes except the distantly related jakobids and Diphylleia, and it uniquely possesses heterologous, nucleus-, and mitochondrion-encoded cytochrome c maturase systems. To comprehensively examine mitochondrial genome reduction, we also assembled mitochondrial genomes from picozoans and colponemids and re-annotated existing mitochondrial genomes using hidden Markov model gene profiles. This revealed over a dozen previously overlooked mitochondrial genes at the level of eukaryotic supergroups. Analysis of trends over evolutionary time demonstrates that gene transfer to the nucleus was non-linear, that it occurred in waves of exponential decrease, and that much of it took place comparatively early, massively independently, and with lineage-specific rates. This process has led to differential gene retention, suggesting that gene-rich mitochondrial genomes are not a product of their early divergence. Parallel transfer of mitochondrial genes and their functional replacement by new nuclear factors are important in models for the origin of eukaryotes, especially as major gaps in our knowledge of eukaryotic diversity at the deepest level remain unfilled.

RevDate: 2018-02-07

Lin SC, DG Hardie (2018)

AMPK: Sensing Glucose as well as Cellular Energy Status.

Cell metabolism, 27(2):299-313.

Mammalian AMPK is known to be activated by falling cellular energy status, signaled by rising AMP/ATP and ADP/ATP ratios. We review recent information about how this occurs but also discuss new studies suggesting that AMPK is able to sense glucose availability independently of changes in adenine nucleotides. The glycolytic intermediate fructose-1,6-bisphosphate (FBP) is sensed by aldolase, which binds to the v-ATPase on the lysosomal surface. In the absence of FBP, interactions between aldolase and the v-ATPase are altered, allowing formation of an AXIN-based AMPK-activation complex containing the v-ATPase, Ragulator, AXIN, LKB1, and AMPK, causing increased Thr172 phosphorylation and AMPK activation. This nutrient-sensing mechanism activates AMPK but also primes it for further activation if cellular energy status subsequently falls. Glucose sensing at the lysosome, in which AMPK and other components of the activation complex act antagonistically with another key nutrient sensor, mTORC1, may have been one of the ancestral roles of AMPK.

RevDate: 2017-12-19
CmpDate: 2017-11-20

Eme L, Spang A, Lombard J, et al (2017)

Archaea and the origin of eukaryotes.

Nature reviews. Microbiology, 15(12):711-723.

Woese and Fox's 1977 paper on the discovery of the Archaea triggered a revolution in the field of evolutionary biology by showing that life was divided into not only prokaryotes and eukaryotes. Rather, they revealed that prokaryotes comprise two distinct types of organisms, the Bacteria and the Archaea. In subsequent years, molecular phylogenetic analyses indicated that eukaryotes and the Archaea represent sister groups in the tree of life. During the genomic era, it became evident that eukaryotic cells possess a mixture of archaeal and bacterial features in addition to eukaryotic-specific features. Although it has been generally accepted for some time that mitochondria descend from endosymbiotic alphaproteobacteria, the precise evolutionary relationship between eukaryotes and archaea has continued to be a subject of debate. In this Review, we outline a brief history of the changing shape of the tree of life and examine how the recent discovery of a myriad of diverse archaeal lineages has changed our understanding of the evolutionary relationships between the three domains of life and the origin of eukaryotes. Furthermore, we revisit central questions regarding the process of eukaryogenesis and discuss what can currently be inferred about the evolutionary transition from the first to the last eukaryotic common ancestor.

RevDate: 2018-06-13
CmpDate: 2018-06-13

Aanen DK, P Eggleton (2017)

Symbiogenesis: Beyond the endosymbiosis theory?.

Journal of theoretical biology, 434:99-103.

Symbiogenesis, literally 'becoming by living together', refers to the crucial role of symbiosis in major evolutionary innovations. The term usually is reserved for the major transition to eukaryotes and to photosynthesising eukaryotic algae and plants by endosymbiosis. However, in some eukaryote lineages endosymbionts have been lost secondarily, showing that symbiosis can trigger a major evolutionary innovation, even if symbionts were lost secondarily. This leads to the intriguing possibility that symbiosis has played a role in other major evolutionary innovations as well, even if not all extant representatives of such groups still have the symbiotic association. We evaluate this hypothesis for two innovations in termites (Termitoidae, also known informally as "Isoptera"): i) the role of flagellate gut protist symbionts in the transition to eusociality from cockroach-like ancestors, and ii) the role of non-gut associated symbionts in the transition to 'higher' termites, characterized by the absence of flagellate gut protists. In both cases we identify a crucial role for symbionts, even though in both cases, subsequently, symbionts were lost again in some lineages. We also briefly discuss additional possible examples of symbiogenesis. We conclude that symbiogenesis is more broadly applicable than just for the endosymbiotic origin of eukaryotes and photosynthetic eukaryotes, and may be a useful concept to acknowledge the important role of symbiosis for evolutionary innovation. However, we do not accept Lynn Margulis's view that symbiogenesis will lead to a paradigm shift from neoDarwinism, as the role of symbiosis in evolutionary change can be integrated with existing theory perfectly.

RevDate: 2018-03-26
CmpDate: 2018-01-31

Zachar I, E Szathmáry (2017)

Breath-giving cooperation: critical review of origin of mitochondria hypotheses : Major unanswered questions point to the importance of early ecology.

Biology direct, 12(1):19 pii:10.1186/s13062-017-0190-5.

The origin of mitochondria is a unique and hard evolutionary problem, embedded within the origin of eukaryotes. The puzzle is challenging due to the egalitarian nature of the transition where lower-level units took over energy metabolism. Contending theories widely disagree on ancestral partners, initial conditions and unfolding of events. There are many open questions but there is no comparative examination of hypotheses. We have specified twelve questions about the observable facts and hidden processes leading to the establishment of the endosymbiont that a valid hypothesis must address. We have objectively compared contending hypotheses under these questions to find the most plausible course of events and to draw insight on missing pieces of the puzzle. Since endosymbiosis borders evolution and ecology, and since a realistic theory has to comply with both domains' constraints, the conclusion is that the most important aspect to clarify is the initial ecological relationship of partners. Metabolic benefits are largely irrelevant at this initial phase, where ecological costs could be more disruptive. There is no single theory capable of answering all questions indicating a severe lack of ecological considerations. A new theory, compliant with recent phylogenomic results, should adhere to these criteria.

REVIEWERS: This article was reviewed by Michael W. Gray, William F. Martin and Purificación López-García.

RevDate: 2017-12-06
CmpDate: 2017-11-01

Fort P, A Blangy (2017)

The Evolutionary Landscape of Dbl-Like RhoGEF Families: Adapting Eukaryotic Cells to Environmental Signals.

Genome biology and evolution, 9(6):1471-1486.

The dynamics of cell morphology in eukaryotes is largely controlled by small GTPases of the Rho family. Rho GTPases are activated by guanine nucleotide exchange factors (RhoGEFs), of which diffuse B-cell lymphoma (Dbl)-like members form the largest family. Here, we surveyed Dbl-like sequences from 175 eukaryotic genomes and illuminate how the Dbl family evolved in all eukaryotic supergroups. By combining probabilistic phylogenetic approaches and functional domain analysis, we show that the human Dbl-like family is made of 71 members, structured into 20 subfamilies. The 71 members were already present in ancestral jawed vertebrates, but several members were subsequently lost in specific clades, up to 12% in birds. The jawed vertebrate repertoire was established from two rounds of duplications that occurred between tunicates, cyclostomes, and jawed vertebrates. Duplicated members showed distinct tissue distributions, conserved at least in Amniotes. All 20 subfamilies have members in Deuterostomes and Protostomes. Nineteen subfamilies are present in Porifera, the first phylum that diverged in Metazoa, 14 in Choanoflagellida and Filasterea, single-celled organisms closely related to Metazoa and three in Fungi, the sister clade to Metazoa. Other eukaryotic supergroups show an extraordinary variability of Dbl-like repertoires as a result of repeated and independent gain and loss events. Last, we observed that in Metazoa, the number of Dbl-like RhoGEFs varies in proportion of cell signaling complexity. Overall, our analysis supports the conclusion that Dbl-like RhoGEFs were present at the origin of eukaryotes and evolved as highly adaptive cell signaling mediators.

RevDate: 2018-06-13
CmpDate: 2018-06-13

Lane N (2017)

Serial endosymbiosis or singular event at the origin of eukaryotes?.

Journal of theoretical biology, 434:58-67.

'On the Origin of Mitosing Cells' heralded a new way of seeing cellular evolution, with symbiosis at its heart. Lynn Margulis (then Sagan) marshalled an impressive array of evidence for endosymbiosis, from cell biology to atmospheric chemistry and Earth history. Despite her emphasis on symbiosis, she saw plenty of evidence for gradualism in eukaryotic evolution, with multiple origins of mitosis and sex, repeated acquisitions of plastids, and putative evolutionary intermediates throughout the microbial world. Later on, Margulis maintained her view of multiple endosymbioses giving rise to other organelles such as hydrogenosomes, in keeping with the polyphyletic assumptions of the serial endosymbiosis theory. She stood at the threshold of the phylogenetic era, and anticipated its potential. Yet while predicting that the nucleotide sequences of genes would enable a detailed reconstruction of eukaryotic evolution, Margulis did not, and could not, imagine the radically different story that would eventually emerge from comparative genomics. The last eukaryotic common ancestor now seems to have been essentially a modern eukaryotic cell that had already evolved mitosis, meiotic sex, organelles and endomembrane systems. The long search for missing evolutionary intermediates has failed to turn up a single example, and those discussed by Margulis turn out to have evolved reductively from more complex ancestors. Strikingly, Margulis argued that all eukaryotes had mitochondria in her 1967 paper (a conclusion that she later disavowed). But she developed her ideas in the context of atmospheric oxygen and aerobic respiration, neither of which is consistent with more recent geological and phylogenetic findings. Instead, a modern synthesis of genomics and bioenergetics points to the endosymbiotic restructuring of eukaryotic genomes in relation to bioenergetic membranes as the singular event that permitted the evolution of morphological complexity.

RevDate: 2017-08-08
CmpDate: 2017-08-08

Harish A, CG Kurland (2017)

Akaryotes and Eukaryotes are independent descendants of a universal common ancestor.

Biochimie, 138:168-183.

We reconstructed a global tree of life (ToL) with non-reversible and non-stationary models of genome evolution that root trees intrinsically. We implemented Bayesian model selection tests and compared the statistical support for four conflicting ToL hypotheses. We show that reconstructions obtained with a Bayesian implementation (Klopfstein et al., 2015) are consistent with reconstructions obtained with an empirical Sankoff parsimony (ESP) implementation (Harish et al., 2013). Both are based on the genome contents of coding sequences for protein domains (superfamilies) from hundreds of genomes. Thus, we conclude that the independent descent of Eukaryotes and Akaryotes (archaea and bacteria) from the universal common ancestor (UCA) is the most probable as well as the most parsimonious hypothesis for the evolutionary origins of extant genomes. Reconstructions of ancestral proteomes by both Bayesian and ESP methods suggest that at least 70% of unique domain-superfamilies known in extant species were present in the UCA. In addition, identification of a vast majority (96%) of the mitochondrial superfamilies in the UCA proteome precludes a symbiotic hypothesis for the origin of eukaryotes. Accordingly, neither the archaeal origin of eukaryotes nor the bacterial origin of mitochondria is supported by the data. The proteomic complexity of the UCA suggests that the evolution of cellular phenotypes in the two primordial lineages, Akaryotes and Eukaryotes, was driven largely by duplication of common superfamilies as well as by loss of unique superfamilies. Finally, innovation of novel superfamilies has played a surprisingly small role in the evolution of Akaryotes and only a marginal role in the evolution of Eukaryotes.

RevDate: 2018-07-02
CmpDate: 2018-07-02

Martin WF, R Cerff (2017)

Physiology, phylogeny, early evolution, and GAPDH.

Protoplasma, 254(5):1823-1834.

The chloroplast and cytosol of plant cells harbor a number of parallel biochemical reactions germane to the Calvin cycle and glycolysis, respectively. These reactions are catalyzed by nuclear encoded, compartment-specific isoenzymes that differ in their physiochemical properties. The chloroplast cytosol isoenzymes of D-glyceraldehyde-3-phosphate dehydrogenase (GAPDH) harbor evidence of major events in the history of life: the origin of the first genes, the bacterial-archaeal split, the origin of eukaryotes, the evolution of protein compartmentation during eukaryote evolution, the origin of plastids, and the secondary endosymbiosis among the algae with complex plastids. The reaction mechanism of GAPDH entails phosphorolysis of a thioester to yield an energy-rich acyl phosphate bond, a chemistry that points to primitive pathways of energy conservation that existed even before the origin of the first free-living cells. Here, we recount the main insights that chloroplast and cytosolic GAPDH provided into endosymbiosis and physiological evolution.

RevDate: 2018-01-04
CmpDate: 2018-01-04

Staley JT, JA Fuerst (2017)

Ancient, highly conserved proteins from a LUCA with complex cell biology provide evidence in support of the nuclear compartment commonality (NuCom) hypothesis.

Research in microbiology, 168(5):395-412.

The nuclear compartment commonality (NuCom) hypothesis posits a complex last common ancestor (LUCA) with membranous compartments including a nuclear membrane. Such a LUCA then evolved to produce two nucleated lineages of the tree of life: the Planctomycetes-Verrucomicrobia-Chlamydia superphylum (PVC) within the Bacteria, and the Eukarya. We propose that a group of ancient essential protokaryotic signature proteins (PSPs) originating in LUCA were incorporated into ancestors of PVC Bacteria and Eukarya. Tubulins, ubiquitin system enzymes and sterol-synthesizing enzymes are consistent with early origins of these features shared between the PVC superphylum and Eukarya.

RevDate: 2018-07-16
CmpDate: 2017-07-24

Domazet-Lošo T, Carvunis AR, Albà MM, et al (2017)

No Evidence for Phylostratigraphic Bias Impacting Inferences on Patterns of Gene Emergence and Evolution.

Molecular biology and evolution, 34(4):843-856.

Phylostratigraphy is a computational framework for dating the emergence of DNA and protein sequences in a phylogeny. It has been extensively applied to make inferences on patterns of genome evolution, including patterns of disease gene evolution, ontogeny and de novo gene origination. Phylostratigraphy typically relies on BLAST searches along a species tree, but new simulation studies have raised concerns about the ability of BLAST to detect remote homologues and its impact on phylostratigraphic inferences. Here, we re-assessed these simulations. We found that, even with a possible overall BLAST false negative rate between 11-15%, the large majority of sequences assigned to a recent evolutionary origin by phylostratigraphy is unaffected by technical concerns about BLAST. Where the results of the simulations did cast doubt on previously reported findings, we repeated the original analyses but now excluded all questionable sequences. The originally described patterns remained essentially unchanged. These new analyses strongly support phylostratigraphic inferences, including: genes that emerged after the origin of eukaryotes are more likely to be expressed in the ectoderm than in the endoderm or mesoderm in Drosophila, and the de novo emergence of protein-coding genes from non-genic sequences occurs through proto-gene intermediates in yeast. We conclude that BLAST is an appropriate and sufficiently sensitive tool in phylostratigraphic analysis that does not appear to introduce significant biases into evolutionary pattern inferences.

RevDate: 2018-06-21
CmpDate: 2017-07-31

Nasir A, Kim KM, Da Cunha V, et al (2016)

Arguments Reinforcing the Three-Domain View of Diversified Cellular Life.

Archaea (Vancouver, B.C.), 2016:1851865.

The archaeal ancestor scenario (AAS) for the origin of eukaryotes implies the emergence of a new kind of organism from the fusion of ancestral archaeal and bacterial cells. Equipped with this "chimeric" molecular arsenal, the resulting cell would gradually accumulate unique genes and develop the complex molecular machineries and cellular compartments that are hallmarks of modern eukaryotes. In this regard, proteins related to phagocytosis and cell movement should be present in the archaeal ancestor, thus identifying the recently described candidate archaeal phylum "Lokiarchaeota" as resembling a possible candidate ancestor of eukaryotes. Despite its appeal, AAS seems incompatible with the genomic, molecular, and biochemical differences that exist between Archaea and Eukarya. In particular, the distribution of conserved protein domain structures in the proteomes of cellular organisms and viruses appears hard to reconcile with the AAS. In addition, concerns related to taxon and character sampling, presupposing bacterial outgroups in phylogenies, and nonuniform effects of protein domain structure rearrangement and gain/loss in concatenated alignments of protein sequences cast further doubt on AAS-supporting phylogenies. Here, we evaluate AAS against the traditional "three-domain" world of cellular organisms and propose that the discovery of Lokiarchaeota could be better reconciled under the latter view, especially in light of several additional biological and technical considerations.

RevDate: 2018-03-15
CmpDate: 2018-03-15

Kutschera U (2016)

Haeckel's 1866 tree of life and the origin of eukaryotes.

Nature microbiology, 1(8):16114 pii:nmicrobiol2016114.

RevDate: 2017-04-25
CmpDate: 2017-03-01

Garg SG, WF Martin (2016)

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor.

Genome biology and evolution, 8(6):1950-1970 pii:evw136.

Theories for the origin of sex traditionally start with an asexual mitosing cell and add recombination, thereby deriving meiosis from mitosis. Though sex was clearly present in the eukaryote common ancestor, the order of events linking the origin of sex and the origin of mitosis is unknown. Here, we present an evolutionary inference for the origin of sex starting with a bacterial ancestor of mitochondria in the cytosol of its archaeal host. We posit that symbiotic association led to the origin of mitochondria and gene transfer to host's genome, generating a nucleus and a dedicated translational compartment, the eukaryotic cytosol, in which-by virtue of mitochondria-metabolic energy was not limiting. Spontaneous protein aggregation (monomer polymerization) and Adenosine Tri-phosphate (ATP)-dependent macromolecular movement in the cytosol thereby became selectable, giving rise to continuous microtubule-dependent chromosome separation (reduction division). We propose that eukaryotic chromosome division arose in a filamentous, syncytial, multinucleated ancestor, in which nuclei with insufficient chromosome numbers could complement each other through mRNA in the cytosol and generate new chromosome combinations through karyogamy. A syncytial (or coenocytic, a synonym) eukaryote ancestor, or Coeca, would account for the observation that the process of eukaryotic chromosome separation is more conserved than the process of eukaryotic cell division. The first progeny of such a syncytial ancestor were likely equivalent to meiospores, released into the environment by the host's vesicle secretion machinery. The natural ability of archaea (the host) to fuse and recombine brought forth reciprocal recombination among fusing (syngamy and karyogamy) progeny-sex-in an ancestrally meiotic cell cycle, from which the simpler haploid and diploid mitotic cell cycles arose. The origin of eukaryotes was the origin of vertical lineage inheritance, and sex was required to keep vertically evolving lineages viable by rescuing the incipient eukaryotic lineage from Muller's ratchet. The origin of mitochondria was, in this view, the decisive incident that precipitated symbiosis-specific cell biological problems, the solutions to which were the salient features that distinguish eukaryotes from prokaryotes: A nuclear membrane, energetically affordable ATP-dependent protein-protein interactions in the cytosol, and a cell cycle involving reduction division and reciprocal recombination (sex).

RevDate: 2018-03-26
CmpDate: 2017-12-13

Markov AV, IS Kaznacheev (2016)

Evolutionary consequences of polyploidy in prokaryotes and the origin of mitosis and meiosis.

Biology direct, 11:28 pii:10.1186/s13062-016-0131-8.

BACKGROUND: The origin of eukaryote-specific traits such as mitosis and sexual reproduction remains disputable. There is growing evidence that both mitosis and eukaryotic sex (i.e., the alternation of syngamy and meiosis) may have already existed in the basal eukaryotes. The mating system of the halophilic archaeon Haloferax volcanii probably represents an intermediate stage between typical prokaryotic and eukaryotic sex. H. volcanii is highly polyploid, as well as many other Archaea. Here, we use computer simulation to explore genetic and evolutionary outcomes of polyploidy in amitotic prokaryotes and its possible role in the origin of mitosis, meiosis and eukaryotic sex.

RESULTS: Modeling suggests that polyploidy can confer strong short-term evolutionary advantage to amitotic prokaryotes. However, it also promotes the accumulation of recessive deleterious mutations and the risk of extinction in the long term, especially in highly mutagenic environment. There are several possible strategies that amitotic polyploids can use in order to reduce the genetic costs of polyploidy while retaining its benefits. Interestingly, most of these strategies resemble different components or aspects of eukaryotic sex. They include asexual ploidy cycles, equalization of genome copies by gene conversion, high-frequency lateral gene transfer between relatives, chromosome exchange coupled with homologous recombination, and the evolution of more accurate chromosome distribution during cell division (mitosis). Acquisition of mitosis by an amitotic polyploid results in chromosome diversification and specialization. Ultimately, it transforms a polyploid cell into a functionally monoploid one with multiple unique, highly redundant chromosomes. Specialization of chromosomes makes the previously evolved modes of promiscuous chromosome shuffling deleterious. This can result in selective pressure to develop accurate mechanisms of homolog pairing, and, ultimately, meiosis.

CONCLUSION: Emergence of mitosis and the first evolutionary steps towards eukaryotic sex could have taken place in the ancestral polyploid, amitotic proto-eukaryotes, as they were struggling to survive in the highly mutagenic environment of the Early Proterozoic shallow water microbial communities, through the succession of the following stages: (1) acquisition of high-frequency between-individual genetic exchange coupled with homologous recombination; (2) acquisition of mitosis, followed by rapid chromosome diversification and specialization; (3) evolution of homolog synapsis and meiosis. Additional evidence compatible with this scenario includes mass acquisition of new families of paralogous genes by the basal eukaryotes, and recently discovered correlation between polyploidy and the presence of histones in Archaea.

REVIEWER: This article was reviewed by Eugene Koonin, Uri Gophna and Armen Mulkidjanian. For the full reviews, please go to the Reviewers' comments section.

RevDate: 2018-01-03
CmpDate: 2017-09-01

Radzvilavicius AL (2016)

Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes.

Journal of theoretical biology, 404:160-168.

Sexual reproduction is a trait shared by all complex life, but the complete account of its origin is missing. Virtually all theoretical work on the evolution of sex has been centered around the benefits of reciprocal recombination among nuclear genes, paying little attention to the evolutionary dynamics of multi-copy mitochondrial genomes. Here I develop a mathematical model to study the evolution of nuclear alleles inducing cell fusion in an ancestral population of clonal proto-eukaryotes. Segregational drift maintains high mitochondrial variance between clonally reproducing hosts, but the effect of segregation is opposed by cytoplasmic mixing which tends to reduce variation between cells in favor of higher heterogeneity within the cell. Despite the reduced long-term population fitness, alleles responsible for sexual cell fusion can spread to fixation. The evolution of sex requires negative epistatic interactions between mitochondrial mutations under strong purifying selection, low mutation load and weak mitochondrial-nuclear associations. I argue that similar conditions could have been maintained during the late stages of eukaryogenesis, facilitating the evolution of sexual cell fusion and meiotic recombination without compromising the stability of the emerging complex cell.

RevDate: 2017-02-20
CmpDate: 2016-04-30

Blackstone NW (2016)

An Evolutionary Framework for Understanding the Origin of Eukaryotes.

Biology, 5(2): pii:biology5020018.

Two major obstacles hinder the application of evolutionary theory to the origin of eukaryotes. The first is more apparent than real-the endosymbiosis that led to the mitochondrion is often described as "non-Darwinian" because it deviates from the incremental evolution championed by the modern synthesis. Nevertheless, endosymbiosis can be accommodated by a multi-level generalization of evolutionary theory, which Darwin himself pioneered. The second obstacle is more serious-all of the major features of eukaryotes were likely present in the last eukaryotic common ancestor thus rendering comparative methods ineffective. In addition to a multi-level theory, the development of rigorous, sequence-based phylogenetic and comparative methods represents the greatest achievement of modern evolutionary theory. Nevertheless, the rapid evolution of major features in the eukaryotic stem group requires the consideration of an alternative framework. Such a framework, based on the contingent nature of these evolutionary events, is developed and illustrated with three examples: the putative intron proliferation leading to the nucleus and the cell cycle; conflict and cooperation in the origin of eukaryotic bioenergetics; and the inter-relationship between aerobic metabolism, sterol synthesis, membranes, and sex. The modern synthesis thus provides sufficient scope to develop an evolutionary framework to understand the origin of eukaryotes.

RevDate: 2017-12-20
CmpDate: 2017-07-12

Surkont J, JB Pereira-Leal (2016)

Are There Rab GTPases in Archaea?.

Molecular biology and evolution, 33(7):1833-1842.

A complex endomembrane system is one of the hallmarks of Eukaryotes. Vesicle trafficking between compartments is controlled by a diverse protein repertoire, including Rab GTPases. These small GTP-binding proteins contribute identity and specificity to the system, and by working as molecular switches, trigger multiple events in vesicle budding, transport, and fusion. A diverse collection of Rab GTPases already existed in the ancestral Eukaryote, yet, it is unclear how such elaborate repertoire emerged. A novel archaeal phylum, the Lokiarchaeota, revealed that several eukaryotic-like protein systems, including small GTPases, are present in Archaea. Here, we test the hypothesis that the Rab family of small GTPases predates the origin of Eukaryotes. Our bioinformatic pipeline detected multiple putative Rab-like proteins in several archaeal species. Our analyses revealed the presence and strict conservation of sequence features that distinguish eukaryotic Rabs from other small GTPases (Rab family motifs), mapping to the same regions in the structure as in eukaryotic Rabs. These mediate Rab-specific interactions with regulators of the REP/GDI (Rab Escort Protein/GDP dissociation Inhibitor) family. Sensitive structure-based methods further revealed the existence of REP/GDI-like genes in Archaea, involved in isoprenyl metabolism. Our analysis supports a scenario where Rabs differentiated into an independent family in Archaea, interacting with proteins involved in membrane biogenesis. These results further support the archaeal nature of the eukaryotic ancestor and provide a new insight into the intermediate stages and the evolutionary path toward the complex membrane-associated signaling circuits that characterize the Ras superfamily of small GTPases, and specifically Rab proteins.

RevDate: 2017-09-22
CmpDate: 2016-03-21

Pittis AA, T Gabaldón (2016)

Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry.

Nature, 531(7592):101-104.

The origin of eukaryotes stands as a major conundrum in biology. Current evidence indicates that the last eukaryotic common ancestor already possessed many eukaryotic hallmarks, including a complex subcellular organization. In addition, the lack of evolutionary intermediates challenges the elucidation of the relative order of emergence of eukaryotic traits. Mitochondria are ubiquitous organelles derived from an alphaproteobacterial endosymbiont. Different hypotheses disagree on whether mitochondria were acquired early or late during eukaryogenesis. Similarly, the nature and complexity of the receiving host are debated, with models ranging from a simple prokaryotic host to an already complex proto-eukaryote. Most competing scenarios can be roughly grouped into either mito-early, which consider the driving force of eukaryogenesis to be mitochondrial endosymbiosis into a simple host, or mito-late, which postulate that a significant complexity predated mitochondrial endosymbiosis. Here we provide evidence for late mitochondrial endosymbiosis. We use phylogenomics to directly test whether proto-mitochondrial proteins were acquired earlier or later than other proteins of the last eukaryotic common ancestor. We find that last eukaryotic common ancestor protein families of alphaproteobacterial ancestry and of mitochondrial localization show the shortest phylogenetic distances to their closest prokaryotic relatives, compared with proteins of different prokaryotic origin or cellular localization. Altogether, our results shed new light on a long-standing question and provide compelling support for the late acquisition of mitochondria into a host that already had a proteome of chimaeric phylogenetic origin. We argue that mitochondrial endosymbiosis was one of the ultimate steps in eukaryogenesis and that it provided the definitive selective advantage to mitochondria-bearing eukaryotes over less complex forms.

RevDate: 2018-02-27
CmpDate: 2016-06-23

López-García P, D Moreira (2015)

Open Questions on the Origin of Eukaryotes.

Trends in ecology & evolution, 30(11):697-708.

Despite recent progress, the origin of the eukaryotic cell remains enigmatic. It is now known that the last eukaryotic common ancestor was complex and that endosymbiosis played a crucial role in eukaryogenesis at least via the acquisition of the alphaproteobacterial ancestor of mitochondria. However, the nature of the mitochondrial host is controversial, although the recent discovery of an archaeal lineage phylogenetically close to eukaryotes reinforces models proposing archaea-derived hosts. We argue that, in addition to improved phylogenomic analyses with more comprehensive taxon sampling to pinpoint the closest prokaryotic relatives of eukaryotes, determining plausible mechanisms and selective forces at the origin of key eukaryotic features, such as the nucleus or the bacterial-like eukaryotic membrane system, is essential to constrain existing models.

RevDate: 2017-02-20
CmpDate: 2016-07-06

Koonin EV (2015)

Archaeal ancestors of eukaryotes: not so elusive any more.

BMC biology, 13:84 pii:10.1186/s12915-015-0194-5.

The origin of eukaryotes is one of the hardest problems in evolutionary biology and sometimes raises the ominous specter of irreducible complexity. Reconstruction of the gene repertoire of the last eukaryotic common ancestor (LECA) has revealed a highly complex organism with a variety of advanced features but no detectable evolutionary intermediates to explain their origin. Recently, however, genome analysis of diverse archaea led to the discovery of apparent ancestral versions of several signature eukaryotic systems, such as the actin cytoskeleton and the ubiquitin network, that are scattered among archaea. These findings inspired the hypothesis that the archaeal ancestor of eukaryotes was an unusually complex form with an elaborate intracellular organization. The latest striking discovery made by deep metagenomic sequencing vindicates this hypothesis by showing that in phylogenetic trees eukaryotes fall within a newly identified archaeal group, the Lokiarchaeota, which combine several eukaryotic signatures previously identified in different archaea. The discovery of complex archaea that are the closest living relatives of eukaryotes is most compatible with the symbiogenetic scenario for eukaryogenesis.

RevDate: 2017-10-07
CmpDate: 2017-04-06

Scheid P (2015)

Viruses in close associations with free-living amoebae.

Parasitology research, 114(11):3959-3967.

As both groups of organisms, free-living amoebae (FLA) and viruses, can be found in aquatic environments side by side, it appears obvious that there are multiple interactions with respect to host-endocytobiont relationships. Several relationships between viruses and protozoan hosts are described and it was the discovery of the so called "giant viruses," associated with amoebae, which gave another dimension to these interactions. Mimiviruses, Pandoraviruses and Pithoviruses are examples for interesting viral endocytobionts within FLA. In the Mimivirus viral factories, viral DNA undergoes replication and transcription, and the DNA is prepared to be packed in procapsids. Theses Mimivirus factories can be considered as efficient "production lines" where, at any given moment, all stages of viral generation including membrane biogenesis, capsid assembly and genome encapsidation, are occurring concomitantly. There are some hints that similar replication factories are involved as well during the Pandoravirus development. Some scientists favour the assumption that the giant viruses have received many of their genes from their hosts or from sympatric occurring endocytobionts via lateral gene transfer. This hypothesis would mean that this type of transfer has been an important process in the evolution of genomes in the context of the intracellular parasitic or endocytobiotic lifestyle. In turn, that would migitate against hypothesizing development of a new branch in the tree of life. Based on the described scenarios to explain the presence of genes related to translation, it is also possible that earlier ancestors of today's DNA viruses were involved in the origin of eukaryotes. That possibly could in turn support the idea that cellular organisms could have evolved from viruses with growing autarkic properties. In future we expect the discovery of further (giant) viruses within free-living amoebae and other protozoa through genomic, transcriptomic and proteomic analyses.

RevDate: 2017-02-20
CmpDate: 2016-06-03

Koonin EV (2015)

Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier?.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 370(1678):20140333.

The origin of eukaryotes is a fundamental, forbidding evolutionary puzzle. Comparative genomic analysis clearly shows that the last eukaryotic common ancestor (LECA) possessed most of the signature complex features of modern eukaryotic cells, in particular the mitochondria, the endomembrane system including the nucleus, an advanced cytoskeleton and the ubiquitin network. Numerous duplications of ancestral genes, e.g. DNA polymerases, RNA polymerases and proteasome subunits, also can be traced back to the LECA. Thus, the LECA was not a primitive organism and its emergence must have resulted from extensive evolution towards cellular complexity. However, the scenario of eukaryogenesis, and in particular the relationship between endosymbiosis and the origin of eukaryotes, is far from being clear. Four recent developments provide new clues to the likely routes of eukaryogenesis. First, evolutionary reconstructions suggest complex ancestors for most of the major groups of archaea, with the subsequent evolution dominated by gene loss. Second, homologues of signature eukaryotic proteins, such as actin and tubulin that form the core of the cytoskeleton or the ubiquitin system, have been detected in diverse archaea. The discovery of this 'dispersed eukaryome' implies that the archaeal ancestor of eukaryotes was a complex cell that might have been capable of a primitive form of phagocytosis and thus conducive to endosymbiont capture. Third, phylogenomic analyses converge on the origin of most eukaryotic genes of archaeal descent from within the archaeal evolutionary tree, specifically, the TACK superphylum. Fourth, evidence has been presented that the origin of the major archaeal phyla involved massive acquisition of bacterial genes. Taken together, these findings make the symbiogenetic scenario for the origin of eukaryotes considerably more plausible and the origin of the organizational complexity of eukaryotic cells more readily explainable than they appeared until recently.

RevDate: 2017-02-20
CmpDate: 2016-06-03

Martin WF, Garg S, V Zimorski (2015)

Endosymbiotic theories for eukaryote origin.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 370(1678):20140330.

For over 100 years, endosymbiotic theories have figured in thoughts about the differences between prokaryotic and eukaryotic cells. More than 20 different versions of endosymbiotic theory have been presented in the literature to explain the origin of eukaryotes and their mitochondria. Very few of those models account for eukaryotic anaerobes. The role of energy and the energetic constraints that prokaryotic cell organization placed on evolutionary innovation in cell history has recently come to bear on endosymbiotic theory. Only cells that possessed mitochondria had the bioenergetic means to attain eukaryotic cell complexity, which is why there are no true intermediates in the prokaryote-to-eukaryote transition. Current versions of endosymbiotic theory have it that the host was an archaeon (an archaebacterium), not a eukaryote. Hence the evolutionary history and biology of archaea increasingly comes to bear on eukaryotic origins, more than ever before. Here, we have compiled a survey of endosymbiotic theories for the origin of eukaryotes and mitochondria, and for the origin of the eukaryotic nucleus, summarizing the essentials of each and contrasting some of their predictions to the observations. A new aspect of endosymbiosis in eukaryote evolution comes into focus from these considerations: the host for the origin of plastids was a facultative anaerobe.

RevDate: 2017-09-22
CmpDate: 2016-06-03

Saw JH, Spang A, Zaremba-Niedzwiedzka K, et al (2015)

Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 370(1678):20140328.

The origin of eukaryotes represents an enigmatic puzzle, which is still lacking a number of essential pieces. Whereas it is currently accepted that the process of eukaryogenesis involved an interplay between a host cell and an alphaproteobacterial endosymbiont, we currently lack detailed information regarding the identity and nature of these players. A number of studies have provided increasing support for the emergence of the eukaryotic host cell from within the archaeal domain of life, displaying a specific affiliation with the archaeal TACK superphylum. Recent studies have shown that genomic exploration of yet-uncultivated archaea, the so-called archaeal 'dark matter', is able to provide unprecedented insights into the process of eukaryogenesis. Here, we provide an overview of state-of-the-art cultivation-independent approaches, and demonstrate how these methods were used to obtain draft genome sequences of several novel members of the TACK superphylum, including Lokiarchaeum, two representatives of the Miscellaneous Crenarchaeotal Group (Bathyarchaeota), and a Korarchaeum-related lineage. The maturation of cultivation-independent genomics approaches, as well as future developments in next-generation sequencing technologies, will revolutionize our current view of microbial evolution and diversity, and provide profound new insights into the early evolution of life, including the enigmatic origin of the eukaryotic cell.

RevDate: 2017-09-22
CmpDate: 2016-06-03

Moreira D, P López-García (2015)

Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes?.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 370(1678):20140327.

The recent discovery of diverse very large viruses, such as the mimivirus, has fostered a profusion of hypotheses positing that these viruses define a new domain of life together with the three cellular ones (Archaea, Bacteria and Eucarya). It has also been speculated that they have played a key role in the origin of eukaryotes as donors of important genes or even as the structures at the origin of the nucleus. Thanks to the increasing availability of genome sequences for these giant viruses, those hypotheses are amenable to testing via comparative genomic and phylogenetic analyses. This task is made very difficult by the high evolutionary rate of viruses, which induces phylogenetic artefacts, such as long branch attraction, when inadequate methods are applied. It can be demonstrated that phylogenetic trees supporting viruses as a fourth domain of life are artefactual. In most cases, the presence of homologues of cellular genes in viruses is best explained by recurrent horizontal gene transfer from cellular hosts to their infecting viruses and not the opposite. Today, there is no solid evidence for the existence of a viral domain of life or for a significant implication of viruses in the origin of the cellular domains.

RevDate: 2015-08-07
CmpDate: 2016-04-26

Nasir A, Kim KM, G Caetano-Anollés (2015)

Lokiarchaeota: eukaryote-like missing links from microbial dark matter?.

Trends in microbiology, 23(8):448-450.

Identification and genome sequencing of novel organismal groups can reduce the gap between the sequenced minority and the unexplored majority. The recent discovery of phylum Lokiarchaeota promises understanding of biological history. Here we inquire if Lokiarchaeota truly represent ancient eukaryotic ancestors or just microbial dark matter of expanding archaeal diversity.

RevDate: 2015-04-20
CmpDate: 2016-02-08

Hooper SL, HJ Burstein (2015)

Erratum to: Minimization of extracellular space as a driving force in prokaryote association and the origin of eukaryotes.

Biology direct, 10:11 pii:10.1186/s13062-015-0037-x.

Following the publication of this article [1] it was noticed that, due to an error on the part of the publisher, the 2nd round of comments submitted by Reviewer 1, Dr. López-García, were unintentionally omitted during the peer review process. As a consequence of this error, the authors were unable to reply to Dr. López-García's comments and subsequently revise their manuscript accordingly (where appropriate).In fairness to both the authors and reviewer, Dr. López-García's (Reviewer 1) 2nd round of comments are now included below and Scott L Hooper and Helaine J Burstein (author) were given the opportunity to reply. Any consequent amendments to the research article [1] are outlined in the author's replies.

RevDate: 2017-09-22
CmpDate: 2016-03-09

Grau-Bové X, Sebé-Pedrós A, I Ruiz-Trillo (2015)

The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin.

Molecular biology and evolution, 32(3):726-739.

The origin of the eukaryotic cell is one of the most important transitions in the history of life. However, the emergence and early evolution of eukaryotes remains poorly understood. Recent data have shown that the last eukaryotic common ancestor (LECA) was much more complex than previously thought. The LECA already had the genetic machinery encoding the endomembrane apparatus, spliceosome, nuclear pore, and myosin and kinesin cytoskeletal motors. It is unclear, however, when the functional regulation of these cellular components evolved. Here, we address this question by analyzing the origin and evolution of the ubiquitin (Ub) signaling system, one of the most important regulatory layers in eukaryotes. We delineated the evolution of the whole Ub, Small-Ub-related MOdifier (SUMO), and Ub-fold modifier 1 (Ufm1) signaling networks by analyzing representatives from all major eukaryotic, bacterial, and archaeal lineages. We found that the Ub toolkit had a pre-eukaryotic origin and is present in three extant archaeal groups. The pre-eukaryotic Ub toolkit greatly expanded during eukaryogenesis, through massive gene innovation and diversification of protein domain architectures. This resulted in a LECA with essentially all of the Ub-related genes, including the SUMO and Ufm1 Ub-like systems. Ub and SUMO signaling further expanded during eukaryotic evolution, especially labeling and delabeling enzymes responsible for substrate selection. Additionally, we analyzed protein domain architecture evolution and found that multicellular lineages have the most complex Ub systems in terms of domain architectures. Together, we demonstrate that the Ub system predates the origin of eukaryotes and that a burst of innovation during eukaryogenesis led to a LECA with complex posttranslational regulation.

RevDate: 2017-02-20
CmpDate: 2015-07-08

Hooper SL, HJ Burstein (2014)

Minimization of extracellular space as a driving force in prokaryote association and the origin of eukaryotes.

Biology direct, 9(1):24 pii:1745-6150-9-24.

BACKGROUND: Internalization-based hypotheses of eukaryotic origin require close physical association of host and symbiont. Prior hypotheses of how these associations arose include chance, specific metabolic couplings between partners, and prey-predator/parasite interactions. Since these hypotheses were proposed, it has become apparent that mixed-species, close-association assemblages (biofilms) are widespread and predominant components of prokaryotic ecology. Which forces drove prokaryotes to evolve the ability to form these assemblages are uncertain. Bacteria and archaea have also been found to form membrane-lined interconnections (nanotubes) through which proteins and RNA pass. These observations, combined with the structure of the nuclear envelope and an energetic benefit of close association (see below), lead us to propose a novel hypothesis of the driving force underlying prokaryotic close association and the origin of eukaryotes.

RESULTS: Respiratory proton transport does not alter external pH when external volume is effectively infinite. Close physical association decreases external volume. For small external volumes, proton transport decreases external pH, resulting in each transported proton increasing proton motor force to a greater extent. We calculate here that in biofilms this effect could substantially decrease how many protons need to be transported to achieve a given proton motor force. Based as it is solely on geometry, this energetic benefit would occur for all prokaryotes using proton-based respiration.

CONCLUSIONS: This benefit may be a driving force in biofilm formation. Under this hypothesis a very wide range of prokaryotic species combinations could serve as eukaryotic progenitors. We use this observation and the discovery of prokaryotic nanotubes to propose that eukaryotes arose from physically distinct, functionally specialized (energy factory, protein factory, DNA repository/RNA factory), obligatorily symbiotic prokaryotes in which the protein factory and DNA repository/RNA factory cells were coupled by nanotubes and the protein factory ultimately internalized the other two. This hypothesis naturally explains many aspects of eukaryotic physiology, including the nuclear envelope being a folded single membrane repeatedly pierced by membrane-bound tubules (the nuclear pores), suggests that species analogous or homologous to eukaryotic progenitors are likely unculturable as monocultures, and makes a large number of testable predictions.

REVIEWERS: This article was reviewed by Purificación López-García and Toni Gabaldón.

RevDate: 2017-02-20
CmpDate: 2015-05-15

Cavalier-Smith T (2014)

The neomuran revolution and phagotrophic origin of eukaryotes and cilia in the light of intracellular coevolution and a revised tree of life.

Cold Spring Harbor perspectives in biology, 6(9):a016006 pii:6/9/a016006.

Three kinds of cells exist with increasingly complex membrane-protein targeting: Unibacteria (Archaebacteria, Posibacteria) with one cytoplasmic membrane (CM); Negibacteria with a two-membrane envelope (inner CM; outer membrane [OM]); eukaryotes with a plasma membrane and topologically distinct endomembranes and peroxisomes. I combine evidence from multigene trees, palaeontology, and cell biology to show that eukaryotes and archaebacteria are sisters, forming the clade neomura that evolved ~1.2 Gy ago from a posibacterium, whose DNA segregation and cell division were destabilized by murein wall loss and rescued by the evolving novel neomuran endoskeleton, histones, cytokinesis, and glycoproteins. Phagotrophy then induced coevolving serial major changes making eukaryote cells, culminating in two dissimilar cilia via a novel gliding-fishing-swimming scenario. I transfer Chloroflexi to Posibacteria, root the universal tree between them and Heliobacteria, and argue that Negibacteria are a clade whose OM, evolving in a green posibacterium, was never lost.

RevDate: 2017-02-20
CmpDate: 2015-03-30

Aravind L, Burroughs AM, Zhang D, et al (2014)

Protein and DNA modifications: evolutionary imprints of bacterial biochemical diversification and geochemistry on the provenance of eukaryotic epigenetics.

Cold Spring Harbor perspectives in biology, 6(7):a016063 pii:6/7/a016063.

Epigenetic information, which plays a major role in eukaryotic biology, is transmitted by covalent modifications of nuclear proteins (e.g., histones) and DNA, along with poorly understood processes involving cytoplasmic/secreted proteins and RNAs. The origin of eukaryotes was accompanied by emergence of a highly developed biochemical apparatus for encoding, resetting, and reading covalent epigenetic marks in proteins such as histones and tubulins. The provenance of this apparatus remained unclear until recently. Developments in comparative genomics show that key components of eukaryotic epigenetics emerged as part of the extensive biochemical innovation of secondary metabolism and intergenomic/interorganismal conflict systems in prokaryotes, particularly bacteria. These supplied not only enzymatic components for encoding and removing epigenetic modifications, but also readers of some of these marks. Diversification of these prokaryotic systems and subsequently eukaryotic epigenetics appear to have been considerably influenced by the great oxygenation event in the Earth's history.

RevDate: 2014-08-12
CmpDate: 2015-04-07

Chatre L, M Ricchetti (2014)

Are mitochondria the Achilles' heel of the Kingdom Fungi?.

Current opinion in microbiology, 20:49-54.

A founding event in the origin of eukaryotes is the acquisition of an extraordinary organelle, the mitochondrion, which contains its own genome. Being linked to energy metabolism, oxidative stress, cell signalling, and cell death, the mitochondrion to a certain extent controls life and death in eukaryotic cells. The large metabolic diversity and living strategies of the Kingdom Fungi make their mitochondria of particular evolutionary interest. The review focuses first on the characteristics of mitochondria in the Kingdom Fungi, then on their implications in the organism survival, pathogenicity and resistance, and finally on proposing unconventional strategies to investigate the biology of fungal mitochondria, unveiling the possibility that mitochondria play as the Achilles' heel of this kingdom.

RevDate: 2017-02-20
CmpDate: 2015-03-10

Koonin EV (2014)

Carl Woese's vision of cellular evolution and the domains of life.

RNA biology, 11(3):197-204.

In a series of conceptual articles published around the millennium, Carl Woese emphasized that evolution of cells is the central problem of evolutionary biology, that the three-domain ribosomal tree of life is an essential framework for reconstructing cellular evolution, and that the evolutionary dynamics of functionally distinct cellular systems are fundamentally different, with the information processing systems "crystallizing" earlier than operational systems. The advances of evolutionary genomics over the last decade vindicate major aspects of Woese's vision. Despite the observations of pervasive horizontal gene transfer among bacteria and archaea, the ribosomal tree of life comes across as a central statistical trend in the "forest" of phylogenetic trees of individual genes, and hence, an appropriate scaffold for evolutionary reconstruction. The evolutionary stability of information processing systems, primarily translation, becomes ever more striking with the accumulation of comparative genomic data indicating that nearly all of the few universal genes encode translation system components. Woese's view on the fundamental distinctions between the three domains of cellular life also withstand the test of comparative genomics, although his non-acceptance of symbiogenetic scenarios for the origin of eukaryotes might not. Above all, Woese's key prediction that understanding evolution of microbes will be the core of the new evolutionary biology appears to be materializing.

RevDate: 2017-09-22
CmpDate: 2014-10-28

Williams TA, TM Embley (2014)

Archaeal "dark matter" and the origin of eukaryotes.

Genome biology and evolution, 6(3):474-481.

Current hypotheses about the history of cellular life are mainly based on analyses of cultivated organisms, but these represent only a small fraction of extant biodiversity. The sequencing of new environmental lineages therefore provides an opportunity to test, revise, or reject existing ideas about the tree of life and the origin of eukaryotes. According to the textbook three domains hypothesis, the eukaryotes emerge as the sister group to a monophyletic Archaea. However, recent analyses incorporating better phylogenetic models and an improved sampling of the archaeal domain have generally supported the competing eocyte hypothesis, in which core genes of eukaryotic cells originated from within the Archaea, with important implications for eukaryogenesis. Given this trend, it was surprising that a recent analysis incorporating new genomes from uncultivated Archaea recovered a strongly supported three domains tree. Here, we show that this result was due in part to the use of a poorly fitting phylogenetic model and also to the inclusion by an automated pipeline of genes of putative bacterial origin rather than nucleocytosolic versions for some of the eukaryotes analyzed. When these issues were resolved, analyses including the new archaeal lineages placed core eukaryotic genes within the Archaea. These results are consistent with a number of recent studies in which improved archaeal sampling and better phylogenetic models agree in supporting the eocyte tree over the three domains hypothesis.

RevDate: 2017-02-20
CmpDate: 2014-09-29

Keeling PJ (2014)

The impact of history on our perception of evolutionary events: endosymbiosis and the origin of eukaryotic complexity.

Cold Spring Harbor perspectives in biology, 6(2): pii:6/2/a016196.

Evolutionary hypotheses are correctly interpreted as products of the data they set out to explain, but they are less often recognized as being heavily influenced by other factors. One of these is the history of preceding thought, and here I look back on historically important changes in our thinking about the role of endosymbiosis in the origin of eukaryotic cells. Specifically, the modern emphasis on endosymbiotic explanations for numerous eukaryotic features, including the cell itself (the so-called chimeric hypotheses), can be seen not only as resulting from the advent of molecular and genomic data, but also from the intellectual acceptance of the endosymbiotic origin of mitochondria and plastids. This transformative idea may have unduly affected how other aspects of the eukaryotic cell are explained, in effect priming us to accept endosymbiotic explanations for endogenous processes. Molecular and genomic data, which were originally harnessed to answer questions about cell evolution, now so dominate our thinking that they largely define the question, and the original questions about how eukaryotic cellular architecture evolved have been neglected. This is unfortunate because, as Roger Stanier pointed out, these cellular changes represent life's "greatest single evolutionary discontinuity," and on this basis I advocate a return to emphasizing evolutionary cell biology when thinking about the origin of eukaryotes, and suggest that endogenous explanations will prevail when we refocus on the evolution of the cell.

RevDate: 2017-02-20
CmpDate: 2014-09-29

Guo M, Zhou Q, Zhou Y, et al (2014)

Genomic evolution of 11 type strains within family Planctomycetaceae.

PloS one, 9(1):e86752 pii:PONE-D-13-29164.

The species in family Planctomycetaceae are ideal groups for investigating the origin of eukaryotes. Their cells are divided by a lipidic intracytoplasmic membrane and they share a number of eukaryote-like molecular characteristics. However, their genomic structures, potential abilities, and evolutionary status are still unknown. In this study, we searched for common protein families and a core genome/pan genome based on 11 sequenced species in family Planctomycetaceae. Then, we constructed phylogenetic tree based on their 832 common protein families. We also annotated the 11 genomes using the Clusters of Orthologous Groups database. Moreover, we predicted and reconstructed their core/pan metabolic pathways using the KEGG (Kyoto Encyclopedia of Genes and Genomes) orthology system. Subsequently, we identified genomic islands (GIs) and structural variations (SVs) among the five complete genomes and we specifically investigated the integration of two Planctomycetaceae plasmids in all 11 genomes. The results indicate that Planctomycetaceae species share diverse genomic variations and unique genomic characteristics, as well as have huge potential for human applications.

RevDate: 2017-09-22
CmpDate: 2015-01-05

Sebé-Pedrós A, Grau-Bové X, Richards TA, et al (2014)

Evolution and classification of myosins, a paneukaryotic whole-genome approach.

Genome biology and evolution, 6(2):290-305.

Myosins are key components of the eukaryotic cytoskeleton, providing motility for a broad diversity of cargoes. Therefore, understanding the origin and evolutionary history of myosin classes is crucial to address the evolution of eukaryote cell biology. Here, we revise the classification of myosins using an updated taxon sampling that includes newly or recently sequenced genomes and transcriptomes from key taxa. We performed a survey of eukaryotic genomes and phylogenetic analyses of the myosin gene family, reconstructing the myosin toolkit at different key nodes in the eukaryotic tree of life. We also identified the phylogenetic distribution of myosin diversity in terms of number of genes, associated protein domains and number of classes in each taxa. Our analyses show that new classes (i.e., paralogs) and domain architectures were continuously generated throughout eukaryote evolution, with a significant expansion of myosin abundance and domain architectural diversity at the stem of Holozoa, predating the origin of animal multicellularity. Indeed, single-celled holozoans have the most complex myosin complement among eukaryotes, with paralogs of most myosins previously considered animal specific. We recover a dynamic evolutionary history, with several lineage-specific expansions (e.g., the myosin III-like gene family diversification in choanoflagellates), convergence in protein domain architectures (e.g., fungal and animal chitin synthase myosins), and important secondary losses. Overall, our evolutionary scheme demonstrates that the ancestral eukaryote likely had a complex myosin repertoire that included six genes with different protein domain architectures. Finally, we provide an integrative and robust classification, useful for future genomic and functional studies on this crucial eukaryotic gene family.

RevDate: 2017-02-20
CmpDate: 2014-11-17

Rochette NC, Brochier-Armanet C, M Gouy (2014)

Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes.

Molecular biology and evolution, 31(4):832-845.

The evolutionary origin of eukaryotes is a question of great interest for which many different hypotheses have been proposed. These hypotheses predict distinct patterns of evolutionary relationships for individual genes of the ancestral eukaryotic genome. The availability of numerous completely sequenced genomes covering the three domains of life makes it possible to contrast these predictions with empirical data. We performed a systematic analysis of the phylogenetic relationships of ancestral eukaryotic genes with archaeal and bacterial genes. In contrast with previous studies, we emphasize the critical importance of methods accounting for statistical support, horizontal gene transfer, and gene loss, and we disentangle the processes underlying the phylogenomic pattern we observe. We first recover a clear signal indicating that a fraction of the bacteria-like eukaryotic genes are of alphaproteobacterial origin. Then, we show that the majority of bacteria-related eukaryotic genes actually do not point to a relationship with a specific bacterial taxonomic group. We also provide evidence that eukaryotes branch close to the last archaeal common ancestor. Our results demonstrate that there is no phylogenetic support for hypotheses involving a fusion with a bacterium other than the ancestor of mitochondria. Overall, they leave only two possible interpretations, respectively, based on the early-mitochondria hypotheses, which suppose an early endosymbiosis of an alphaproteobacterium in an archaeal host and on the slow-drip autogenous hypothesis, in which early eukaryotic ancestors were particularly prone to horizontal gene transfers.

RevDate: 2017-02-20
CmpDate: 2014-07-21

Forterre P (2013)

The common ancestor of archaea and eukarya was not an archaeon.

Archaea (Vancouver, B.C.), 2013:372396.

It is often assumed that eukarya originated from archaea. This view has been recently supported by phylogenetic analyses in which eukarya are nested within archaea. Here, I argue that these analyses are not reliable, and I critically discuss archaeal ancestor scenarios, as well as fusion scenarios for the origin of eukaryotes. Based on recognized evolutionary trends toward reduction in archaea and toward complexity in eukarya, I suggest that their last common ancestor was more complex than modern archaea but simpler than modern eukaryotes (the bug in-between scenario). I propose that the ancestors of archaea (and bacteria) escaped protoeukaryotic predators by invading high temperature biotopes, triggering their reductive evolution toward the "prokaryotic" phenotype (the thermoreduction hypothesis). Intriguingly, whereas archaea and eukarya share many basic features at the molecular level, the archaeal mobilome resembles more the bacterial than the eukaryotic one. I suggest that selection of different parts of the ancestral virosphere at the onset of the three domains played a critical role in shaping their respective biology. Eukarya probably evolved toward complexity with the help of retroviruses and large DNA viruses, whereas similar selection pressure (thermoreduction) could explain why the archaeal and bacterial mobilomes somehow resemble each other.

RevDate: 2017-11-10
CmpDate: 2014-01-07

Williams TA, Foster PG, Cox CJ, et al (2013)

An archaeal origin of eukaryotes supports only two primary domains of life.

Nature, 504(7479):231-236.

The discovery of the Archaea and the proposal of the three-domains 'universal' tree, based on ribosomal RNA and core genes mainly involved in protein translation, catalysed new ideas for cellular evolution and eukaryotic origins. However, accumulating evidence suggests that the three-domains tree may be incorrect: evolutionary trees made using newer methods place eukaryotic core genes within the Archaea, supporting hypotheses in which an archaeon participated in eukaryotic origins by founding the host lineage for the mitochondrial endosymbiont. These results provide support for only two primary domains of life--Archaea and Bacteria--because eukaryotes arose through partnership between them.

RevDate: 2017-09-22
CmpDate: 2014-10-23

Bogumil D, Alvarez-Ponce D, Landan G, et al (2014)

Integration of two ancestral chaperone systems into one: the evolution of eukaryotic molecular chaperones in light of eukaryogenesis.

Molecular biology and evolution, 31(2):410-418.

Eukaryotic genomes are mosaics of genes acquired from their prokaryotic ancestors, the eubacterial endosymbiont that gave rise to the mitochondrion and its archaebacterial host. Genomic footprints of the prokaryotic merger at the origin of eukaryotes are still discernable in eukaryotic genomes, where gene expression and function correlate with their prokaryotic ancestry. Molecular chaperones are essential in all domains of life as they assist the functional folding of their substrate proteins and protect the cell against the cytotoxic effects of protein misfolding. Eubacteria and archaebacteria code for slightly different chaperones, comprising distinct protein folding pathways. Here we study the evolution of the eukaryotic protein folding pathways following the endosymbiosis event. A phylogenetic analysis of all 64 chaperones encoded in the Saccharomyces cerevisiae genome revealed 25 chaperones of eubacterial ancestry, 11 of archaebacterial ancestry, 10 of ambiguous prokaryotic ancestry, and 18 that may represent eukaryotic innovations. Several chaperone families (e.g., Hsp90 and Prefoldin) trace their ancestry to only one prokaryote group, while others, such as Hsp40 and Hsp70, are of mixed ancestry, with members contributed from both prokaryotic ancestors. Analysis of the yeast chaperone-substrate interaction network revealed no preference for interaction between chaperones and substrates of the same origin. Our results suggest that the archaebacterial and eubacterial protein folding pathways have been reorganized and integrated into the present eukaryotic pathway. The highly integrated chaperone system of yeast is a manifestation of the central role of chaperone-mediated folding in maintaining cellular fitness. Most likely, both archaebacterial and eubacterial chaperone systems were essential at the very early stages of eukaryogenesis, and the retention of both may have offered new opportunities for expanding the scope of chaperone-mediated folding.

RevDate: 2013-08-23
CmpDate: 2014-04-22

van der Giezen M (2013)

Evolution: one thread to unite them all.

Current biology : CB, 23(16):R679-81.

Mitochondria play import roles in the overall metabolism of eukaryotes. Traditionally, they have played a secondary role to the nucleus in the origin of eukaryotes. However, their relative positions in this crucial event for eukaryotic evolution might be reversed.

RevDate: 2013-11-04
CmpDate: 2014-01-07

Blackstone NW (2013)

Evolution and cell physiology. 2. The evolution of cell signaling: from mitochondria to Metazoa.

American journal of physiology. Cell physiology, 305(9):C909-15.

The history of life is a history of levels-of-selection transitions. Each transition requires mechanisms that mediate conflict among the lower-level units. In the origins of multicellular eukaryotes, cell signaling is one such mechanism. The roots of cell signaling, however, may extend to the previous major transition, the origin of eukaryotes. Energy-converting protomitochondria within a larger cell allowed eukaryotes to transcend the surface-to-volume constraints inherent in the design of prokaryotes. At the same time, however, protomitochondria can selfishly allocate energy to their own replication. Metabolic signaling may have mediated this principal conflict in several ways. Variation of the protomitochondria was constrained by stoichiometry and strong metabolic demand (state 3) exerted by the protoeukaryote. Variation among protoeukaryotes was increased by the sexual stage of the life cycle, triggered by weak metabolic demand (state 4), resulting in stochastic allocation of protomitochondria to daughter cells. Coupled with selection, many selfish protomitochondria could thus be removed from the population. Hence, regulation of states 3 and 4, as, for instance, provided by the CO2/soluble adenylyl cyclase/cAMP pathway in mitochondria, was critical for conflict mediation. Subsequently, as multicellular eukaryotes evolved, metabolic signaling pathways employed by eukaryotes to mediate conflict within cells could now be co-opted into conflict mediation between cells. For example, in some fungi, the CO2/soluble adenylyl cyclase/cAMP pathway regulates the transition from yeast to forms with hyphae. In animals, this pathway regulates the maturation of sperm. While the particular features (sperm and hyphae) are distinct, both may involve between-cell conflicts that required mediation.

RevDate: 2017-02-20
CmpDate: 2014-01-23

Blackstone NW (2013)

Why did eukaryotes evolve only once? Genetic and energetic aspects of conflict and conflict mediation.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 368(1622):20120266 pii:rstb.2012.0266.

According to multi-level theory, evolutionary transitions require mediating conflicts between lower-level units in favour of the higher-level unit. By this view, the origin of eukaryotes and the origin of multicellularity would seem largely equivalent. Yet, eukaryotes evolved only once in the history of life, whereas multicellular eukaryotes have evolved many times. Examining conflicts between evolutionary units and mechanisms that mediate these conflicts can illuminate these differences. Energy-converting endosymbionts that allow eukaryotes to transcend surface-to-volume constraints also can allocate energy into their own selfish replication. This principal conflict in the origin of eukaryotes can be mediated by genetic or energetic mechanisms. Genome transfer diminishes the heritable variation of the symbiont, but requires the de novo evolution of the protein-import apparatus and was opposed by selection for selfish symbionts. By contrast, metabolic signalling is a shared primitive feature of all cells. Redox state of the cytosol is an emergent feature that cannot be subverted by an individual symbiont. Hypothetical scenarios illustrate how metabolic regulation may have mediated the conflicts inherent at different stages in the origin of eukaryotes. Aspects of metabolic regulation may have subsequently been coopted from within-cell to between-cell pathways, allowing multicellularity to emerge repeatedly.

RevDate: 2017-02-20
CmpDate: 2014-01-23

Lane N, Martin WF, Raven JA, et al (2013)

Energy, genes and evolution: introduction to an evolutionary synthesis.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 368(1622):20120253 pii:rstb.2012.0253.

Life is the harnessing of chemical energy in such a way that the energy-harnessing device makes a copy of itself. No energy, no evolution. The 'modern synthesis' of the past century explained evolution in terms of genes, but this is only part of the story. While the mechanisms of natural selection are correct, and increasingly well understood, they do little to explain the actual trajectories taken by life on Earth. From a cosmic perspective-what is the probability of life elsewhere in the Universe, and what are its probable traits?-a gene-based view of evolution says almost nothing. Irresistible geological and environmental changes affected eukaryotes and prokaryotes in very different ways, ones that do not relate to specific genes or niches. Questions such as the early emergence of life, the morphological and genomic constraints on prokaryotes, the singular origin of eukaryotes, and the unique and perplexing traits shared by all eukaryotes but not found in any prokaryote, are instead illuminated by bioenergetics. If nothing in biology makes sense except in the light of evolution, nothing in evolution makes sense except in the light of energetics. This Special Issue of Philosophical Transactions examines the interplay between energy transduction and genome function in the major transitions of evolution, with implications ranging from planetary habitability to human health. We hope that these papers will contribute to a new evolutionary synthesis of energetics and genetics.

RevDate: 2015-04-27
CmpDate: 2013-06-27

Alvarez-Ponce D, Lopez P, Bapteste E, et al (2013)

Gene similarity networks provide tools for understanding eukaryote origins and evolution.

Proceedings of the National Academy of Sciences of the United States of America, 110(17):E1594-603.

The complexity and depth of the relationships between the three domains of life challenge the reliability of phylogenetic methods, encouraging the use of alternative analytical tools. We reconstructed a gene similarity network comprising the proteomes of 14 eukaryotes, 104 prokaryotes, 2,389 viruses and 1,044 plasmids. This network contains multiple signatures of the chimerical origin of Eukaryotes as a fusion of an archaebacterium and a eubacterium that could not have been observed using phylogenetic trees. A number of connected components (gene sets with stronger similarities than expected by chance) contain pairs of eukaryotic sequences exhibiting no direct detectable similarity. Instead, many eukaryotic sequences were indirectly connected through a "eukaryote-archaebacterium-eubacterium-eukaryote" similarity path. Furthermore, eukaryotic genes highly connected to prokaryotic genes from one domain tend not to be connected to genes from the other prokaryotic domain. Genes of archaebacterial and eubacterial ancestry tend to perform different functions and to act at different subcellular compartments, but in such an intertwined way that suggests an early rather than late integration of both gene repertoires. The archaebacterial repertoire has a similar size in all eukaryotic genomes whereas the number of eubacterium-derived genes is much more variable, suggesting a higher plasticity of this gene repertoire. Consequently, highly reduced eukaryotic genomes contain more genes of archaebacterial than eubacterial affinity. Connected components with prokaryotic and eukaryotic genes tend to include viral and plasmid genes, compatible with a role of gene mobility in the origin of Eukaryotes. Our analyses highlight the power of network approaches to study deep evolutionary events.

RevDate: 2013-01-29
CmpDate: 2013-08-02

Martijn J, TJ Ettema (2013)

From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell.

Biochemical Society transactions, 41(1):451-457.

The evolutionary origin of the eukaryotic cell represents an enigmatic, yet largely incomplete, puzzle. Several mutually incompatible scenarios have been proposed to explain how the eukaryotic domain of life could have emerged. To date, convincing evidence for these scenarios in the form of intermediate stages of the proposed eukaryogenesis trajectories is lacking, presenting the emergence of the complex features of the eukaryotic cell as an evolutionary deus ex machina. However, recent advances in the field of phylogenomics have started to lend support for a model that places a cellular fusion event at the basis of the origin of eukaryotes (symbiogenesis), involving the merger of an as yet unknown archaeal lineage that most probably belongs to the recently proposed 'TACK superphylum' (comprising Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota) with an alphaproteobacterium (the protomitochondrion). Interestingly, an increasing number of so-called ESPs (eukaryotic signature proteins) is being discovered in recently sequenced archaeal genomes, indicating that the archaeal ancestor of the eukaryotic cell might have been more eukaryotic in nature than presumed previously, and might, for example, have comprised primitive phagocytotic capabilities. In the present paper, we review the evolutionary transition from archaeon to eukaryote, and propose a new model for the emergence of the eukaryotic cell, the 'PhAT (phagocytosing archaeon theory)', which explains the emergence of the cellular and genomic features of eukaryotes in the light of a transiently complex phagocytosing archaeon.

RevDate: 2016-10-19
CmpDate: 2013-05-09

Field MC, Horn D, Alsford S, et al (2012)

Telomeres, tethers and trypanosomes.

Nucleus (Austin, Tex.), 3(6):478-486.

Temporal and spatial organization of the nucleus is critical for the control of transcription, mRNA processing and the assembly of ribosomes. This includes the occupancy of specific territories by mammalian chromosomes, the presence of subnuclear compartments such as the nucleolus and Cajal bodies and the division of chromatin between active and inactive states. These latter are commonly associated with the location of DNA within euchromatin and heterochromatin respectively; critically these distinctions arise through modifications to chromatin-associated proteins, including histones, as well as the preferential localization of heterochromatin at the nuclear periphery. Most research on nuclear organization has focused on metazoa and fungi; however, recent technical advances have made more divergent eukaryotes accessible to study, with some surprising results. For example, the organization of heterochromatin is mediated in metazoan nuclei in large part by lamins, the prototypical intermediate filament proteins. Despite the presence of heterochromatin, detected both biochemically and by EM in most eukaryotic organisms, until this year lamins were thought to be restricted to metazoan taxa, and the proteins comprising the lamina in other lineages were unknown. Recent work indicates the presence of lamin orthologs in amoeba, while trypanosomatids possess a large coiled-coil protein, NUP-1, that performs functions analogous to lamins. These data indicate that the presence of a nuclear lamina is substantially more widespread than previously thought, with major implications for the evolution of eukaryotic gene expression mechanisms. We discuss these and other recent findings on the organization of nuclei in diverse organisms, and the implications of these findings for the evolutionary origin of eukaryotes.

RevDate: 2017-02-20
CmpDate: 2013-12-11

Aravind L, Anantharaman V, Zhang D, et al (2012)

Gene flow and biological conflict systems in the origin and evolution of eukaryotes.

Frontiers in cellular and infection microbiology, 2:89.

The endosymbiotic origin of eukaryotes brought together two disparate genomes in the cell. Additionally, eukaryotic natural history has included other endosymbiotic events, phagotrophic consumption of organisms, and intimate interactions with viruses and endoparasites. These phenomena facilitated large-scale lateral gene transfer and biological conflicts. We synthesize information from nearly two decades of genomics to illustrate how the interplay between lateral gene transfer and biological conflicts has impacted the emergence of new adaptations in eukaryotes. Using apicomplexans as example, we illustrate how lateral transfer from animals has contributed to unique parasite-host interfaces comprised of adhesion- and O-linked glycosylation-related domains. Adaptations, emerging due to intense selection for diversity in the molecular participants in organismal and genomic conflicts, being dispersed by lateral transfer, were subsequently exapted for eukaryote-specific innovations. We illustrate this using examples relating to eukaryotic chromatin, RNAi and RNA-processing systems, signaling pathways, apoptosis and immunity. We highlight the major contributions from catalytic domains of bacterial toxin systems to the origin of signaling enzymes (e.g., ADP-ribosylation and small molecule messenger synthesis), mutagenic enzymes for immune receptor diversification and RNA-processing. Similarly, we discuss contributions of bacterial antibiotic/siderophore synthesis systems and intra-genomic and intra-cellular selfish elements (e.g., restriction-modification, mobile elements and lysogenic phages) in the emergence of chromatin remodeling/modifying enzymes and RNA-based regulation. We develop the concept that biological conflict systems served as evolutionary "nurseries" for innovations in the protein world, which were delivered to eukaryotes via lateral gene flow to spur key evolutionary innovations all the way from nucleogenesis to lineage-specific adaptations.

RevDate: 2017-02-20
CmpDate: 2012-11-08

Godde JS (2012)

Breaking through a phylogenetic impasse: a pair of associated archaea might have played host in the endosymbiotic origin of eukaryotes.

Cell & bioscience, 2(1):29 pii:2045-3701-2-29.

For over a century, the origin of eukaryotes has been a topic of intense debate among scientists. Although it has become widely accepted that organelles such as the mitochondria and chloroplasts arose via endosymbiosis, the origin of the eukaryotic nucleus remains enigmatic. Numerous models for the origin of the nucleus have been proposed over the years, many of which use endosymbiosis to explain its existence. Proposals of microbes whose ancestors may have served as either a host or a guest in various endosymbiotic scenarios abound, none of which have been able to sufficiently incorporate the cell biological as well as phylogenetic data which links these organisms to the nucleus. While it is generally agreed that eukaryotic nuclei share more features in common with archaea rather than with bacteria, different studies have identified either one or the other of the two major groups of archaea as potential ancestors, leading to somewhat of a stalemate. This paper seeks to resolve this impasse by presenting evidence that not just one, but a pair of archaea might have served as host to the bacterial ancestor of the mitochondria. This pair may have consisted of ancestors of both Ignicoccus hospitalis as well as its ectosymbiont/ectoparasite 'Nanoarchaeum equitans'.

RevDate: 2016-10-19
CmpDate: 2013-04-04

Magrangeas F, Avet-Loiseau H, Gouraud W, et al (2013)

Minor clone provides a reservoir for relapse in multiple myeloma.

Leukemia, 27(2):473-481.

Recent studies have provided direct evidence for genetic variegation in subclones for various cancer types. However, little is known about subclonal evolutionary processes according to treatment and subsequent relapse in multiple myeloma (MM). This issue was addressed in a cohort of 24 MM patients treated either with conventional chemotherapy or with the proteasome inhibitor, bortezomib. As MM is a highly heterogeneous disease associated with a large number of chromosomal abnormalities, a subset of secondary genetic events that seem to reflect progression, 1q21 gain, NF-κB-activating mutations, RB1 and TP53 deletions, was examined. By using high-resolution single-nucleotide polymorphism arrays, subclones were identified with nonlinear complex evolutionary histories. Such reordering of the spectrum of genetic lesions, identified in a third of MM patients during therapy, is likely to reflect the selection of genetically distinct subclones, not initially competitive against the dominant population but which survived chemotherapy, thrived and acquired new anomalies. In addition, the emergence of minor subclones at relapse appeared to be significantly associated with bortezomib treatment. These data support the idea that new strategies for future clinical trials in MM should combine targeted therapy and subpopulations' control to eradicate all myeloma subclones in order to obtain long-term remission.

RevDate: 2014-04-11
CmpDate: 2013-01-30

Katz LA (2012)

Origin and diversification of eukaryotes.

Annual review of microbiology, 66:411-427.

The bulk of the diversity of eukaryotic life is microbial. Although the larger eukaryotes-namely plants, animals, and fungi-dominate our visual landscapes, microbial lineages compose the greater part of both genetic diversity and biomass, and contain many evolutionary innovations. Our understanding of the origin and diversification of eukaryotes has improved substantially with analyses of molecular data from diverse lineages. These data have provided insight into the nature of the genome of the last eukaryotic common ancestor (LECA). Yet, the origin of key eukaryotic features, namely the nucleus and cytoskeleton, remains poorly understood. In contrast, the past decades have seen considerable refinement in hypotheses on the major branching events in the evolution of eukaryotic diversity. New insights have also emerged, including evidence for the acquisition of mitochondria at the time of the origin of eukaryotes and data supporting the dynamic nature of genomes in LECA.

RevDate: 2012-09-24
CmpDate: 2013-01-04

Lodé T (2012)

For quite a few chromosomes more: the origin of eukaryotes….

Journal of molecular biology, 423(2):135-142.

The evolution of eukaryotes addresses an enigmatic question: what are the evolutionary advantages of having a nucleus? The nucleus is traditionally thought to act as protection for DNA, but eukaryotes are more fragile than bacteria. The compartmentalization of the eukaryotic cell might stem from invaginations of the plasma membrane, and I argue that this autogenous origin of the nucleus constituted a selective innovation caused by cellular constraints due to a large genome. The protoeukaryotic nucleus appears to be a physical and chemical solution to the problem of large amounts of DNA in the form of many linear chromosomes. The selective advantages of having a nuclear envelope are to house a large genome in a stabilized structure and to decouple gene translation from transcription. Supporting the karyogenic model, this new hypothesis opens an original perspective to help in understanding the very ancient origin of eukaryotes.

RevDate: 2017-09-22
CmpDate: 2012-07-24

Thiergart T, Landan G, Schenk M, et al (2012)

An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin.

Genome biology and evolution, 4(4):466-485.

To test the predictions of competing and mutually exclusive hypotheses for the origin of eukaryotes, we identified from a sample of 27 sequenced eukaryotic and 994 sequenced prokaryotic genomes 571 genes that were present in the eukaryote common ancestor and that have homologues among eubacterial and archaebacterial genomes. Maximum-likelihood trees identified the prokaryotic genomes that most frequently contained genes branching as the sister to the eukaryotic nuclear homologues. Among the archaebacteria, euryarchaeote genomes most frequently harbored the sister to the eukaryotic nuclear gene, whereas among eubacteria, the α-proteobacteria were most frequently represented within the sister group. Only 3 genes out of 571 gave a 3-domain tree. Homologues from α-proteobacterial genomes that branched as the sister to nuclear genes were found more frequently in genomes of facultatively anaerobic members of the rhiozobiales and rhodospirilliales than in obligate intracellular ricketttsial parasites. Following α-proteobacteria, the most frequent eubacterial sister lineages were γ-proteobacteria, δ-proteobacteria, and firmicutes, which were also the prokaryote genomes least frequently found as monophyletic groups in our trees. Although all 22 higher prokaryotic taxa sampled (crenarchaeotes, γ-proteobacteria, spirochaetes, chlamydias, etc.) harbor genes that branch as the sister to homologues present in the eukaryotic common ancestor, that is not evidence of 22 different prokaryotic cells participating at eukaryote origins because prokaryotic "lineages" have laterally acquired genes for more than 1.5 billion years since eukaryote origins. The data underscore the archaebacterial (host) nature of the eukaryotic informational genes and the eubacterial (mitochondrial) nature of eukaryotic energy metabolism. The network linking genes of the eukaryote ancestor to contemporary homologues distributed across prokaryotic genomes elucidates eukaryote gene origins in a dialect cognizant of gene transfer in nature.

RevDate: 2015-01-28
CmpDate: 2012-05-14

Xie Q, Wang Y, Lin J, et al (2012)

Potential key bases of ribosomal RNA to kingdom-specific spectra of antibiotic susceptibility and the possible archaeal origin of eukaryotes.

PloS one, 7(1):e29468.

In support of the hypothesis of the endosymbiotic origin of eukaryotes, much evidence has been found to support the idea that some organelles of eukaryotic cells originated from bacterial ancestors. Less attention has been paid to the identity of the host cell, although some biochemical and molecular genetic properties shared by archaea and eukaryotes have been documented. Through comparing 507 taxa of 16S-18S rDNA and 347 taxa of 23S-28S rDNA, we found that archaea and eukaryotes share twenty-six nucleotides signatures in ribosomal DNA. These signatures exist in all living eukaryotic organisms, whether protist, green plant, fungus, or animal. This evidence explicitly supports the archaeal origin of eukaryotes. In the ribosomal RNA, besides A2058 in Escherichia coli vs. G2400 in Saccharomyces cerevisiae, there still exist other twenties of sites, in which the bases are kingdom-specific. Some of these sites concentrate in the peptidyl transferase centre (PTC) of the 23S-28S rRNA. The results suggest potential key sites to explain the kingdom-specific spectra of drug resistance of ribosomes.

RevDate: 2011-11-28
CmpDate: 2012-03-15

Guy L, TJ Ettema (2011)

The archaeal 'TACK' superphylum and the origin of eukaryotes.

Trends in microbiology, 19(12):580-587.

Although most hypotheses to explain the emergence of the eukaryotic lineage are conflicting, some consensus exists concerning the requirement of a genomic fusion between archaeal and bacterial components. Recent phylogenomic studies have provided support for eocyte-like scenarios in which the alleged 'archaeal parent' of the eukaryotic cell emerged from the Crenarchaeota/Thaumarchaeota. Here, we provide evidence for a scenario in which this archaeal parent emerged from within the 'TACK' superphylum that comprises the Thaumarchaeota, Crenarchaeota and Korarchaeota, as well as the recently proposed phylum 'Aigarchaeota'. In support of this view, functional and comparative genomics studies have unearthed an increasing number of features that are uniquely shared by the TACK superphylum and eukaryotes, including proteins involved in cytokinesis, membrane remodeling, cell shape determination and protein recycling.

RevDate: 2017-10-04
CmpDate: 2012-03-08

Vesteg M, J Krajčovič (2011)

The falsifiability of the models for the origin of eukaryotes.

Current genetics, 57(6):367-390.

One group of hypotheses suggests archaeal and/or bacterial ancestry of eukaryotes, while the second group suggests that the ancestor of eukaryotes was different. Especially, the followers of the first group of hypotheses should ask the following: is the replacement of archaeal lipids by bacterial (or vice versa) possible? Do the phylogenies support the origin of one domain from another (or the others)? Can we consider the nutritional mode to resolve the problems of cell origin(s)? Is there any evidence that the ancestor of eukaryotes was intron-free? Would the symbiosis of α-proteobacterial ancestors of mitochondria be successful in an asexual host? Is there evidence that the last universal common ancestor (LUCA) or the last eukaryotic common ancestor was bounded by one membrane only? With respect to the current knowledge about cells and their molecular components, the answer to most of these questions is: No! A model for the origins of domains is briefly presented which cannot be assigned as false through the current scientific data, and is rather consistent with the assumption that eukaryotes are direct descendants of neither archaea nor bacteria. It is proposed that the domain Bacteria arose the first, and that the last common ancestor of Archaea and Eukarya was a pre-cell or a progenote similar to LUCA. The pre-karyote (the host entity for α-proteobacterial ancestors of mitochondria) was probably bounded by two membranes, possessed spliceosomal introns and spliceosomes, was sexual, and α-proteobacterial ancestors of mitochondria were most likely parasites of the pre-karyote periplasm (intermembrane space).

RevDate: 2017-02-20
CmpDate: 2011-10-13

Schlüter A, Ruiz-Trillo I, A Pujol (2011)

Phylogenomic evidence for a myxococcal contribution to the mitochondrial fatty acid beta-oxidation.

PloS one, 6(7):e21989.

BACKGROUND: The origin of eukaryotes remains a fundamental question in evolutionary biology. Although it is clear that eukaryotic genomes are a chimeric combination of genes of eubacterial and archaebacterial ancestry, the specific ancestry of most eubacterial genes is still unknown. The growing availability of microbial genomes offers the possibility of analyzing the ancestry of eukaryotic genomes and testing previous hypotheses on their origins.

Here, we have applied a phylogenomic analysis to investigate a possible contribution of the Myxococcales to the first eukaryotes. We conducted a conservative pipeline with homologous sequence searches against a genomic sampling of 40 eukaryotic and 357 prokaryotic genomes. The phylogenetic reconstruction showed that several eukaryotic proteins traced to Myxococcales. Most of these proteins were associated with mitochondrial lipid intermediate pathways, particularly enzymes generating reducing equivalents with pivotal roles in fatty acid β-oxidation metabolism. Our data suggest that myxococcal species with the ability to oxidize fatty acids transferred several genes to eubacteria that eventually gave rise to the mitochondrial ancestor. Later, the eukaryotic nucleocytoplasmic lineage acquired those metabolic genes through endosymbiotic gene transfer.

CONCLUSIONS/SIGNIFICANCE: Our results support a prokaryotic origin, different from α-proteobacteria, for several mitochondrial genes. Our data reinforce a fluid prokaryotic chromosome model in which the mitochondrion appears to be an important entry point for myxococcal genes to enter eukaryotes.

RevDate: 2017-02-20
CmpDate: 2011-11-28

Lane N (2011)

Energetics and genetics across the prokaryote-eukaryote divide.

Biology direct, 6:35 pii:1745-6150-6-35.

BACKGROUND: All complex life on Earth is eukaryotic. All eukaryotic cells share a common ancestor that arose just once in four billion years of evolution. Prokaryotes show no tendency to evolve greater morphological complexity, despite their metabolic virtuosity. Here I argue that the eukaryotic cell originated in a unique prokaryotic endosymbiosis, a singular event that transformed the selection pressures acting on both host and endosymbiont.

RESULTS: The reductive evolution and specialisation of endosymbionts to mitochondria resulted in an extreme genomic asymmetry, in which the residual mitochondrial genomes enabled the expansion of bioenergetic membranes over several orders of magnitude, overcoming the energetic constraints on prokaryotic genome size, and permitting the host cell genome to expand (in principle) over 200,000-fold. This energetic transformation was permissive, not prescriptive; I suggest that the actual increase in early eukaryotic genome size was driven by a heavy early bombardment of genes and introns from the endosymbiont to the host cell, producing a high mutation rate. Unlike prokaryotes, with lower mutation rates and heavy selection pressure to lose genes, early eukaryotes without genome-size limitations could mask mutations by cell fusion and genome duplication, as in allopolyploidy, giving rise to a proto-sexual cell cycle. The side effect was that a large number of shared eukaryotic basal traits accumulated in the same population, a sexual eukaryotic common ancestor, radically different to any known prokaryote.

CONCLUSIONS: The combination of massive bioenergetic expansion, release from genome-size constraints, and high mutation rate favoured a protosexual cell cycle and the accumulation of eukaryotic traits. These factors explain the unique origin of eukaryotes, the absence of true evolutionary intermediates, and the evolution of sex in eukaryotes but not prokaryotes.

REVIEWERS: This article was reviewed by: Eugene Koonin, William Martin, Ford Doolittle and Mark van der Giezen. For complete reports see the Reviewers' Comments section.

RevDate: 2011-01-24
CmpDate: 2011-05-02

Poole AM, N Neumann (2011)

Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis.

Research in microbiology, 162(1):71-76.

An archaeal origin of eukaryotes is often equated with the engulfment of the bacterial ancestor of mitochondria by an archaeon. Such an event is problematic in that it is not supported by archaeal cell biology. We show that placing phylogenetic results within a stem-and-crown framework eliminates such incompatibilities, and that an archaeal origin for eukaryotes (as suggested from recent phylogenies) can be uncontroversially reconciled with phagocytosis as the mechanism for engulfment of the mitochondrial ancestor. This is significant because it eliminates a perceived problem with eukaryote origins: that an archaeal origin of eukaryotes (as under the Eocyte hypothesis) cannot be reconciled with existing cell biological mechanisms through which bacteria may take up residence inside eukaryote cells.

RevDate: 2017-02-20
CmpDate: 2010-09-28

Gribaldo S, Poole AM, Daubin V, et al (2010)

The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse?.

Nature reviews. Microbiology, 8(10):743-752.

The origin of eukaryotes and their evolutionary relationship with the Archaea is a major biological question and the subject of intense debate. In the context of the classical view of the universal tree of life, the Archaea and the Eukarya have a common ancestor, the nature of which remains undetermined. Alternative views propose instead that the Eukarya evolved directly from a bona fide archaeal lineage. Several recent large-scale phylogenomic studies using an array of approaches are divided in supporting either one or the other scenario, despite analysing largely overlapping data sets of universal genes. We examine the reasons for such a lack of consensus and consider how alternative approaches may enable progress in answering this fascinating and as-yet-unresolved question.

RevDate: 2017-02-20
CmpDate: 2010-09-29

Koonin EV (2010)

The origin and early evolution of eukaryotes in the light of phylogenomics.

Genome biology, 11(5):209.

Phylogenomics of eukaryote supergroups suggest a highly complex last common ancestor of eukaryotes and a key role of mitochondrial endosymbiosis in the origin of eukaryotes.

RevDate: 2016-11-26
CmpDate: 2011-01-10

Sørensen DM, Buch-Pedersen MJ, MG Palmgren (2010)

Structural divergence between the two subgroups of P5 ATPases.

Biochimica et biophysica acta, 1797(6-7):846-855.

Evolution of P5 type ATPases marks the origin of eukaryotes but still they remain the least characterized pumps in the superfamily of P-type ATPases. Phylogenetic analysis of available sequences suggests that P5 ATPases should be divided into at least two subgroups, P5A and P5B. P5A ATPases have been identified in the endoplasmic reticulum and seem to have basic functions in protein maturation and secretion. P5B ATPases localize to vacuolar/lysosomal or apical membranes and in animals play a role in hereditary neuronal diseases. Here we have used a bioinformatical approach to identify differences in the primary sequences between the two subgroups. P5A and P5B ATPases appear have a very different membrane topology from other P-type ATPases with two and one, respectively, additional transmembrane segments inserted in the N-terminal end. Based on conservation of residues in the transmembrane region, the two P5 subgroups most likely have different substrate specificities although these cannot be predicted from their sequences. Furthermore, sequence differences between P5A and P5B ATPases are identified in the catalytic domains that could influence key kinetic properties differentially. Together these findings indicate that P5A and P5B ATPases are structurally and functionally different.

RevDate: 2017-02-20
CmpDate: 2009-12-29

Marín I (2009)

Diversification of the cullin family.

BMC evolutionary biology, 9:267 pii:1471-2148-9-267.

BACKGROUND: Cullins are proteins involved in ubiquitination through their participation in multisubunit ubiquitin ligase complexes. In this study, I use comparative genomic data to establish the pattern of emergence and diversification of cullins in eukaryotes.

RESULTS: The available data indicate that there were three cullin genes before the unikont/bikont split, which I have called Culalpha, Culbeta and Culgamma. Fungal species have quite strictly conserved these three ancestral genes, with only occasional lineage-specific duplications. On the contrary, several additional genes appeared in the animal or plant lineages. For example, the human genes Cul1, Cul2, Cul5, Cul7 and Parc all derive from the ancestral Culalpha gene. These results, together with the available functional data, suggest that three different types of ubiquitin ligase cullin-containing complexes were already present in early eukaryotic evolution: 1) SCF-like complexes with Culalpha proteins; 2) Culbeta/BTB complexes; and, 3) Complexes containing Culgamma and DDB1-like proteins. Complexes containing elongins have arisen more recently and perhaps twice independently in animals and fungi.

CONCLUSION: Most of the known types of cullin-containing ubiquitin ligase complexes are ancient. The available data suggest that, since the origin of eukaryotes, complex diversity has been mostly generated by combining closely related subunits, while radical innovations, giving rise to novel types of complexes, have been scarce. However, several protist groups not examined so far contain highly divergent cullins, indicating that additional types of complexes may exist.

RevDate: 2010-11-18
CmpDate: 2009-08-20

Zimmer C (2009)

Origins. On the origin of eukaryotes.

Science (New York, N.Y.), 325(5941):666-668.

RevDate: 2017-02-20
CmpDate: 2011-07-14

Vesteg M, J Krajcovic (2008)

Origin of eukaryotic cells as a symbiosis of parasitic alpha-proteobacteria in the periplasm of two-membrane-bounded sexual pre-karyotes.

Communicative & integrative biology, 1(1):104-113.

The last universal common ancestor (LUCA) might have been either prokaryotic- or eukaryotic-like. Nevertheless, the universally distributed components suggest rather LUCA consistent with the pre-cell theory of Kandler. The hypotheses for the origin of eukaryotes are briefly summarized. The models under which prokaryotes or their chimeras were direct ancestors of eukaryotes are criticized. It is proposed that the pre-karyote (a host entity for alpha-proteobacteria) was a remnant of pre-cellular world, and was unlucky to have evolved fusion prohibiting cell surface, and thus could have evolved sex. The DNA damage checkpoint pathway could have represented the only pre-karyotic checkpoint control allowing division only when DNA was completely replicated without mistakes. The fusion of two partially diploid (in S-phase blocked) pre-karyotes might have represented another repair strategy. After completing replication of both haploid sets, DNA damage checkpoint would allow two subsequent rounds of fission. Alternatively, pre-karyote might have possessed two membranes inherited from LUCA. Under this hypothesis symbiotic alpha-proteobacterial ancestors of mitochondria might have ancestrally been selfish parasites of pre-karyote intermembrane space whose infection might have been analogous to infection of G(-)-bacterial periplasm by Bdellovibrio sp. It is suggested that eukaryotic plasma membrane might be derived from pre-karyote outer membrane and nuclear/ER membrane might be derived from pre-karyote inner membrane. Thus the nucleoplasm might be derived from pre-karyote cytoplasm and eukaryotic cytoplasm might be homologous to pre-karyote periplasm.

RevDate: 2010-11-18
CmpDate: 2009-09-23

Davidov Y, E Jurkevitch (2009)

Predation between prokaryotes and the origin of eukaryotes.

BioEssays : news and reviews in molecular, cellular and developmental biology, 31(7):748-757.

Accumulating data suggest that the eukaryotic cell originated from a merger of two prokaryotes, an archaeal host and a bacterial endosymbiont. However, since prokaryotes are unable to perform phagocytosis, the means by which the endosymbiont entered its host is an enigma. We suggest that a predatory or parasitic interaction between prokaryotes provides a reasonable explanation for this conundrum. According to the model presented here, the host in this interaction was an anaerobic archaeon with a periplasm-like space. The predator was a small (facultative) aerobic alpha-proteobacterium, which penetrated and replicated within the host periplasm, and later became the mitochondria. Plausible conditions under which this interaction took place and circumstances that may have led to the contemporary complex eukaryotic cell are discussed.

RevDate: 2017-02-20

Tekle YI, Parfrey LW, LA Katz (2009)

Molecular Data are Transforming Hypotheses on the Origin and Diversification of Eukaryotes.

Bioscience, 59(6):471-481.

The explosion of molecular data has transformed hypotheses on both the origin of eukaryotes and the structure of the eukaryotic tree of life. Early ideas about the evolution of eukaryotes arose through analyses of morphology by light microscopy and later electron microscopy. Though such studies have proven powerful at resolving more recent events, theories on origins and diversification of eukaryotic life have been substantially revised in light of analyses of molecular data including gene and, increasingly, whole genome sequences. By combining these approaches, progress has been made in elucidating both the origin and diversification of eukaryotes. Yet many aspects of the evolution of eukaryotic life remain to be illuminated.

RevDate: 2017-02-20
CmpDate: 2009-01-27

Cox CJ, Foster PG, Hirt RP, et al (2008)

The archaebacterial origin of eukaryotes.

Proceedings of the National Academy of Sciences of the United States of America, 105(51):20356-20361.

The origin of the eukaryotic genetic apparatus is thought to be central to understanding the evolution of the eukaryotic cell. Disagreement about the source of the relevant genes has spawned competing hypotheses for the origins of the eukaryote nuclear lineage. The iconic rooted 3-domains tree of life shows eukaryotes and archaebacteria as separate groups that share a common ancestor to the exclusion of eubacteria. By contrast, the eocyte hypothesis has eukaryotes originating within the archaebacteria and sharing a common ancestor with a particular group called the Crenarchaeota or eocytes. Here, we have investigated the relative support for each hypothesis from analysis of 53 genes spanning the 3 domains, including essential components of the eukaryotic nucleic acid replication, transcription, and translation apparatus. As an important component of our analysis, we investigated the fit between model and data with respect to composition. Compositional heterogeneity is a pervasive problem for reconstruction of ancient relationships, which, if ignored, can produce an incorrect tree with strong support. To mitigate its effects, we used phylogenetic models that allow for changing nucleotide or amino acid compositions over the tree and data. Our analyses favor a topology that supports the eocyte hypothesis rather than archaebacterial monophyly and the 3-domains tree of life.

RevDate: 2008-10-20
CmpDate: 2008-11-18

Saruhashi S, Hamada K, Miyata D, et al (2008)

Comprehensive analysis of the origin of eukaryotic genomes.

Genes & genetic systems, 83(4):285-291.

There is currently no consensus on the evolutionary origin of eukaryotes. In the search of the ancestors of eukaryotes, we analyzed the phylogeny of 46 genomes, including those of 2 eukaryotes, 8 archaea, and 36 eubacteria. To avoid the effects of gene duplications, we used inparalog pairs of genes with orthologous relationships. First, we grouped these inparalogs into the functional categories of the nucleus, cytoplasm, and mitochondria. Next, we counted the sister groups of eukaryotes in prokaryotic phyla and plotted them on a standard phylogenetic tree. Finally, we used Pearson's chi-square test to estimate the origin of the genomes from specific prokaryotic ancestors. The results suggest the eukaryotic nuclear genome descends from an archaea that was neither euryarchaeota nor crenarchaeota and that the mitochondrial genome descends from alpha-proteobacteria. In contrast, genes related to the cytoplasm do not appear to originate from a specific group of prokaryotes.

RevDate: 2017-02-20
CmpDate: 2009-02-26

Scofield DG, M Lynch (2008)

Evolutionary diversification of the Sm family of RNA-associated proteins.

Molecular biology and evolution, 25(11):2255-2267.

The Sm family of proteins is closely associated with RNA metabolism throughout all life. These proteins form homomorphic and heteromorphic rings consisting of six or seven subunits with a characteristic central pore, the presence of which is critical for binding U-rich regions of single-stranded RNA. Eubacteria and Archaea typically carry one or two forms of Sm proteins and assemble one homomorphic ring per Sm protein. Eukaryotes typically carry 16 or more Sm proteins that assemble to form heteromorphic rings which lie at the center of a number of critical RNA-associated small nuclear ribonucleoproteins (snRNPs). High Sm protein diversity and heteromorphic Sm rings are features stretching back to the origin of eukaryotes; very deep phylogenetic divisions among existing Sm proteins indicate simultaneous evolution across essentially all existing eukaryotic life. Two basic forms of heteromorphic Sm rings are found in eukaryotes. Fixed Sm rings are highly stable and static and are assembled around an RNA cofactor. Flexible Sm rings also stabilize and chaperone RNA but assemble in the absence of an RNA substrate and, more significantly, associate with and dissociate from RNA substrates more freely than fixed rings. This suggests that the conformation of flexible Sm rings might be modified in some specific manner to facilitate association and dissociation with RNA. Diversification of eukaryotic Sm proteins may have been initiated by gene transfers and/or genome clashes that accompanied the origin of the eukaryotic cell itself, with further diversification driven by a greater need for steric specificity within increasingly complex snRNPs.

RevDate: 2017-02-20
CmpDate: 2009-03-23

Jékely G (2008)

Origin of the nucleus and Ran-dependent transport to safeguard ribosome biogenesis in a chimeric cell.

Biology direct, 3:31 pii:1745-6150-3-31.

BACKGROUND: The origin of the nucleus is a central problem about the origin of eukaryotes. The common ancestry of nuclear pore complexes (NPC) and vesicle coating complexes indicates that the nucleus evolved via the modification of a pre-existing endomembrane system. Such an autogenous scenario is cell biologically feasible, but it is not clear what were the selective or neutral mechanisms that had led to the origin of the nuclear compartment.

RESULTS: A key selective force during the autogenous origin of the nucleus could have been the need to segregate ribosome factories from the cytoplasm where ribosomal proteins (RPs) of the protomitochondrium were synthesized. After its uptake by an anuclear cell the protomitochondrium transferred several of its RP genes to the host genome. Alphaproteobacterial RPs and archaebacterial-type host ribosomes were consequently synthesized in the same cytoplasm. This could have led to the formation of chimeric ribosomes. I propose that the nucleus evolved when the host cell compartmentalised its ribosome factories and the tightly linked genome to reduce ribosome chimerism. This was achieved in successive stages by first evolving karyopherin and RanGTP dependent chaperoning of RPs, followed by the evolution of a membrane network to serve as a diffusion barrier, and finally a hydrogel sieve to ensure selective permeability at nuclear pores. Computer simulations show that a gradual segregation of cytoplasm and nucleoplasm via these steps can progressively reduce ribosome chimerism.

CONCLUSION: Ribosome chimerism can provide a direct link between the selective forces for and the mechanisms of evolving nuclear transport and compartmentalisation. The detailed molecular scenario presented here provides a solution to the gradual evolution of nuclear compartmentalization from an anuclear stage.

REVIEWERS: This article was reviewed by Eugene V Koonin, Martijn Huynen, Anthony M. Poole and Patrick Forterre.

RevDate: 2015-03-05
CmpDate: 2008-10-14

Vesteg M, J Krajcovic (2008)

On the origin of eukaryotic cytoskeleton.

Rivista di biologia, 101(1):109-118.

The origin of eukaryote-specific cytoskeletal proteins is an issue which is closely related to the origin of the domain Eukarya. As nearly all of these proteins are not found in prokaryotes, the prokaryotic origin of eukaryotic cytoskeletal network suggested by most models is questionable. Eukaryotic cytoskeletal proteins might descend from subpopulations of pre-cells co-existing with Bacteria and Archaea prior to the origin of eukaryotes. The pre-karyote (the host for a-proteobacterial ancestors of mitochondria) might have already possessed eukaryotic-like cytoskeleton. A possible role for viruses in the origin of eukaryotic cytoskeletal proteins is discussed. Viruses parasitizing on pre-cells and/or on the pre-karyote might have themselves used several eukaryotic-like cytoskeletal proteins for segregation and packing of their genomes.

RevDate: 2017-02-20
CmpDate: 2008-09-22

Yutin N, Makarova KS, Mekhedov SL, et al (2008)

The deep archaeal roots of eukaryotes.

Molecular biology and evolution, 25(8):1619-1630.

The set of conserved eukaryotic protein-coding genes includes distinct subsets one of which appears to be most closely related to and, by inference, derived from archaea, whereas another one appears to be of bacterial, possibly, endosymbiotic origin. The "archaeal" genes of eukaryotes, primarily, encode components of information-processing systems, whereas the "bacterial" genes are predominantly operational. The precise nature of the archaeo-eukaryotic relationship remains uncertain, and it has been variously argued that eukaryotic informational genes evolved from the homologous genes of Euryarchaeota or Crenarchaeota (the major branches of extant archaea) or that the origin of eukaryotes lies outside the known diversity of archaea. We describe a comprehensive set of 355 eukaryotic genes of apparent archaeal origin identified through ortholog detection and phylogenetic analysis. Phylogenetic hypothesis testing using constrained trees, combined with a systematic search for shared derived characters in the form of homologous inserts in conserved proteins, indicate that, for the majority of these genes, the preferred tree topology is one with the eukaryotic branch placed outside the extant diversity of archaea although small subsets of genes show crenarchaeal and euryarchaeal affinities. Thus, the archaeal genes in eukaryotes appear to descend from a distinct, ancient, and otherwise uncharacterized archaeal lineage that acquired some euryarchaeal and crenarchaeal genes via early horizontal gene transfer.

RevDate: 2008-01-31
CmpDate: 2008-05-20

Carlon E, Dkhissi A, Malki ML, et al (2007)

Stability domains of actin genes and genomic evolution.

Physical review. E, Statistical, nonlinear, and soft matter physics, 76(5 Pt 1):051916.

In eukaryotic genes, the protein coding sequence is split into several fragments, the exons, separated by noncoding DNA stretches, the introns. Prokaryotes do not have introns in their genomes. We report calculations of the stability domains of actin genes for various organisms in the animal, plant, and fungi kingdoms. Actin genes have been chosen because they have been highly conserved during evolution. In these genes, all introns were removed so as to mimic ancient genes at the time of the early eukaryotic development, i.e., before intron insertion. Common stability boundaries are found in evolutionarily distant organisms, which implies that these boundaries date from the early origin of eukaryotes. In general, the boundaries correspond with intron positions in the actins of vertebrates and other animals, but not much for plants and fungi. The sharpest boundary is found in a locus where fungi, algae, and animals have introns in positions separated by one nucleotide only, which identifies a hot spot for insertion. These results suggest that some introns may have been incorporated into the genomes through a thermodynamically driven mechanism, in agreement with previous observations on human genes. They also suggest a different mechanism for intron insertion in plants and animals.

RevDate: 2017-09-22
CmpDate: 2008-02-11

Zhu S (2007)

Evidence for myxobacterial origin of eukaryotic defensins.

Immunogenetics, 59(12):949-954.

Antimicrobial defensins with the cysteine-stabilized alpha-helical and beta-sheet (CS alpha beta) motif are a large family of ancient, evolutionarily related innate immunity effectors of multicellular organisms. Although the widespread distribution in plants, fungi, and invertebrates suggests their uniqueness to Eukarya, it is unknown whether these eukaryotic defensins originated before or posterior to the emergence of eukaryotes. In this study, we provide evidence in support of the existence of defensin-like peptides (DLPs) in myxobacteria based on structural bioinformatics analysis, which recognized two bacterial peptides with a conserved cysteine-stabilized alpha-helical motif, a nested structural unit of the CS alpha beta motif. Similarity in sequence and structure to fungal DLPs together with restricted distribution to the myxobacteria as well as central role of the myxobacteria in the origin of eukaryotes suggest that the bacterial DLPs represent the ancestor of the eukaryotic defensins and could mediate immune defense of early eukaryotes after gene transfer to the proto-eukaryotic genome. Our work thus offers a basis for further investigation of prokaryotic origin of eukaryotic immune effector molecules.

RevDate: 2017-02-20
CmpDate: 2007-12-12

Sales-Pardo M, Chan AO, Amaral LA, et al (2007)

Evolution of protein families: is it possible to distinguish between domains of life?.

Gene, 402(1-2):81-93.

Understanding evolutionary relationships between species can shed new light into the rooting of the tree of life and the origin of eukaryotes, thus, resulting in a long standing interest in accurately assessing evolutionary parameters at time scales on the order of a billion of years. Prior work suggests large variability in molecular substitution rates, however, we still do not know whether such variability is due to species-specific trends at a genomic scale, or whether it can be attributed to the fluctuations inherent in any stochastic process. Here, we study the statistical properties of gene and protein-family sizes in order to quantify the long time scale evolutionary differences and similarities across species. We first determine the protein families of 209 species of bacteria and 20 species of archaea. We find that we are unable to reject the null hypothesis that the protein-family sizes of these species are drawn from the same distribution. In addition, we find that for species classified in the same phylogenetic branch or in the same lifestyle group, family size distributions are not significantly more similar than for species in different branches. These two findings can be accounted for in terms of a dynamical birth, death, and innovation model that assumes identical protein-family evolutionary rates for all species. Our theoretical and empirical results thus strongly suggest that the variability empirically observed in protein-family size distributions is compatible with the expected stochastic fluctuations for an evolutionary process with identical genomic evolutionary rates. Our findings hold special importance for the plausibility of some theories of the origin of eukaryotes which require drastic changes in evolutionary rates for some period during the last 2 billion years.

RevDate: 2010-11-18
CmpDate: 2007-08-06

Davidov Y, E Jurkevitch (2007)

Comments of Poole and Penny's essay "Evaluating hypotheses for the origin of eukaryotes", BioEssays 29:74-84.

BioEssays : news and reviews in molecular, cellular and developmental biology, 29(6):615-616.

RevDate: 2007-08-03
CmpDate: 2007-10-29

Pisani D, Cotton JA, JO McInerney (2007)

Supertrees disentangle the chimerical origin of eukaryotic genomes.

Molecular biology and evolution, 24(8):1752-1760.

Eukaryotes are traditionally considered to be one of the three natural divisions of the tree of life and the sister group of the Archaebacteria. However, eukaryotic genomes are replete with genes of eubacterial ancestry, and more than 20 mutually incompatible hypotheses have been proposed to account for eukaryote origins. Here we test the predictions of these hypotheses using a novel supertree-based phylogenetic signal-stripping method, and recover supertrees of life based on phylogenies for up to 5,741 single gene families distributed across 185 genomes. Using our signal-stripping method, we show that there are three distinct phylogenetic signals in eukaryotic genomes. In order of strength, these link eukaryotes with the Cyanobacteria, the Proteobacteria, and the Thermoplasmatales, an archaebacterial (euryarchaeotes) group. These signals correspond to distinct symbiotic partners involved in eukaryote evolution: plastids, mitochondria, and the elusive host lineage. According to our whole-genome data, eukaryotes are hardly the sister group of the Archaebacteria, because up to 83% of eukaryotic genes with a prokaryotic homolog have eubacterial, not archaebacterial, origins. The results reject all but two of the current hypotheses for the origin of eukaryotes: those assuming a sulfur-dependent or hydrogen-dependent syntrophy for the origin of mitochondria.

RevDate: 2017-02-10
CmpDate: 2007-06-04

de Duve C (2007)

The origin of eukaryotes: a reappraisal.

Nature reviews. Genetics, 8(5):395-403.

Ever since the elucidation of the main structural and functional features of eukaryotic cells and subsequent discovery of the endosymbiotic origin of mitochondria and plastids, two opposing hypotheses have been proposed to account for the origin of eukaryotic cells. One hypothesis postulates that the main features of these cells, including their ability to capture food by endocytosis and to digest it intracellularly, were developed first, and later had a key role in the adoption of endosymbionts; the other proposes that the transformation was triggered by an interaction between two typical prokaryotic cells, one of which became the host and the other the endosymbiont. Re-examination of this question in the light of cell-biological and phylogenetic data leads to the conclusion that the first model is more likely to be the correct one.

RevDate: 2010-11-18
CmpDate: 2007-01-31

Poole AM, D Penny (2007)

Evaluating hypotheses for the origin of eukaryotes.

BioEssays : news and reviews in molecular, cellular and developmental biology, 29(1):74-84.

Numerous scenarios explain the origin of the eukaryote cell by fusion or endosymbiosis between an archaeon and a bacterium (and sometimes a third partner). We evaluate these hypotheses using the following three criteria. Can the data be explained by the null hypothesis that new features arise sequentially along a stem lineage? Second, hypotheses involving an archaeon and a bacterium should undergo standard phylogenetic tests of gene distribution. Third, accounting for past events by processes observed in modern cells is preferable to postulating unknown processes that have never been observed. For example, there are many eukaryote examples of bacteria as endosymbionts or endoparasites, but none known in archaea. Strictly post-hoc hypotheses that ignore this third criterion should be avoided. Applying these three criteria significantly narrows the number of plausible hypotheses. Given current knowledge, our conclusion is that the eukaryote lineage must have diverged from an ancestor of archaea well prior to the origin of the mitochondrion. Significantly, the absence of ancestrally amitochondriate eukaryotes (archezoa) among extant eukaryotes is neither evidence for an archaeal host for the ancestor of mitochondria, nor evidence against a eukaryotic host.

RevDate: 2017-02-19
CmpDate: 2007-07-31

Poole AM (2006)

Did group II intron proliferation in an endosymbiont-bearing archaeon create eukaryotes?.

Biology direct, 1:36 pii:1745-6150-1-36.

Martin & Koonin recently proposed that the eukaryote nucleus evolved as a quality control mechanism to prevent ribosome readthrough into introns. In their scenario, the bacterial ancestor of mitochondria was resident in an archaeal cell, and group II introns (carried by the fledgling mitochondrion) inserted into coding regions in the archaeal host genome. They suggest that if transcription and translation were coupled, and because splicing is expected to have been slower than translation, the effect of insertion would have been ribosome readthrough into introns, resulting in production of aberrant proteins. The emergence of the nuclear compartment would thus have served to separate transcription and splicing from translation, thereby alleviating this problem. In this article, I argue that Martin & Koonin's model is not compatible with current knowledge. The model requires that group II introns would spread aggressively through an archaeal genome. It is well known that selfish elements can spread through an outbreeding sexual population despite a substantial fitness cost to the host. The same is not true for asexual lineages however, where both theory and observation argue that such elements will be under pressure to reduce proliferation, and may be lost completely. The recent introduction of group II introns into archaea by horizontal transfer provides a natural test case with which to evaluate Martin & Koonin's model. The distribution and behaviour of these introns fits prior theoretical expectations, not the scenario of aggressive proliferation advocated by Martin & Koonin. I therefore conclude that the mitochondrial seed hypothesis for the origin of eukaryote introns, on which their model is based, better explains the early expansion of introns in eukaryotes. The mitochondrial seed hypothesis has the capacity to separate the origin of eukaryotes from the origin of introns, leaving open the possibility that the cell that engulfed the ancestor of mitochondria was a sexually outcrossing eukaryote cell.

RevDate: 2016-11-24
CmpDate: 2007-05-16

Lucas JI, I Marín (2007)

A new evolutionary paradigm for the Parkinson disease gene DJ-1.

Molecular biology and evolution, 24(2):551-561.

The DJ-1 gene is extensively studied because of its involvement in familial Parkinson disease. DJ-1 belongs to a complex superfamily of genes that includes both prokaryotic and eukaryotic representatives. We determine that many prokaryotic groups, such as proteobacteria, cyanobacteria, spirochaetes, firmicutes, or fusobacteria, have genes, often incorrectly called "Thij," that are very close relatives of DJ-1, to the point that they cannot be clearly separated from the eukaryotic DJ-1 genes by phylogenetic analyses of their sequences. In addition, and contrary to a previous study that suggested that DJ-1 genes were animal specific, we show that DJ-1 genes are found in at least 5 of the 6 main eukaryotic groups: opisthokonta (both animals and fungi), plantae, chromalveolata, excavata, and amoebozoa. Our results thus provide strong evidence for DJ-1 genes originating before the origin of eukaryotes. Interestingly, we found that some fungal species, among them the model yeast Schizosaccharomyces pombe, have DJ-1-like genes, most likely orthologous to the animal genes. This finding opens new ways for the analysis of the functions of this group of genes.

RevDate: 2011-05-03
CmpDate: 2007-06-18

McInerney JO, M Wilkinson (2005)

New methods ring changes for the tree of life.

Trends in ecology & evolution, 20(3):105-107.

Relationships among prokaryotes and the origin of eukaryotes have both proven controversial, with results depending upon the gene sequences and methods used. Extensive horizontal gene transfer is one possible reason why inferring such deep phylogenetic relationships is difficult. In two recent papers, Lake and Rivera introduce new methods that can be used to reconstruct the genomic tree in the presence of horizontal gene transfers, but which suggest that a ring rather than a tree is a better representation of some parts of the history of life on Earth.

RevDate: 2016-10-20
CmpDate: 2005-11-15

Lebkova NP, AP Kuznetsova (2005)

[Intracellular symbiosis and energetic role of bacteria in gill epithelium of freshwater mollusks and fishes].

Izvestiia Akademii nauk. Seriia biologicheskaia.

Penetration of bacteria by endocytosis into gill epithelial cells has been revealed in animals of different evolutionary levels (freshwater mollusks and fishes). These data confirm the leading role of endosymbiosis in the origin of eukaryotes from prokaryotes and in the evolution of animal life.

RevDate: 2016-10-20
CmpDate: 2005-11-03

Markov AV, AM Kulikov (2005)

[Homologous protein domains in superkingdoms Archaea, Bacteria, and Eukaryota and the problem of the origin of eukaryotes].

Izvestiia Akademii nauk. Seriia biologicheskaia.

The distribution of protein domains was analyzed in superkingdoms Archaea, Bacteria, and Eukaryota. About a half of eukaryotic domains have prokaryotic origin. Many domains related to information processing in the nucleocytoplasm were inherited from archaea. Sets of domains associated with metabolism and regulatory and signaling systems were inherited from bacteria. Many signaling and regulatory domains common for bacteria and eukaryotes were responsible for the cellular interaction of bacteria with other components of the microbial community but were involved in coordination of the activity of eukaryotic organelles and cells in multicellular organisms. Many eukaryotic domains of bacterial origin could not originate from ancestral mitochondria and plastids but rather were adopted from other bacteria. An archaeon with the induced incorporation of alien genetic material could be the ancestor of the eukaryotic nucleocytoplasm.

RevDate: 2017-04-08
CmpDate: 2005-06-24

Simonson AB, Servin JA, Skophammer RG, et al (2005)

Decoding the genomic tree of life.

Proceedings of the National Academy of Sciences of the United States of America, 102 Suppl 1:6608-6613.

Genomes hold within them the record of the evolution of life on Earth. But genome fusions and horizontal gene transfer (HGT) seem to have obscured sufficiently the gene sequence record such that it is difficult to reconstruct the phylogenetic tree of life. HGT among prokaryotes is not random, however. Some genes (informational genes) are more difficult to transfer than others (operational genes). Furthermore, environmental, metabolic, and genetic differences among organisms restrict HGT, so that prokaryotes preferentially share genes with other prokaryotes having properties in common, including genome size, genome G+C composition, carbon utilization, oxygen utilization/sensitivity, and temperature optima, further complicating attempts to reconstruct the tree of life. A new method of phylogenetic reconstruction based on gene presence and absence, called conditioned reconstruction, has improved our prospects for reconstructing prokaryotic evolution. It is also able to detect past genome fusions, such as the fusion that appears to have created the first eukaryote. This genome fusion between a deep branching eubacterium, possibly an ancestor of the cyanobacterium and a proteobacterium, with an archaeal eocyte (crenarchaea), appears to be the result of an early symbiosis. Given new tools and new genes from relevant organisms, it should soon be possible to test current and future fusion theories for the origin of eukaryotes and to discover the general outlines of the prokaryotic tree of life.

RevDate: 2017-09-22
CmpDate: 2005-04-18

Horiike T, Hamada K, Miyata D, et al (2004)

The origin of eukaryotes is suggested as the symbiosis of pyrococcus into gamma-proteobacteria by phylogenetic tree based on gene content.

Journal of molecular evolution, 59(5):606-619.

Attempts were made to define the relationship among the three domains (eukaryotes, archaea, and eubacteria) using phylogenetic tree analyses of 16S rRNA sequences as well as of other protein sequences. Since the results are inconsistent, it is implied that the eukaryotic genome has a chimeric structure. In our previous studies, the origin of eukaryotes to be the symbiosis of archaea into eubacteria using the whole open reading frames (ORF) of many genomes was suggested. In these studies, the species participating in the symbiosis were not clarified, and the effect of gene duplication after speciation (in-paralog) was not addressed. To avoid the influence of the in-paralog, we developed a new method to calculate orthologous ORFs. Furthermore, we separated eukaryotic in-paralogs into three groups by sequence similarity to archaea, eubacteria (other than alpha-proteobacteria), and alpha-proteobacteria and treated them as individual organisms. The relationship between the three ORF groups and the functional classification was clarified by this analysis. The introduction of this new method into the phylogenetic tree analysis of 66 organisms (4 eukaryotes, 13 archaea, and 49 eubacteria) based on gene content suggests the symbiosis of pyrococcus into gamma-proteobacteria as the origin of eukaryotes.

RevDate: 2010-11-18
CmpDate: 2006-03-31

Jékely G (2005)

Glimpsing over the event horizon: evolution of nuclear pores and envelope.

Cell cycle (Georgetown, Tex.), 4(2):297-299.

The origin of eukaryotes from prokaryotic ancestors is one of the major evolutionary transitions in the history of life. The nucleus, a membrane bound compartment for confining the genome, is a central feature of eukaryotic cells and its origin also has to be a central feature of any workable theory that ventures to explain eukaryotic origins. Recent bioinformatic analyses of components of the nuclear pore complex (NPC), the nuclear envelope (NE), and the nuclear transport systems revealed exciting evolutionary connections (e.g., between NPC and coated vesicles) and provided a useful record of the phyletic distribution and history of NPC and NE components. These analyses allow us to refine theories on the origin and evolution of the nucleus, and consequently, of the eukaryotic cell.

RevDate: 2010-11-18
CmpDate: 2005-04-01

Vishwanath P, Favaretto P, Hartman H, et al (2004)

Ribosomal protein-sequence block structure suggests complex prokaryotic evolution with implications for the origin of eukaryotes.

Molecular phylogenetics and evolution, 33(3):615-625.

Amino acid sequence alignments of orthologous ribosomal proteins found in Bacteria, Archaea, and Eukaryota display, relative to one another, an unusual segment or block structure, with major evolutionary implications. Within each of the prokaryotic phylodomains the sequences exhibit substantial similarity, but cross-domain alignments break up into (a) universal blocks (conserved in both phylodomains), (b) bacterial blocks (unalignable with any archaeal counterparts), and (c) archaeal blocks (unalignable with any bacterial counterparts). Sequences of those eukaryotic cytoplasmic riboproteins that have orthologs in both Bacteria and Archaea, exclusively match the archaeal block structure. The distinct blocks do not correlate consistently with any identifiable functional or structural feature including RNA and protein contacts. This phylodomain-specific block pattern also exists in a number of other proteins associated with protein synthesis, but not among enzymes of intermediary metabolism. While the universal blocks imply that modern Bacteria and Archaea (as defined by their translational machinery) clearly have had a common ancestor, the phylodomain-specific blocks imply that these two groups derive from single, phylodomain-specific types that came into existence at some point long after that common ancestor. The simplest explanation for this pattern would be a major evolutionary bottleneck, or other scenario that drastically limited the progenitors of modern prokaryotic diversity at a time considerably after the evolution of a fully functional translation apparatus. The vast range of habitats and metabolisms that prokaryotes occupy today would thus reflect divergent evolution after such a restricting event. Interestingly, phylogenetic analysis places the origin of eukaryotes at about the same time and shows a closer relationship of the eukaryotic ribosome-associated proteins to crenarchaeal rather than euryarchaeal counterparts.

RevDate: 2006-11-15
CmpDate: 2004-09-30

Rivera MC, JA Lake (2004)

The ring of life provides evidence for a genome fusion origin of eukaryotes.

Nature, 431(7005):152-155.

Genomes hold within them the record of the evolution of life on Earth. But genome fusions and horizontal gene transfer seem to have obscured sufficiently the gene sequence record such that it is difficult to reconstruct the phylogenetic tree of life. Here we determine the general outline of the tree using complete genome data from representative prokaryotes and eukaryotes and a new genome analysis method that makes it possible to reconstruct ancient genome fusions and phylogenetic trees. Our analyses indicate that the eukaryotic genome resulted from a fusion of two diverse prokaryotic genomes, and therefore at the deepest levels linking prokaryotes and eukaryotes, the tree of life is actually a ring of life. One fusion partner branches from deep within an ancient photosynthetic clade, and the other is related to the archaeal prokaryotes. The eubacterial organism is either a proteobacterium, or a member of a larger photosynthetic clade that includes the Cyanobacteria and the Proteobacteria.

RevDate: 2010-11-18
CmpDate: 2004-03-18

Jékely G (2003)

Small GTPases and the evolution of the eukaryotic cell.

BioEssays : news and reviews in molecular, cellular and developmental biology, 25(11):1129-1138.

The origin of eukaryotes is one of the major challenges of evolutionary cell biology. Other than the endosymbiotic origin of mitochondria and chloroplasts, the steps leading to eukaryotic endomembranes and endoskeleton are poorly understood. Ras-family small GTPases are key regulators of cytoskeleton dynamics, vesicular trafficking and nuclear function. They are specific for eukaryotes and their expansion probably traces the evolution of core eukaryote features. The phylogeny of small GTPases suggests that the first endomembranes to evolve during eukaryote evolution had secretory, and not phagocytic, function. Based on the reconstruction of putative roles for ancestral small GTPases, a hypothetical scenario on the origins of the first endomembranes, the nucleus, and phagocytosis is presented.

RevDate: 2017-10-27
CmpDate: 2003-07-18

Spring J (2003)

Major transitions in evolution by genome fusions: from prokaryotes to eukaryotes, metazoans, bilaterians and vertebrates.

Journal of structural and functional genomics, 3(1-4):19-25.

The major transitions in human evolution from prokaryotes to eukaryotes, from protozoans to metazoans, from the first animals to bilaterians and finally from a primitive chordate to vertebrates were all accompanied by increases in genome complexity. Rare fusion of divergent genomes rather than continuous single gene duplications could explain these jumps in evolution. The origin of eukaryotes was proposed to be due to a symbiosis of Archaea and Bacteria. Symbiosis is clearly seen as the source for mitochondria. A fundamental difference of higher eukaryotes is the cycle from haploidy to diploidy, a well-regulated genome duplication. Of course, self-fertilization exists, but the potential of sex increases with the difference of the haploid stages, such as the sperm and the egg. What should be the advantage of having two identical copies of a gene? Still, genes duplicate all the time and even genomes duplicate rather often. In plants, polyploidy is well recognized, but seems to be abundant in fungi and even in animals, too. However, hybridization, rather than autopolyploidy, seems to be the potential mechanism for creating something new. The problem with chimaeric, symbiotic or reticulate evolution events is that they blur phylogenetic lineages. Unrecognized paralogous genes or random loss of one of the paralogs in different lineages can lead to false conclusions. Horizontal genome transfer, genome fusion or hybridization might be only truly innovative combined with rare geological transitions such as change to an oxygen atmosphere, snowball Earth events or the Cambrian explosion, but correlates well with the major transitions in evolution.

RevDate: 2009-11-19
CmpDate: 2003-10-16

Watson RA, JB Pollack (2003)

A computational model of symbiotic composition in evolutionary transitions.

Bio Systems, 69(2-3):187-209.

Several of the major transitions in evolutionary history, such as the symbiogenic origin of eukaryotes from prokaryotes, share the feature that existing entities became the components of composite entities at a higher-level of organization. This composition of pre-adapted extant entities into a new whole is a fundamentally different source of variation from the gradual accumulation of small random variations, and it has some interesting consequences for issues of evolvability. Intuitively, the pre-adaptation of sets of features in reproductively independent specialists suggests a form of 'divide and conquer' decomposition of the adaptive domain. Moreover, the compositions resulting from one level may become the components for compositions at the next level, thus scaling-up the variation mechanism. In this paper, we explore and develop these concepts using a simple abstract model of symbiotic composition to examine its impact on evolvability. To exemplify the adaptive capacity of the composition model, we employ a scale-invariant fitness landscape exhibiting significant ruggedness at all scales. Whilst innovation by mutation and by conventional evolutionary algorithms becomes increasingly more difficult as evolution continues in this landscape, innovation by composition is not impeded as it discovers and assembles component entities through successive hierarchical levels.


RJR Experience and Expertise


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.


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.


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.


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.


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.


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.


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.


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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E-mail: RJR8222@gmail.com

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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