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Bibliography on: Origin of Eukaryotes

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ESP: PubMed Auto Bibliography 14 Nov 2022 at 02:01 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: 2022-10-11

Nachmias D, Melnikov N, Zorea A, et al (2022)

Asgard ESCRT-III and VPS4 reveal conserved chromatin binding properties of the ESCRT machinery.

The ISME journal [Epub ahead of print].

The archaeal Asgard superphylum currently stands as the most promising prokaryotic candidate, from which eukaryotic cells emerged. This unique superphylum encodes for eukaryotic signature proteins (ESP) that could shed light on the origin of eukaryotes, but the properties and function of these proteins is largely unresolved. Here, we set to understand the function of an Asgard archaeal protein family, namely the ESCRT machinery, that is conserved across all domains of life and executes basic cellular eukaryotic functions, including membrane constriction during cell division. We find that ESCRT proteins encoded in Loki archaea, express in mammalian and yeast cells, and that the Loki ESCRT-III protein, CHMP4-7, resides in the eukaryotic nucleus in both organisms. Moreover, Loki ESCRT-III proteins associated with chromatin, recruited their AAA-ATPase VPS4 counterpart to organize in discrete foci in the mammalian nucleus, and directly bind DNA. The human ESCRT-III protein, CHMP1B, exhibited similar nuclear properties and recruited both human and Asgard VPS4s to nuclear foci, indicating interspecies interactions. Mutation analysis revealed a role for the N terminal region of ESCRT-III in mediating these phenotypes in both human and Asgard ESCRTs. These findings suggest that ESCRT proteins hold chromatin binding properties that were highly preserved through the billion years of evolution separating Asgard archaea and humans. The conserved chromatin binding properties of the ESCRT membrane remodeling machinery, reported here, may have important implications for the origin of eukaryogenesis.

RevDate: 2022-10-11

Silva VSD, CR Machado (2022)

Sex in protists: A new perspective on the reproduction mechanisms of trypanosomatids.

Genetics and molecular biology, 45(3):e20220065 pii:S1415-47572022000300401.

The Protist kingdom individuals are the most ancestral representatives of eukaryotes. They have inhabited Earth since ancient times and are currently found in the most diverse environments presenting a great heterogeneity of life forms. The unicellular and multicellular algae, photosynthetic and heterotrophic organisms, as well as free-living and pathogenic protozoa represents the protist group. The evolution of sex is directly associated with the origin of eukaryotes being protists the earliest protagonists of sexual reproduction on earth. In eukaryotes, the recombination through genetic exchange is a ubiquitous mechanism that can be stimulated by DNA damage. Scientific evidences support the hypothesis that reactive oxygen species (ROS) induced DNA damage can promote sexual recombination in eukaryotes which might have been a decisive factor for the origin of sex. The fact that some recombination enzymes also participate in meiotic sex in modern eukaryotes reinforces the idea that sexual reproduction emerged as consequence of specific mechanisms to cope with mutations and alterations in genetic material. In this review we will discuss about origin of sex and different strategies of evolve sexual reproduction in some protists such that cause human diseases like malaria, toxoplasmosis, sleeping sickness, Chagas disease, and leishmaniasis.

RevDate: 2022-07-26

Schavemaker PE, M Lynch (2022)

Flagellar energy costs across the tree of life.

eLife, 11: pii:77266.

Flagellar-driven motility grants unicellular organisms the ability to gather more food and avoid predators, but the energetic costs of construction and operation of flagella are considerable. Paths of flagellar evolution depend on the deviations between fitness gains and energy costs. Using structural data available for all three major flagellar types (bacterial, archaeal, and eukaryotic), flagellar construction costs were determined for Escherichia coli, Pyrococcus furiosus, and Chlamydomonas reinhardtii. Estimates of cell volumes, flagella numbers, and flagellum lengths from the literature yield flagellar costs for another ~200 species. The benefits of flagellar investment were analysed in terms of swimming speed, nutrient collection, and growth rate; showing, among other things, that the cost-effectiveness of bacterial and eukaryotic flagella follows a common trend. However, a comparison of whole-cell costs and flagellum costs across the Tree of Life reveals that only cells with larger cell volumes than the typical bacterium could evolve the more expensive eukaryotic flagellum. These findings provide insight into the unsolved evolutionary question of why the three domains of life each carry their own type of flagellum.

RevDate: 2022-06-29

Romei M, Sapriel G, Imbert P, et al (2022)

Protein folds as synapomorphies of the tree of life.

Evolution; international journal of organic evolution [Epub ahead of print].

Several studies showed that folds (topology of protein secondary structures) distribution in proteomes may be a global proxy to build phylogeny. Then, some folds should be synapomorphies (derived characters exclusively shared among taxa). However, previous studies used methods that did not allow synapomorphy identification, which requires congruence analysis of folds as individual characters. Here, we map SCOP folds onto a sample of 210 species across the tree of life (TOL). Congruence is assessed using retention index of each fold for the TOL, and principal component analysis for deeper branches. Using a bicluster mapping approach we define synapomorphic blocks of folds (SBF) sharing similar presence/absence patterns. Among the 1,232 folds, 20% are universally present in our TOL, while 54% are reliable synapomorphies. These results are similar with CATH and ECOD databases. Eukaryotes are characterized by a large number of them, and several SBFs clearly supported nested eukaryotic clades (divergence times from 1,100 to 380 mya). While clearly separated, the three superkingdoms reveal a strong mosaic pattern. This pattern is consistent with the dual origin of eukaryotes, and witness secondary endosymbiosis in their phothosynthetic clades. Our study unveils direct analysis of folds synapomorphies as key characters to unravel evolutionary history of species. This article is protected by copyright. All rights reserved.

RevDate: 2022-02-17

Albers S, Ashmore J, Pollard T, et al (2022)

Origin of eukaryotes: What can be learned from the first successfully isolated Asgard archaeon.

Faculty reviews, 11:3.

The origin of cellular complexity characterizing eukaryotic cells remains a central unresolved issue in the study of diversification of cellular life on Earth. The isolation by Imachi et al.1 of a member of the Asgard archaea2 - a contemporary relative of organisms thought to have given rise to eukaryotic cells about 2 billion years ago - now promises new insight. The complete genome sequence of the isolated Lokiarchaeum strain confirms that the eukaryotic signature proteins (ESPs) previously identified in the Lokiarchaeota3 and other Asgard archaea2 are indeed encoded by these archaeal genomes and do not represent contamination from eukaryotes. These ESPs encode homologs of eukaryotic actins, small GTPases and the ESCRT complex proteins and are required for the functioning of complex eukaryotic cells. The new, slowly growing, anaerobic laboratory strain allows a first direct look at these organisms and provides key insights into the morphology and metabolism of an Asgard archaeal organism. The work has provided valuable information for other laboratories that aim to isolate and characterize related organisms from other environments.

RevDate: 2022-01-06

Aouad M, Flandrois JP, Jauffrit F, et al (2022)

A divide-and-conquer phylogenomic approach based on character supermatrices resolves early steps in the evolution of the Archaea.

BMC ecology and evolution, 22(1):1.

BACKGROUND: The recent rise in cultivation-independent genome sequencing has provided key material to explore uncharted branches of the Tree of Life. This has been particularly spectacular concerning the Archaea, projecting them at the center stage as prominently relevant to understand early stages in evolution and the emergence of fundamental metabolisms as well as the origin of eukaryotes. Yet, resolving deep divergences remains a challenging task due to well-known tree-reconstruction artefacts and biases in extracting robust ancient phylogenetic signal, notably when analyzing data sets including the three Domains of Life. Among the various strategies aimed at mitigating these problems, divide-and-conquer approaches remain poorly explored, and have been primarily based on reconciliation among single gene trees which however notoriously lack ancient phylogenetic signal.

RESULTS: We analyzed sub-sets of full supermatrices covering the whole Tree of Life with specific taxonomic sampling to robustly resolve different parts of the archaeal phylogeny in light of their current diversity. Our results strongly support the existence and early emergence of two main clades, Cluster I and Cluster II, which we name Ouranosarchaea and Gaiarchaea, and we clarify the placement of important novel archaeal lineages within these two clades. However, the monophyly and branching of the fast evolving nanosized DPANN members remains unclear and worth of further study.

CONCLUSIONS: We inferred a well resolved rooted phylogeny of the Archaea that includes all recently described phyla of high taxonomic rank. This phylogeny represents a valuable reference to study the evolutionary events associated to the early steps of the diversification of the archaeal domain. Beyond the specifics of archaeal phylogeny, our results demonstrate the power of divide-and-conquer approaches to resolve deep phylogenetic relationships, which should be applied to progressively resolve the entire Tree of Life.

RevDate: 2021-08-11

Xie R, Wang Y, Huang D, et al (2021)

Expanding Asgard members in the domain of Archaea sheds new light on the origin of eukaryotes.

Science China. Life sciences [Epub ahead of print].

The hypothesis that eukaryotes originated from within the domain Archaea has been strongly supported by recent phylogenomic analyses placing Heimdallarchaeota-Wukongarchaeota branch from the Asgard superphylum as the closest known archaeal sister-group to eukaryotes. However, our understanding is still limited in terms of the relationship between eukaryotes and archaea, as well as the evolution and ecological functions of the Asgard archaea. Here, we describe three previously unknown phylum-level Asgard archaeal lineages, tentatively named Sigyn-, Freyr- and Njordarchaeota. Additional members in Wukongarchaeota and Baldrarchaeota from distinct environments are also reported here, further expanding their ecological roles and metabolic capacities. Comprehensive phylogenomic analyses further supported the origin of eukaryotes within Asgard archaea and a new lineage Njordarchaeota was supposed as the known closest branch with the eukaryotic nuclear host lineage. Metabolic reconstruction suggests that Njordarchaeota may have a heterotrophic lifestyle with capability of peptides and amino acids utilization, while Sigynarchaeota and Freyrarchaeota also have the potentials to fix inorganic carbon via the Wood-Ljungdahl pathway and degrade organic matters. Additionally, the Ack/Pta pathway for homoacetogenesis and de novo anaerobic cobalamin biosynthesis pathway were found in Freyrarchaeota and Wukongrarchaeota, respectively. Some previously unidentified eukaryotic signature proteins for intracellular membrane trafficking system, and the homologue of mu/sigma subunit of adaptor protein complex, were identified in Freyrarchaeota. This study expands the Asgard superphylum, sheds new light on the evolution of eukaryotes and improves our understanding of ecological functions of the Asgard archaea.

RevDate: 2021-08-03

Gabaldón T (2021)

Origin and Early Evolution of the Eukaryotic Cell.

Annual review of microbiology [Epub ahead of print].

The origin of eukaryotes has been defined as the major evolutionary transition since the origin of life itself. Most hallmark traits of eukaryotes, such as their intricate intracellular organization, can be traced back to a putative common ancestor that predated the broad diversity of extant eukaryotes. However, little is known about the nature and relative order of events that occurred in the path from preexisting prokaryotes to this already sophisticated ancestor. The origin of mitochondria from the endosymbiosis of an alphaproteobacterium is one of the few robustly established events to which most hypotheses on the origin of eukaryotes are anchored, but the debate is still open regarding the time of this acquisition, the nature of the host, and the ecological and metabolic interactions between the symbiotic partners. After the acquisition of mitochondria, eukaryotes underwent a fast radiation into several major clades whose phylogenetic relationships have been largely elusive. Recent progress in the comparative analyses of a growing number of genomes is shedding light on the early events of eukaryotic evolution as well as on the root and branching patterns of the tree of eukaryotes. Here I discuss current knowledge and debates on the origin and early evolution of eukaryotes. I focus particularly on how phylogenomic analyses have challenged some of the early assumptions about eukaryotic evolution, including the widespread idea that mitochondrial symbiosis in an archaeal host was the earliest event in eukaryogenesis. Expected final online publication date for the Annual Review of Microbiology, Volume 75 is October 2021. Please see for revised estimates.

RevDate: 2021-07-29

Skejo J, Garg SG, Gould SB, et al (2021)

Evidence for a Syncytial Origin of Eukaryotes from Ancestral State Reconstruction.

Genome biology and evolution, 13(7):.

Modern accounts of eukaryogenesis entail an endosymbiotic encounter between an archaeal host and a proteobacterial endosymbiont, with subsequent evolution giving rise to a unicell possessing a single nucleus and mitochondria. The mononucleate state of the last eukaryotic common ancestor (LECA) is seldom, if ever, questioned, even though cells harboring multiple (syncytia, coenocytes, and polykaryons) are surprisingly common across eukaryotic supergroups. Here, we present a survey of multinucleated forms. Ancestral character state reconstruction for representatives of 106 eukaryotic taxa using 16 different possible roots and supergroup sister relationships, indicate that LECA, in addition to being mitochondriate, sexual, and meiotic, was multinucleate. LECA exhibited closed mitosis, which is the rule for modern syncytial forms, shedding light on the mechanics of its chromosome segregation. A simple mathematical model shows that within LECA's multinucleate cytosol, relationships among mitochondria and nuclei were neither one-to-one, nor one-to-many, but many-to-many, placing mitonuclear interactions and cytonuclear compatibility at the evolutionary base of eukaryotic cell origin. Within a syncytium, individual nuclei and individual mitochondria function as the initial lower-level evolutionary units of selection, as opposed to individual cells, during eukaryogenesis. Nuclei within a syncytium rescue each other's lethal mutations, thereby postponing selection for viable nuclei and cytonuclear compatibility to the generation of spores, buffering transitional bottlenecks at eukaryogenesis. The prokaryote-to-eukaryote transition is traditionally thought to have left no intermediates, yet if eukaryogenesis proceeded via a syncytial common ancestor, intermediate forms have persisted to the present throughout the eukaryotic tree as syncytia but have so far gone unrecognized.

RevDate: 2021-05-26

Liu Y, Makarova KS, Huang WC, et al (2021)

Expanded diversity of Asgard archaea and their relationships with eukaryotes.

Nature, 593(7860):553-557.

Asgard is a recently discovered superphylum of archaea that appears to include the closest archaeal relatives of eukaryotes1-5. Debate continues as to whether the archaeal ancestor of eukaryotes belongs within the Asgard superphylum or whether this ancestor is a sister group to all other archaea (that is, a two-domain versus a three-domain tree of life)6-8. Here we present a comparative analysis of 162 complete or nearly complete genomes of Asgard archaea, including 75 metagenome-assembled genomes that-to our knowledge-have not previously been reported. Our results substantially expand the phylogenetic diversity of Asgard and lead us to propose six additional phyla that include a deep branch that we have provisionally named Wukongarchaeota. Our phylogenomic analysis does not resolve unequivocally the evolutionary relationship between eukaryotes and Asgard archaea, but instead-depending on the choice of species and conserved genes used to build the phylogeny-supports either the origin of eukaryotes from within Asgard (as a sister group to the expanded Heimdallarchaeota-Wukongarchaeota branch) or a deeper branch for the eukaryote ancestor within archaea. Our comprehensive protein domain analysis using the 162 Asgard genomes results in a major expansion of the set of eukaryotic signature proteins. The Asgard eukaryotic signature proteins show variable phyletic distributions and domain architectures, which is suggestive of dynamic evolution through horizontal gene transfer, gene loss, gene duplication and domain shuffling. The phylogenomics of the Asgard archaea points to the accumulation of the components of the mobile archaeal 'eukaryome' in the archaeal ancestor of eukaryotes (within or outside Asgard) through extensive horizontal gene transfer.

RevDate: 2021-05-20

Nasir A, Mughal F, G Caetano-Anollés (2021)

The tree of life describes a tripartite cellular world.

BioEssays : news and reviews in molecular, cellular and developmental biology, 43(6):e2000343.

The canonical view of a 3-domain (3D) tree of life was recently challenged by the discovery of Asgardarchaeota encoding eukaryote signature proteins (ESPs), which were treated as missing links of a 2-domain (2D) tree. Here we revisit the debate. We discuss methodological limitations of building trees with alignment-dependent approaches, which often fail to satisfactorily address the problem of ''gaps.'' In addition, most phylogenies are reconstructed unrooted, neglecting the power of direct rooting methods. Alignment-free methodologies lift most difficulties but require employing realistic evolutionary models. We argue that the discoveries of Asgards and ESPs, by themselves, do not rule out the 3D tree, which is strongly supported by comparative and evolutionary genomic analyses and vast genomic and biochemical superkingdom distinctions. Given uncertainties of retrodiction and interpretation difficulties, we conclude that the 3D view has not been falsified but instead has been strengthened by genomic analyses. In turn, the objections to the 2D model have not been lifted. The debate remains open. Also see the video abstract here:

RevDate: 2021-04-30

Lazcano A, J Peretó (2021)

Prokaryotic symbiotic consortia and the origin of nucleated cells: A critical review of Lynn Margulis hypothesis.

Bio Systems, 204:104408.

The publication in the late 1960s of Lynn Margulis endosymbiotic proposal is a scientific milestone that brought to the fore of evolutionary discussions the issue of the origin of nucleated cells. Although it is true that the times were ripe, the timely publication of Lynn Margulis' original paper was the product of an intellectually bold 29-years old scientist, who based on the critical analysis of the available scientific information produced an all-encompassing, sophisticated narrative scheme on the origin of eukaryotic cells as a result of the evolution of prokaryotic consortia and, in bold intellectual stroke, put it all in the context of planetary evolution. A critical historical reassessment of her original proposal demonstrates that her hypothesis was not a simple archival outline of past schemes, but a renewed historical narrative of prokaryotic evolution and the role of endosymbiosis in the origin of eukaryotes. Although it is now accepted that the closest bacterial relatives of mitochondria and plastids are α-proteobacteria and cyanobacteria, respectively, comparative genomics demonstrates the mosaic character of the organelle genomes. The available evidence has completely refuted Margulis' proposal of an exogenous origin for eukaryotic flagella, the (9 + 2) basal bodies, and centromeres, but we discuss in detail the reasons that led her to devote considerable efforts to argue for a symbiotic origin of the eukaryotic motility. An analysis of the arguments successfully employed by Margulis in her persuasive advocacy of endosymbiosis, combined with the discussions of her flaws and the scientific atmosphere during the period in which she formulated her proposals, are critical for a proper appraisal of the historical conditions that shaped her theory and its acceptance.

RevDate: 2021-09-25

Carlisle EM, Jobbins M, Pankhania V, et al (2021)

Experimental taphonomy of organelles and the fossil record of early eukaryote evolution.

Science advances, 7(5):.

The timing of origin of eukaryotes and the sequence of eukaryogenesis are poorly constrained because their fossil record is difficult to interpret. Claims of fossilized organelles have been discounted on the unsubstantiated perception that they decay too quickly for fossilization. We experimentally characterized the pattern and time scale of decay of nuclei, chloroplasts, and pyrenoids in red and green algae, demonstrating that they persist for many weeks postmortem as physical substrates available for preservation, a time scale consistent with known mechanisms of fossilization. Chloroplasts exhibit greater decay resistance than nuclei; pyrenoids are unlikely to be preserved, but their presence could be inferred from spaces within fossil chloroplasts. Our results are compatible with differential organelle preservation in seed plants. Claims of fossilized organelles in Proterozoic fossils can no longer be dismissed on grounds of plausibility, prompting reinterpretation of the early eukaryotic fossil record and the prospect of a fossil record of eukaryogenesis.

RevDate: 2021-05-13

Collens AB, LA Katz (2021)

Opinion: Genetic Conflict With Mobile Elements Drives Eukaryotic Genome Evolution, and Perhaps Also Eukaryogenesis.

The Journal of heredity, 112(1):140-144.

Through analyses of diverse microeukaryotes, we have previously argued that eukaryotic genomes are dynamic systems that rely on epigenetic mechanisms to distinguish germline (i.e., DNA to be inherited) from soma (i.e., DNA that undergoes polyploidization, genome rearrangement, etc.), even in the context of a single nucleus. Here, we extend these arguments by including two well-documented observations: (1) eukaryotic genomes interact frequently with mobile genetic elements (MGEs) like viruses and transposable elements (TEs), creating genetic conflict, and (2) epigenetic mechanisms regulate MGEs. Synthesis of these ideas leads to the hypothesis that genetic conflict with MGEs contributed to the evolution of a dynamic eukaryotic genome in the last eukaryotic common ancestor (LECA), and may have contributed to eukaryogenesis (i.e., may have been a driver in the evolution of FECA, the first eukaryotic common ancestor). Sex (i.e., meiosis) may have evolved within the context of the development of germline-soma distinctions in LECA, as this process resets the germline genome by regulating/eliminating somatic (i.e., polyploid, rearranged) genetic material. Our synthesis of these ideas expands on hypotheses of the origin of eukaryotes by integrating the roles of MGEs and epigenetics.

RevDate: 2021-01-30

Kowallik KV, WF Martin (2021)

The origin of symbiogenesis: An annotated English translation of Mereschkowsky's 1910 paper on the theory of two plasma lineages.

Bio Systems, 199:104281.

In 1910, the Russian biologist Konstantin Sergejewitch Mereschkowsky (Константин Сергеевич Мережковский, in standard transliterations also written as Konstantin Sergeevič Merežkovskij and Konstantin Sergeevich Merezhkovsky) published a notable synthesis of observations and inferences concerning the origin of life and the origin of nucleated cells. His theory was based on physiology and leaned heavily upon the premise that thermophilic autotrophs were ancient. The ancestors of plants and animals were inferred as ancestrally mesophilic anucleate heterotrophs (Monera) that became complex and diverse through endosymbiosis. He placed a phylogenetic root in the tree of life among anaerobic autotrophic bacteria that lack chlorophyll. His higher level classification of all microbes and macrobes in the living world was based upon the presence or absence of past endosymbiotic events. The paper's primary aim was to demonstrate that all life forms descend from two fundamentally distinct organismal lineages, called mykoplasma and amoeboplasma, whose very nature was so different that, in his view, they could only have arisen independently of one another and at different times during Earth history. The mykoplasma arose at a time when the young Earth was still hot, it later gave rise to cyanobacteria, which in turn gave rise to plastids. The product of the second origin of life, the amoeboplasma, arose after the Earth had cooled and autotrophs had generated substrates for heterotrophic growth. Lineage diversification of that second plasma brought forth, via serial endosymbioses, animals (one symbiosis) and then plants (two symbioses, the second being the plastid). The paper was published in German, rendering it inaccessible to many interested scholars. Here we translate the 1910 paper in full and briefly provide some context.

RevDate: 2021-01-06
CmpDate: 2021-01-06

Gao ZW, L Wang (2020)

[Progress in elucidating the origin of eukaryotes].

Yi chuan = Hereditas, 42(10):929-948.

Knowledge of the origin of eukaryotes is key to broadening our understanding of the eukaryotic genome and the relationship among internal structures within a eukaryotic cell. Since the discovery of archaea in 1977 and the proposal of three-domain tree of life by the American microbiologist Carl Woese, the intimate relationship in evolution between eukaryotes and archaea has been demonstrated by considerable experiments and analyses. From the beginning of the 21st century, with the development of phylogenetic methods and the discovery of new archaeal phyla more related to eukaryotes, increasing evidence has shown that Eukarya and Archaea should be merged into one domain, leading to a two-domain tree of life. Nowadays, the Asgard superphylum discovered via metagenomic analysis is regarded as the closest prokaryotes to eukaryotes. Nevertheless, several key questions are still under debate, such as what the ancestors of the eukaryotes were and when mitochondria emerged. Here, we review the current research progress regarding the changes of the tree of life and the detailed eukaryotic evolutionary mechanism. We show that the recent findings have greatly improved our knowledge on the origin of eukaryotes, which will pave the way for future studies.

RevDate: 2021-01-12
CmpDate: 2021-01-12

Cai M, Richter-Heitmann T, Yin X, et al (2021)

Ecological features and global distribution of Asgard archaea.

The Science of the total environment, 758:143581.

Asgard is a newly proposed archaeal superphylum, which has been suggested to hold the key to decipher the origin of Eukaryotes. However, their ecology remains largely unknown. Here, we conducted a meta-analysis of publicly available Asgard-associated 16S rRNA gene fragments, and found that just three previously proposed clades (Lokiarchaeota, Thorarchaeota, and Asgard clade 4) are widely distributed, whereas the other seven clades (phylum or class level) are restricted to the sediment biosphere. Asgard archaea, especially Loki- and Thorarchaeota, seem to adapt to marine sediments, and water depth (the depth of the sediment below water surface) and salinity might be crucial factors for the proportion of these microorganisms as revealed by multivariate regression analyses. However, the abundance of Asgard archaea exhibited distinct environmental drivers at the clade-level; for instance, the proportion of Asgard clade 4 was higher in less saline environments (salinity <6.35 psu), while higher for Heimdallarchaeota-AAG and Asgard clade 2 in more saline environment (salinity ≥35 psu). Furthermore, co-occurrence analysis allowed us to find a significant non-random association of different Asgard clades with other groups (e.g., Lokiarchaeota with Deltaproteobacteria and Anaerolineae; Odinarchaeota with Bathyarchaeota), suggesting different interaction potentials among these clades. Overall, these findings reveal Asgard archaea as a ubiquitous group worldwide and provide initial insights into their ecological features on a global scale.

RevDate: 2021-09-07
CmpDate: 2021-09-07

Schrumpfová PP, J Fajkus (2020)

Composition and Function of Telomerase-A Polymerase Associated with the Origin of Eukaryotes.

Biomolecules, 10(10):.

The canonical DNA polymerases involved in the replication of the genome are unable to fully replicate the physical ends of linear chromosomes, called telomeres. Chromosomal termini thus become shortened in each cell cycle. The maintenance of telomeres requires telomerase-a specific RNA-dependent DNA polymerase enzyme complex that carries its own RNA template and adds telomeric repeats to the ends of chromosomes using a reverse transcription mechanism. Both core subunits of telomerase-its catalytic telomerase reverse transcriptase (TERT) subunit and telomerase RNA (TR) component-were identified in quick succession in Tetrahymena more than 30 years ago. Since then, both telomerase subunits have been described in various organisms including yeasts, mammals, birds, reptiles and fish. Despite the fact that telomerase activity in plants was described 25 years ago and the TERT subunit four years later, a genuine plant TR has only recently been identified by our group. In this review, we focus on the structure, composition and function of telomerases. In addition, we discuss the origin and phylogenetic divergence of this unique RNA-dependent DNA polymerase as a witness of early eukaryotic evolution. Specifically, we discuss the latest information regarding the recently discovered TR component in plants, its conservation and its structural features.

RevDate: 2021-09-25

Stairs CW, Dharamshi JE, Tamarit D, et al (2020)

Chlamydial contribution to anaerobic metabolism during eukaryotic evolution.

Science advances, 6(35):eabb7258.

The origin of eukaryotes is a major open question in evolutionary biology. Multiple hypotheses posit that eukaryotes likely evolved from a syntrophic relationship between an archaeon and an alphaproteobacterium based on H2 exchange. However, there are no strong indications that modern eukaryotic H2 metabolism originated from archaea or alphaproteobacteria. Here, we present evidence for the origin of H2 metabolism genes in eukaryotes from an ancestor of the Anoxychlamydiales-a group of anaerobic chlamydiae, newly described here, from marine sediments. Among Chlamydiae, these bacteria uniquely encode genes for H2 metabolism and other anaerobiosis-associated pathways. Phylogenetic analyses of several components of H2 metabolism reveal that Anoxychlamydiales homologs are the closest relatives to eukaryotic sequences. We propose that an ancestor of the Anoxychlamydiales contributed these key genes during the evolution of eukaryotes, supporting a mosaic evolutionary origin of eukaryotic metabolism.

RevDate: 2021-04-12
CmpDate: 2021-04-12

Feltrin RDS, Segatto ALA, de Souza TA, et al (2020)

Open gaps in the evolution of the eukaryotic nucleotide excision repair.

DNA repair, 95:102955.

Nucleotide excision repair (NER) is the most versatile DNA repair pathway as it removes different kinds of bulky lesions. Due to its essential role for genome integrity, it has appeared early in the evolution of species. However, most published studies are focused on humans, mice, yeast or bacteria. Considering the large amount of information on genome databases, it is currently possible to retrieve sequences from NER components in many organisms. Therefore, we have characterized the potential orthologs of 10 critical components of the human NER pathway in 12 eukaryotic species by using similarity and structural criteria through the use of bioinformatics tools. This approach has allowed us to characterize gene and protein structures comparatively, taking a glance at some evolutionary aspects of the NER pathway. We have obtained significant search results for the majority of the proteins in most of the organisms studied, mainly for factors that play a pivotal role in the pathway. However, we have revisited significant differences and found new aspects that may imply a distinct functioning of this pathway in different organisms. Through the demonstration of the heterogeneity of the gene structures and a variety in the protein architecture of the NER components evaluated, our results show important differences between human NER and evolutionarily distant eukaryotes. We highlight the lack of a canonical XPD in chicken, the divergence of XPA in plants and protozoans and the absence of XPE in the invertebrate species analyzed. In spite of this, it is remarkable the presence of this excision repair mechanism in a high number of evolutionary distant organisms, being present since the origin of eukaryotes.

RevDate: 2021-08-17
CmpDate: 2021-08-17

Lane N (2020)

How energy flow shapes cell evolution.

Current biology : CB, 30(10):R471-R476.

How mitochondria shaped the evolution of eukaryotic complexity has been controversial for decades. The discovery of the Asgard archaea, which harbor close phylogenetic ties to the eukaryotes, supports the idea that a critical endosymbiosis between an archaeal host and a bacterial endosymbiont transformed the selective constraints present at the origin of eukaryotes. Cultured Asgard archaea are typically prokaryotic in both size and internal morphology, albeit featuring extensive protrusions. The acquisition of the mitochondrial predecessor by an archaeal host cell fundamentally altered the topology of genes in relation to bioenergetic membranes. Mitochondria internalised not only the bioenergetic membranes but also the genetic machinery needed for local control of oxidative phosphorylation. Gene loss from mitochondria enabled expansion of the nuclear genome, giving rise to an extreme genomic asymmetry that is ancestral to all extant eukaryotes. This genomic restructuring gave eukaryotes thousands of fold more energy availability per gene. In principle, that difference can support more and larger genes, far more non-coding DNA, greater regulatory complexity, and thousands of fold more protein synthesis per gene. These changes released eukaryotes from the bioenergetic constraints on prokaryotes, facilitating the evolution of morphological complexity.

RevDate: 2021-07-31
CmpDate: 2020-10-20

Baker BJ, De Anda V, Seitz KW, et al (2020)

Diversity, ecology and evolution of Archaea.

Nature microbiology, 5(7):887-900.

Compared to bacteria, our knowledge of archaeal biology is limited. Historically, microbiologists have mostly relied on culturing and single-gene diversity surveys to understand Archaea in nature. However, only six of the 27 currently proposed archaeal phyla have cultured representatives. Advances in genomic sequencing and computational approaches are revolutionizing our understanding of Archaea. The recovery of genomes belonging to uncultured groups from the environment has resulted in the description of several new phyla, many of which are globally distributed and are among the predominant organisms on the planet. In this Review, we discuss how these genomes, together with long-term enrichment studies and elegant in situ measurements, are providing insights into the metabolic capabilities of the Archaea. We also debate how such studies reveal how important Archaea are in mediating an array of ecological processes, including global carbon and nutrient cycles, and how this increase in archaeal diversity has expanded our view of the tree of life and early archaeal evolution, and has provided new insights into the origin of eukaryotes.

RevDate: 2020-10-27
CmpDate: 2020-10-27

Bateman A (2020)

Division of labour in a matrix, rather than phagocytosis or endosymbiosis, as a route for the origin of eukaryotic cells.

Biology direct, 15(1):8.

Two apparently irreconcilable models dominate research into the origin of eukaryotes. In one model, amitochondrial proto-eukaryotes emerged autogenously from the last universal common ancestor of all cells. Proto-eukaryotes subsequently acquired mitochondrial progenitors by the phagocytic capture of bacteria. In the second model, two prokaryotes, probably an archaeon and a bacterial cell, engaged in prokaryotic endosymbiosis, with the species resident within the host becoming the mitochondrial progenitor. Both models have limitations. A search was therefore undertaken for alternative routes towards the origin of eukaryotic cells. The question was addressed by considering classes of potential pathways from prokaryotic to eukaryotic cells based on considerations of cellular topology. Among the solutions identified, one, called here the "third-space model", has not been widely explored. A version is presented in which an extracellular space (the third-space), serves as a proxy cytoplasm for mixed populations of archaea and bacteria to "merge" as a transitionary complex without obligatory endosymbiosis or phagocytosis and to form a precursor cell. Incipient nuclei and mitochondria diverge by division of labour. The third-space model can accommodate the reorganization of prokaryote-like genomes to a more eukaryote-like genome structure. Nuclei with multiple chromosomes and mitosis emerge as a natural feature of the model. The model is compatible with the loss of archaeal lipid biochemistry while retaining archaeal genes and provides a route for the development of membranous organelles such as the Golgi apparatus and endoplasmic reticulum. Advantages, limitations and variations of the "third-space" models are discussed. REVIEWERS: This article was reviewed by Damien Devos, Buzz Baum and Michael Gray.

RevDate: 2021-02-23
CmpDate: 2020-07-27

López-García P, D Moreira (2020)

The Syntrophy hypothesis for the origin of eukaryotes revisited.

Nature microbiology, 5(5):655-667.

The discovery of Asgard archaea, phylogenetically closer to eukaryotes than other archaea, together with improved knowledge of microbial ecology, impose new constraints on emerging models for the origin of the eukaryotic cell (eukaryogenesis). Long-held views are metamorphosing in favour of symbiogenetic models based on metabolic interactions between archaea and bacteria. These include the classical Searcy's and Hydrogen hypothesis, and the more recent Reverse Flow and Entangle-Engulf-Endogenize models. Two decades ago, we put forward the Syntrophy hypothesis for the origin of eukaryotes based on a tripartite metabolic symbiosis involving a methanogenic archaeon (future nucleus), a fermentative myxobacterial-like deltaproteobacterium (future eukaryotic cytoplasm) and a metabolically versatile methanotrophic alphaproteobacterium (future mitochondrion). A refined version later proposed the evolution of the endomembrane and nuclear membrane system by invagination of the deltaproteobacterial membrane. Here, we adapt the Syntrophy hypothesis to contemporary knowledge, shifting from the original hydrogen and methane-transfer-based symbiosis (HM Syntrophy) to a tripartite hydrogen and sulfur-transfer-based model (HS Syntrophy). We propose a sensible ecological scenario for eukaryogenesis in which eukaryotes originated in early Proterozoic microbial mats from the endosymbiosis of a hydrogen-producing Asgard archaeon within a complex sulfate-reducing deltaproteobacterium. Mitochondria evolved from versatile, facultatively aerobic, sulfide-oxidizing and, potentially, anoxygenic photosynthesizing alphaproteobacterial endosymbionts that recycled sulfur in the consortium. The HS Syntrophy hypothesis accounts for (endo)membrane, nucleus and metabolic evolution in a realistic ecological context. We compare and contrast the HS Syntrophy hypothesis to other models of eukaryogenesis, notably in terms of the mode and tempo of eukaryotic trait evolution, and discuss several model predictions and how these can be tested.

RevDate: 2020-07-24
CmpDate: 2020-07-24

Cai M, Liu Y, Yin X, et al (2020)

Diverse Asgard archaea including the novel phylum Gerdarchaeota participate in organic matter degradation.

Science China. Life sciences, 63(6):886-897.

Asgard is an archaeal superphylum that might hold the key to understand the origin of eukaryotes, but its diversity and ecological roles remain poorly understood. Here, we reconstructed 15 metagenomic-assembled genomes from coastal sediments covering most known Asgard archaea and a novel group, which is proposed as a new Asgard phylum named as the "Gerdarchaeota". Genomic analyses predict that Gerdarchaeota are facultative anaerobes in utilizing both organic and inorganic carbon. Unlike their closest relatives Heimdallarchaeota, Gerdarchaeota have genes encoding for cellulase and enzymes involved in the tetrahydromethanopterin-based Wood-Ljungdahl pathway. Transcriptomics showed that most of our identified Asgard archaea are capable of degrading organic matter, including peptides, amino acids and fatty acids, occupying ecological niches in different depths of layers of the sediments. Overall, this study broadens the diversity of the mysterious Asgard archaea and provides evidence for their ecological roles in coastal sediments.

RevDate: 2020-09-28

Schäffer DE, Iyer LM, Burroughs AM, et al (2020)

Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum.

Frontiers in genetics, 11:34.

The origin of eukaryotes was marked by the emergence of several novel subcellular systems. One such is the calcium (Ca2+)-stores system of the endoplasmic reticulum, which profoundly influences diverse aspects of cellular function including signal transduction, motility, division, and biomineralization. We use comparative genomics and sensitive sequence and structure analyses to investigate the evolution of this system. Our findings reconstruct the core form of the Ca2+-stores system in the last eukaryotic common ancestor as having at least 15 proteins that constituted a basic system for facilitating both Ca2+ flux across endomembranes and Ca2+-dependent signaling. We present evidence that the key EF-hand Ca2+-binding components had their origins in a likely bacterial symbiont other than the mitochondrial progenitor, whereas the protein phosphatase subunit of the ancestral calcineurin complex was likely inherited from the asgard archaeal progenitor of the stem eukaryote. This further points to the potential origin of the eukaryotes in a Ca2+-rich biomineralized environment such as stromatolites. We further show that throughout eukaryotic evolution there were several acquisitions from bacteria of key components of the Ca2+-stores system, even though no prokaryotic lineage possesses a comparable system. Further, using quantitative measures derived from comparative genomics we show that there were several rounds of lineage-specific gene expansions, innovations of novel gene families, and gene losses correlated with biological innovation such as the biomineralized molluscan shells, coccolithophores, and animal motility. The burst of innovation of new genes in animals included the wolframin protein associated with Wolfram syndrome in humans. We show for the first time that it contains previously unidentified Sel1, EF-hand, and OB-fold domains, which might have key roles in its biochemistry.

RevDate: 2021-08-18
CmpDate: 2020-05-07

Imachi H, Nobu MK, Nakahara N, et al (2020)

Isolation of an archaeon at the prokaryote-eukaryote interface.

Nature, 577(7791):519-525.

The origin of eukaryotes remains unclear1-4. Current data suggest that eukaryotes may have emerged from an archaeal lineage known as 'Asgard' archaea5,6. Despite the eukaryote-like genomic features that are found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear, owing to the lack of cultured representatives and corresponding physiological insights. Here we report the decade-long isolation of an Asgard archaeon related to Lokiarchaeota from deep marine sediment. The archaeon-'Candidatus Prometheoarchaeum syntrophicum' strain MK-D1-is an anaerobic, extremely slow-growing, small coccus (around 550 nm in diameter) that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexes have been proposed for Asgard archaea6, the isolate has no visible organelle-like structure. Instead, Ca. P. syntrophicum is morphologically complex and has unique protrusions that are long and often branching. On the basis of the available data obtained from cultivation and genomics, and reasoned interpretations of the existing literature, we propose a hypothetical model for eukaryogenesis, termed the entangle-engulf-endogenize (also known as E3) model.

RevDate: 2020-02-20
CmpDate: 2020-02-20

Caspermeyer J (2020)

Scientists Identify Rare Evolutionary Intermediates That Help to Understand the Origin of Eukaryotes.

Molecular biology and evolution, 37(1):305-306.

RevDate: 2021-07-31
CmpDate: 2020-07-16

Orsi WD, Vuillemin A, Rodriguez P, et al (2020)

Metabolic activity analyses demonstrate that Lokiarchaeon exhibits homoacetogenesis in sulfidic marine sediments.

Nature microbiology, 5(2):248-255.

The genomes of the Asgard superphylum of Archaea hold clues pertaining to the nature of the host cell that acquired the mitochondrion at the origin of eukaryotes1-4. Representatives of the Asgard candidate phylum Candidatus Lokiarchaeota (Lokiarchaeon) have the capacity for acetogenesis and fermentation5-7, but how their metabolic activity responds to environmental conditions is poorly understood. Here, we show that in anoxic Namibian shelf sediments, Lokiarchaeon gene expression levels are higher than those of bacterial phyla and increase with depth below the seafloor. Lokiarchaeon gene expression was significantly different across a hypoxic-sulfidic redox gradient, whereby genes involved in growth, fermentation and H2-dependent carbon fixation had the highest expression under the most reducing (sulfidic) conditions. Quantitative stable isotope probing revealed that anaerobic utilization of CO2 and diatomaceous extracellular polymeric substances by Lokiarchaeon was higher than the bacterial average, consistent with higher expression of Lokiarchaeon genes, including those involved in transport and fermentation of sugars and amino acids. The quantitative stable isotope probing and gene expression data demonstrate homoacetogenic activity of Candidatus Lokiarchaeota, whereby fermentative H2 production from organic substrates is coupled with the Wood-Ljungdahl carbon fixation pathway8. The high energetic efficiency provided by homoacetogenesis8 helps to explain the elevated metabolic activity of Lokiarchaeon in this anoxic, energy-limited setting.

RevDate: 2021-08-27
CmpDate: 2021-08-27

Divarathna MVM, Rafeek RAM, F Noordeen (2020)

A review on epidemiology and impact of human metapneumovirus infections in children using TIAB search strategy on PubMed and PubMed Central articles.

Reviews in medical virology, 30(1):e2090.

Acute respiratory tract infections (ARTI) contribute to morbidity and mortality in children globally. Viruses including human metapneumovirus (hMPV) account for most ARTIs. The virus causes upper and lower respiratory tract infections mostly in young children and contributes to hospitalization of individuals with asthma,chronic obstructive pulmonary diseases and cancer. Moreover, hMPV pauses a considerable socio-economic impact creating a substantial disease burden wherever it has been studied, although hMPV testing is relatively new in many countries. We aimed to comprehensively analyze the epidemiological aspects including prevalence, disease burden and seasonality of hMPV infections in children in the world. We acquired published data extracted from PubMed and PubMed Central articles using the title and abstract (TIAB)search strategy for the major key words on hMPV infections from 9/54 African, 11/35 American, 20/50 Asian, 2/14 Australian/Oceanian and 20/51 European countries. According to the findings of this review, the prevalence of hMPV infection ranges from 1.1 to 86% in children of less than 5 years of age globally. Presence of many hMPV genotypes (A1, A2, B1, B2) and sub-genotypes (A2a, A2b, A2c, B2a, B2b) suggests a rapid evolution of the virus with limited influence by time and geography. hMPV infection mostly affects children between 2 to 5 years of age. The virus is active throughout the year in the tropics and epidemics occur during the winter and spring in temperate climates, contributing to a substantial disease burden globally.

RevDate: 2020-11-25
CmpDate: 2020-06-17

Keeling PJ (2019)

Combining morphology, behaviour and genomics to understand the evolution and ecology of microbial eukaryotes.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 374(1786):20190085.

Microbial eukaryotes (protists) are structurally, developmentally and behaviourally more complex than their prokaryotic cousins. This complexity makes it more difficult to translate genomic and metagenomic data into accurate functional inferences about systems ranging all the way from molecular and cellular levels to global ecological networks. This problem can be traced back to the advent of the cytoskeleton and endomembrane systems at the origin of eukaryotes, which endowed them with a range of complex structures and behaviours that still largely dominate how they evolve and interact within microbial communities. But unlike the diverse metabolic properties that evolved within prokaryotes, the structural and behavioural characteristics that strongly define how protists function in the environment cannot readily be inferred from genomic data, since there is generally no simple correlation between a gene and a discrete activity or function. A deeper understanding of protists at both cellular and ecological levels, therefore, requires not only high-throughput genomics but also linking such data to direct observations of natural history and cell biology. This is challenging since these observations typically require cultivation, which is lacking for most protists. Potential remedies with current technology include developing a more phylogenetically diverse range of model systems to better represent the diversity, as well as combining high-throughput, single-cell genomics with microscopic documentation of the subject cells to link sequence with structure and behaviour. This article is part of a discussion meeting issue 'Single cell ecology'.

RevDate: 2020-06-30
CmpDate: 2020-06-30

Brunk CF, WF Martin (2019)

Archaeal Histone Contributions to the Origin of Eukaryotes.

Trends in microbiology, 27(8):703-714.

The eukaryotic lineage arose from bacterial and archaeal cells that underwent a symbiotic merger. At the origin of the eukaryote lineage, the bacterial partner contributed genes, metabolic energy, and the building blocks of the endomembrane system. What did the archaeal partner donate that made the eukaryotic experiment a success? The archaeal partner provided the potential for complex information processing. Archaeal histones were crucial in that regard by providing the basic functional unit with which eukaryotes organize DNA into nucleosomes, exert epigenetic control of gene expression, transcribe genes with CCAAT-box promoters, and a manifest cell cycle with condensed chromosomes. While mitochondrial energy lifted energetic constraints on eukaryotic protein production, histone-based chromatin organization paved the path to eukaryotic genome complexity, a critical hurdle en route to the evolution of complex cells.

RevDate: 2019-11-15
CmpDate: 2019-09-13

Spang A, Stairs CW, Dombrowski N, et al (2019)

Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism.

Nature microbiology, 4(7):1138-1148.

The origin of eukaryotes represents an unresolved puzzle in evolutionary biology. Current research suggests that eukaryotes evolved from a merger between a host of archaeal descent and an alphaproteobacterial endosymbiont. The discovery of the Asgard archaea, a proposed archaeal superphylum that includes Lokiarchaeota, Thorarchaeota, Odinarchaeota and Heimdallarchaeota suggested to comprise the closest archaeal relatives of eukaryotes, has helped to elucidate the identity of the putative archaeal host. Whereas Lokiarchaeota are assumed to employ a hydrogen-dependent metabolism, little is known about the metabolic potential of other members of the Asgard superphylum. We infer the central metabolic pathways of Asgard archaea using comparative genomics and phylogenetics to be able to refine current models for the origin of eukaryotes. Our analyses indicate that Thorarchaeota and Lokiarchaeota encode proteins necessary for carbon fixation via the Wood-Ljungdahl pathway and for obtaining reducing equivalents from organic substrates. By contrast, Heimdallarchaeum LC2 and LC3 genomes encode enzymes potentially enabling the oxidation of organic substrates using nitrate or oxygen as electron acceptors. The gene repertoire of Heimdallarchaeum AB125 and Odinarchaeum indicates that these organisms can ferment organic substrates and conserve energy by coupling ferredoxin reoxidation to respiratory proton reduction. Altogether, our genome analyses suggest that Asgard representatives are primarily organoheterotrophs with variable capacity for hydrogen consumption and production. On this basis, we propose the 'reverse flow model', an updated symbiogenetic model for the origin of eukaryotes that involves electron or hydrogen flow from an organoheterotrophic archaeal host to a bacterial symbiont.

RevDate: 2019-08-20
CmpDate: 2019-08-20

Gabaldón T (2018)

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

IUBMB life, 70(12):1188-1196.

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 The Authors. IUBMB Life published by Wiley Periodicals, Inc. on behalf of International Union of Biochemistry and Molecular Biology, 70(12):1188-1196, 2018.

RevDate: 2019-02-15
CmpDate: 2019-02-04

Río Bártulos C, Rogers MB, Williams TA, et al (2018)

Mitochondrial Glycolysis in a Major Lineage of Eukaryotes.

Genome biology and evolution, 10(9):2310-2325.

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 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: 2020-10-13
CmpDate: 2019-10-01

Kauko A, K Lehto (2018)

Eukaryote specific folds: Part of the whole.

Proteins, 86(8):868-881.

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: 2019-03-25
CmpDate: 2019-03-25

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.

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: 2019-11-20

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: 2018-08-06
CmpDate: 2018-08-06

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: 2021-01-09
CmpDate: 2019-06-04

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: 2018-11-13
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: 2019-01-02
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: 2018-11-13
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.

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: 2018-11-13
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: 2019-01-02
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: 2018-11-13
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: 2018-11-13
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: 2019-01-11
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: 2018-12-02
CmpDate: 2018-03-15

Kutschera U (2016)

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

Nature microbiology, 1(8):16114.

RevDate: 2018-11-13
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.

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: 2018-11-13
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.

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: 2020-10-01
CmpDate: 2016-04-30

Blackstone NW (2016)

An Evolutionary Framework for Understanding the Origin of Eukaryotes.

Biology, 5(2):.

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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
CmpDate: 2016-07-06

Koonin EV (2015)

Archaeal ancestors of eukaryotes: not so elusive any more.

BMC biology, 13:84.

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: 2018-11-13
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: 2019-01-30
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: 2019-01-30
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: 2019-01-30
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: 2019-01-30
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: 2018-11-13
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.

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: 2018-11-13
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: 2019-01-09
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.

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: 2018-11-13
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.

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: 2018-11-13
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.

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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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):.

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: 2018-11-13
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.

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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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: 2019-01-08
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: 2018-12-02
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: 2020-09-30
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: 2019-01-08
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.

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: 2018-11-13
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.

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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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: 2020-09-29
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.

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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
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: 2018-11-13
CmpDate: 2011-11-28

Lane N (2011)

Energetics and genetics across the prokaryote-eukaryote divide.

Biology direct, 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: 2018-11-13
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.


ESP Quick Facts

ESP Origins

In the early 1990's, Robert Robbins was a faculty member at Johns Hopkins, where he directed the informatics core of GDB — the human gene-mapping database of the international human genome project. To share papers with colleagues around the world, he set up a small paper-sharing section on his personal web page. This small project evolved into The Electronic Scholarly Publishing Project.

ESP Support

In 1995, Robbins became the VP/IT of the Fred Hutchinson Cancer Research Center in Seattle, WA. Soon after arriving in Seattle, Robbins secured funding, through the ELSI component of the US Human Genome Project, to create the original ESP.ORG web site, with the formal goal of providing free, world-wide access to the literature of classical genetics.

ESP Rationale

Although the methods of molecular biology can seem almost magical to the uninitiated, the original techniques of classical genetics are readily appreciated by one and all: cross individuals that differ in some inherited trait, collect all of the progeny, score their attributes, and propose mechanisms to explain the patterns of inheritance observed.

ESP Goal

In reading the early works of classical genetics, one is drawn, almost inexorably, into ever more complex models, until molecular explanations begin to seem both necessary and natural. At that point, the tools for understanding genome research are at hand. Assisting readers reach this point was the original goal of The Electronic Scholarly Publishing Project.

ESP Usage

Usage of the site grew rapidly and has remained high. Faculty began to use the site for their assigned readings. Other on-line publishers, ranging from The New York Times to Nature referenced ESP materials in their own publications. Nobel laureates (e.g., Joshua Lederberg) regularly used the site and even wrote to suggest changes and improvements.

ESP Content

When the site began, no journals were making their early content available in digital format. As a result, ESP was obliged to digitize classic literature before it could be made available. For many important papers — such as Mendel's original paper or the first genetic map — ESP had to produce entirely new typeset versions of the works, if they were to be available in a high-quality format.

ESP Help

Early support from the DOE component of the Human Genome Project was critically important for getting the ESP project on a firm foundation. Since that funding ended (nearly 20 years ago), the project has been operated as a purely volunteer effort. Anyone wishing to assist in these efforts should send an email to Robbins.

ESP Plans

With the development of methods for adding typeset side notes to PDF files, the ESP project now plans to add annotated versions of some classical papers to its holdings. We also plan to add new reference and pedagogical material. We have already started providing regularly updated, comprehensive bibliographies to the ESP.ORG site.

Electronic Scholarly Publishing
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Papers in Classical Genetics

The ESP began as an effort to share a handful of key papers from the early days of classical genetics. Now the collection has grown to include hundreds of papers, in full-text format.

Digital Books

Along with papers on classical genetics, ESP offers a collection of full-text digital books, including many works by Darwin (and even a collection of poetry — Chicago Poems by Carl Sandburg).


ESP now offers a much improved and expanded collection of timelines, designed to give the user choice over subject matter and dates.


Biographical information about many key scientists.

Selected Bibliographies

Bibliographies on several topics of potential interest to the ESP community are now being automatically maintained and generated on the ESP site.

ESP Picks from Around the Web (updated 07 JUL 2018 )