Open Questions on the Origin of Eukaryotes
Open accessAbstract
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.
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Eukaryotes likely originated from a symbiosis between an archaeal host and a bacterial endosymbiont.
“The latter view is based on the notion that Eukaryotes likely originated from a symbiosis between an archaeal host and a bacterial endosymbiont (e.g.reviewed in Lopez-Garcia and Moreira 2015: Martin et al. 2015), a scenario that has gained recent support from the discovery of the Asgard archaea, which form a monophyletic group with Eukaryotes in phylogenetic analyses and encode various eukaryotic”
From The Emergence of Life (2019) · cites this paper as Lopez-Garcia and Moreira 2015
The “Symbiogenetic models” section describes an increasingly popular hypothesis in which eukaryotes arose through symbiosis between an archaeal host and a bacterial endosymbiont. But the paper calls that direct-origin scenario plausible rather than likely; “Mitochondria: early or late?” says a different scenario, with mitochondrial incorporation later, seemed favored. The claim overstates how firmly the review endorses the proposed timing of the symbiosis. (LLM, conf=0.84)
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Cites
Complex archaea that bridge the gap between prokaryotes and eukaryotes
Spang, A., Saw, J. H., Jørgensen, S. L., Zaremba-Niedzwiedzka, K., Martijn, J., Lind, A. E., van Eijk, R., Schleper, C., Guy, L., & Ettema, T. J. G. (2015) · Nature · doi:10.1038/nature14447 · Cited by 1,324 · see citing works
The Hydrogen Hypothesis for the First Eukaryote
Martin, W., & Müller, M. (1998) · Nature · doi:10.1038/32096 · Cited by 1,282 · see citing works
Tracing the stepwise oxygenation of the Proterozoic ocean
Scott, C., Lyons, T. W., Bekker, A., Shen, Y., Poulton, S. W., Chu, X., & Anbar, A. D. (2008) · Nature · doi:10.1038/nature06811 · Cited by 1,098 · cited 1× · see citing works
“54 Ga) oceans [46] but also in contemporary oceanic (and freshwater) sediments, where Lokiarchaeaota and related archaeal lineages thrive [9].”
BackgroundEstimating the timing of early eukaryotic diversification with multigene molecular clocks
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H., & Katz, L. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110633108 · Cited by 899 · see citing works
Eukaryotic evolution, changes and challenges
Embley, T. M., & Martin, W. (2006) · Nature · doi:10.1038/nature04546 · Cited by 867 · see citing works
Gray, M. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a011403 · Cited by 639 · see citing works
Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era
Ueno, Y., Yamada, K., Yoshida, N., Maruyama, S., & Isozaki, Y. (2006) · Nature · doi:10.1038/nature04584 · Cited by 572 · see citing works
Did DNA replication evolve twice independently?
Leipe, D. D., Aravind, L., & Koonin, E. V. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.17.3389 · Cited by 351 · see citing works
The early evolution of lipid membranes and the three domains of life
Lombard, J., López-García, P., & Moreira, D. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2815 · Cited by 320 · see citing works
Self-citationThe origins of phagocytosis and eukaryogenesis
Yutin, N., Wolf, M. Y., Wolf, Y. I., & Koonin, E. V. (2009) · Biology Direct · doi:10.1186/1745-6150-4-9 · Cited by 247 · cited 1× · see citing works
“Before the discovery of the Lokiarchaeota, symbiogenetic models proposing a direct endosymbiosis of the mitochondrial ancestor within one archaeon had gained popularity [24,26,50] (Figure 2.”
BackgroundEvolution of diverse cell division and vesicle formation systems in Archaea
Makarova, K. S., Yutin, N., Bell, S. D., & Koonin, E. V. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2406 · Cited by 228 · see citing works
Geological constraints on the origin of oxygenic photosynthesis
Farquhar, J., Zerkle, A. L., & Bekker, A. (2011) · Photosynthesis Research · doi:10.1007/s11120-010-9594-0 · Cited by 223 · see citing works
Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry
Mentel, M., & Martin, W. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0031 · Cited by 92 · see citing works
Flagged first, then by citations
Research works printed but not linked: 69
- [1]Adl SM The revised classification of eukaryotes J Eukaryot Microbiol 2012 59 429 493 23020233 PMC3483872
- [3]Lane N Martin W The energetics of genome complexity Nature 2010 467 929 934 20962839
- [4]Timmis JN Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes Nat Rev Genet 2004 5 123 135 14735123
- [6]Poole AM Penny D Evaluating hypotheses for the origin of eukaryotes Bioessays 2007 29 74 84 17187354
- [7]Keeling PJ The impact of history on our perception of evolutionary events: endosymbiosis and the origin of eukaryotic complexity Cold Spring Harb Perspect Biol 2014 6 a016196 24492708 PMC3941238
- [8]McInerney JO The hybrid nature of the Eukaryota and a consilient view of life on Earth Nat Rev Microbiol 2014 12 449 455 24814066
- [10]Embley TM Williams TA Evolution: Steps on the road to eukaryotes Nature 2015 25945740
- [11]Sogin ML Early evolution and the origin of eukaryotes Curr. Opin. Genet. Dev 1991 1 457 463 1822277
- [12]Poole A Early evolution: prokaryotes, the new kids on the block Bioessays 1999 21 880 889 10497339
- [13]Doolittle WF Brown JR Tempo, mode, the progenote, and the universal root Proc. Natl. Acad. Sci. USA 1994 91 6721 6728 8041689 PMC44275
- [14]Cavalier-Smith T The neomuran revolution and phagotrophic origin of eukaryotes and cilia in the light of intracellular coevolution and a revised tree of life Cold Spring Harb Perspect Biol 2014 6 a016006 25183828 PMC4142966
- [15]Fuerst JA Sagulenko E Keys to eukaryality: planctomycetes and ancestral evolution of cellular complexity Front Microbiol 2012 3 167 22586422 PMC3343278
- [16]Diekmann Y Pereira-Leal JB Evolution of intracellular compartmentalization Biochem J 2013 449 319 331 23240612
- [17]Cavalier-Smith T The origin of nuclei and of eukaryotic cells Nature 1975 256 463 468 808732
- [18]McInerney JO Planctomycetes and eukaryotes: a case of analogy not homology Bioessays 2011 33 810 817 21858844 PMC3795523
- [19]von Dohlen CD Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts Nature 2001 412 433 436 11473316
- [20]Godde JS Breaking through a phylogenetic impasse: a pair of associated archaea might have played host in the endosymbiotic origin of eukaryotes Cell Biosci 2012 2 29 22913376 PMC3490757
- [22]Margulis L Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life Proc Natl Acad Sci U S A 1996 93 1071 1076 8577716 PMC40032
- [23]Searcy DG Hartman H Matsuno K Origins of mitochondria and chloroplasts from sulfur-based symbioses The origin and evolution of the cell 1992 47 78 World Scientific
- [25]Guy L Ettema TJ The archaeal ‘TACK’ superphylum and the origin of eukaryotes Trends Microbiol 2011 19 580 587 22018741
- [26]Martijn J Ettema TJ From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell Biochem Soc Trans 2013 41 451 457 23356327
- [28]Gupta RS Golding GB The origin of the eukaryotic cell Trends Biochem Sci 1996 21 166 171 8871398
- [29]Horiike T Origin of eukaryotic cell nuclei by symbiosis of Archaea in Bacteria is revealed by homology-hit analysis Nat Cell Biol 2001 3 210 214 11175755
- [30]Moreira D López-García P Symbiosis between methanogenic archaea and delta-Proteobacteria as the origin of eukaryotes: The syntrophic hypothesis J. Mol. Evol 1998 47 517 530 9797402
- [31]López-García P Moreira D Selective forces for the origin of the eukaryotic nucleus Bioessays 2006 28 525 533 16615090
- [32]Gribaldo S The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat Rev Microbiol 2010 8 743 752 20844558
- [33]Rochette NC Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes Mol Biol Evol 2014 31 832 845 24398320 PMC3969559
- [34]Williams TA Embley TM Archaeal “dark matter” and the origin of eukaryotes Genome Biol Evol 2014 6 474 481 24532674 PMC3971582
- [35]Williams TA An archaeal origin of eukaryotes supports only two primary domains of life Nature 2013 504 231 236 24336283
- [36]Petitjean C Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom proteoarchaeota Genome Biol Evol 2014 7 191 204 25527841 PMC4316627
- [37]Biddle JF Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru Proc Natl Acad Sci U S A 2006 103 3846 3451 16505362 PMC1533785
- [38]Jorgensen SL Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge Proc Natl Acad Sci U S A 2012 109 E2846 2855 23027979 PMC3479504
- [39]Jorgensen SL Quantitative and phylogenetic study of the Deep Sea Archaeal Group in sediments of the Arctic mid-ocean spreading ridge Front Microbiol 2013 4 299 24109477 PMC3790079
- [40]Rodriguez-Ezpeleta N Embley TM The SAR11 group of Alpha-Proteobacteria is not related to the origin of mitochondria PLoS ONE 2012 7 e30520 22291975 PMC3264578
- [41]López-García P Bacterial gene import and mesophilic adaptation in archaea Nat Rev Microbiol 2015 13 447 456 26075362 PMC4601535
- [42]Schluter A Phylogenomic evidence for a myxococcal contribution to the mitochondrial fatty acid beta-oxidation PLoS ONE 2011 6 e21989 21760940 PMC3131387
- [43]Orphan VJ Methods for unveiling cryptic microbial partnerships in nature Curr Opin Microbiol 2009 12 231 237 19447672
- [44]Kouzuma A Microbial interspecies interactions: recent findings in syntrophic consortia Front Microbiol 2015 6 477 26029201 PMC4429618
- [45]Kurland CG Andersson SG Origin and evolution of the mitochondrial proteome Microbiol Mol Biol Rev 2000 64 786 820 11104819 PMC99014
- [47]Hug LA Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes Mol Biol Evol 2010 27 311 324 19805439
- [48]López-García P Moreira D Metabolic symbiosis at the origin of eukaryotes Trends Biochem Sci 1999 24 88 93 10203753
- [49]Raymann K The two-domain tree of life is linked to a new root for the Archaea Proc Natl Acad Sci U S A 2015 112 6670 6675 25964353 PMC4450401
- [51]Thiergart T An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin Genome Biol Evol 2012 4 466 485 22355196 PMC3342870
- [52]Koumandou VL Molecular paleontology and complexity in the last eukaryotic common ancestor Crit Rev Biochem Mol Biol 2013 48 373 396 23895660 PMC3791482
- [53]Cavalier-Smith T Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution Biol Direct 2010 5 7 20132544 PMC2837639
- [54]Jekely G Origin of eukaryotic endomembranes: a critical evaluation of different model scenarios Adv Exp Med Biol 2007 607 38 51 17977457
- [55]Martin W Koonin EV Introns and the origin of nucleus-cytosol compartmentalization Nature 2006 440 41 45 16511485
- [56]Dubilier N Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm Nature 2001 411 298 302 11357130
- [58]Pogozheva ID Structural adaptations of proteins to different biological membranes Biochim Biophys Acta 2013 1828 2592 2608 23811361 PMC3787962
- [59]Koga Y Morii H Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations Microbiol Mol Biol Rev 2007 71 97 120 17347520 PMC1847378
- [60]Lincoln SA Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean Proc Natl Acad Sci U S A 2014 111 9858 9863 24946804 PMC4103328
- [61]Martin W Koonin EV A positive definition of prokaryotes Nature 2006 442 868 16929275
- [62]Woese CR Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya Proc. Natl. Acad. Sci. USA 1990 87 4576 4579 2112744 PMC54159
- [63]Woese CR Fox GE Phylogenetic structure of the prokaryotic domain: the primary kingdoms Proc. Natl. Acad. Sci. USA 1977 74 5088 5090 270744 PMC432104
- [64]López-García P Moreira D Tracking microbial biodiversity through molecular and genomic ecology Res Microbiol 2008 159 67 73 18207371
- [65]Mirkin BG Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes BMC Evol Biol 2003 3 2 12515582 PMC149225
- [67]Rivera MC Genomic evidence for two functionally distinct gene classes Proc. Natl. Acad. Sci. USA 1998 95 6239 6244 9600949 PMC27643
- [68]Ribeiro S Golding GB The mosaic nature of the eukaryotic nucleus Mol Biol Evol 1998 15 779 788 9656480
- [69]Knoll AH Paleobiological perspectives on early eukaryotic evolution Cold Spring Harbor Perspectives in Biology 2014 6 PMC3941219 24384569
- [71]Eme L On the age of eukaryotes: evaluating evidence from fossils and molecular clocks Cold Spring Harb Perspect Biol 2014 6 a016139 25085908 PMC4107988
- [73]Shen Y Isotopic evidence for microbial sulphate reduction in the early Archaean era Nature 2001 410 77 81 11242044
- [74]Stueken EE Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr Nature 2015 520 666 669 25686600
- [76]Allwood AC Stromatolite reef from the Early Archaean era of Australia Nature 2006 441 714 718 16760969
- [77]Hjort K Diversity and reductive evolution of mitochondria among microbial eukaryotes Philos Trans R Soc Lond B Biol Sci 2010 365 713 727 20124340 PMC2817227
- [79]Koonin EV Preview. The incredible expanding ancestor of eukaryotes Cell 2010 140 606 608 20211127 PMC3293451
- [80]Sagan L On the origin of mitosing cells J Theor Biol 1967 14 255 274 11541392
- [81]Schwartz RM Dayhoff MO Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts Science 1978 199 395 403 202030
- [82]Dyall SD Ancient invasions: from endosymbionts to organelles Science 2004 304 253 257 15073369
- [83]McCutcheon JP Moran NA Extreme genome reduction in symbiotic bacteria Nat Rev Microbiol 2012 10 13 26 22064560
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- Authors
- López-García, P., & Moreira, D.
- Affiliations
- Université Paris-Sud (FR)
- ORCID
- Moreira, David
- Venue
- Trends in Ecology & Evolution
- Publisher
- Elsevier BV
- Published
- 2015-11
- Volume
- 30
- Issue
- 11
- Pages
- 697-708
- ISSN
- 0169-5347 (ISSN-L)
- PMC
- PMC4640172
- OpenAlex
- W1908213546
- Cited by
- 135
- References
- 13
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 5 · 2023: 15 · 2022: 10 · 2021: 15 · 2020: 13 · 2019: 20 · 2018: 14 · 2017: 18 · 2016: 13 · 2015: 1 · 2014: 2
- FWCI
- 1.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Trends in Ecology & Evolution (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- eukaryotic origin, endosymbiosis, mitochondrial origin, last eukaryotic common ancestor, phylogenomics
- MeSH terms
- Archaea, Eukaryotic Cells, Biological Evolution, Mitochondria, Phylogeny, Symbiosis, Eukaryota
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