The Archaea was recognized as a third domain of life 40 years ago. Molecular evidence soon suggested that the Eukarya represented a sister group to the Archaea or that eukaryotes descended from archaea.
Culture-independent genomics has revealed the vast diversity existing among the Archaea, including the recently described Asgard superphylum. Phylogenomic analyses have placed the Asgard archaea as the closest prokaryotic relatives of eukaryotes.
Comparative genomic analyses have reconstructed a complex last eukaryotic common ancestor. However, how and in which order these complex eukaryotic features evolved in an Asgard archaea-related ancestor remains largely unclear.
Genomic investigation of Asgard archaea showed that they carry several genes formerly believed to be eukaryotic specific, illuminating early events during eukaryogenesis.
Fully understanding the process of eukaryogenesis requires finding answers to several challenging and intertwined questions. Although we have seemingly answered some of these questions, others remain fiercely debated, and new questions continue to arise.
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.
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Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977). This paper represents one of the most important studies in microbiology of the past century, providing the first evidence that cellular life was composed of three distinct types of organisms — later called Archaea, Bacteria and Eukarya.
Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).
Iwabe, N., Kuma, K., Hasegawa, M., Osawa, S. & Miyata, T. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl Acad. Sci. USA 86, 9355–9359 (1989).
Huet, J., Schnabel, R., Sentenac, A. & Zillig, W. Archaebacteria and eukaryotes possess DNA-dependent RNA polymerases of a common type. EMBO J. 2, 1291–1294 (1983).
Zillig, W. et al. The phylogenetic relations of DNA-dependent RNA polymerases of archaebacteria, eukaryotes, and eubacteria. Can. J. Microbiol. 35, 73–80 (1989).
Lake, J. A., Henderson, E., Oakes, M. & Clark, M. W. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc. Natl Acad. Sci. USA 81, 3786–3790 (1984). This study, based on analyses of ribosome structures, proposes that eukaryotes might have evolved from within the archaeal domain of life.
Rivera, M. C. & Lake, J. A. Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257, 74–76 (1992).
Brown, J. R. & Doolittle, W. F. Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456–502 (1997).
Gribaldo, S., Poole, A. M., Daubin, V., Forterre, P. & Brochier-Armanet, C. The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat. Rev. Microbiol. 8, 743–752 (2010).
Lake, J. A. Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature 331, 184–186 (1988).
Tourasse, N. J. & Gouy, M. Accounting for evolutionary rate variation among sequence sites consistently changes universal phylogenies deduced from rRNA and protein-coding genes. Mol. Phylogenet. Evol. 13, 159–168 (1999).
Baldauf, S. L., Palmer, J. D. & Doolittle, W. F. The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. Proc. Natl Acad. Sci. USA 93, 7749–7754 (1996).
Gouy, M. & Li, W. H. Phylogenetic analysis based on rRNA sequences supports the archaebacterial rather than the eocyte tree. Nature 339, 145–147 (1989).
Cammarano, P., Creti, R., Sanangelantoni, A. M. & Palm, P. The archaea monophyly issue: a phylogeny of translational elongation factor G(2) sequences inferred from an optimized selection of alignment positions. J. Mol. Evol. 49, 524–537 (1999).
Barns, S. M., Fundyga, R. E., Jeffries, M. W. & Pace, N. R. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc. Natl Acad. Sci. USA 91, 1609–1613 (1994).
Barns, S. M., Delwiche, C. F., Palmer, J. D. & Pace, N. R. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc. Natl Acad. Sci. USA 93, 9188–9193 (1996).
Elkins, J. G. et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl Acad. Sci. USA 105, 8102–8107 (2008).
Reigstad, L. J., Jorgensen, S. L. & Schleper, C. Diversity and abundance of Korarchaeota in terrestrial hot springs of Iceland and Kamchatka. ISME J. 4, 346–356 (2010).
Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005).
Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245–252 (2008). This paper proposes the existence of the first archaeal phylum outside of the Crenarchaeota and Euryarchaeota, namely, the Thaumarchaeota.
Walker, C. B. et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl Acad. Sci. USA 107, 8818–8823 (2010).
Spang, A. et al. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331–340 (2010).
Eme, L. et al. Metagenomics of Kamchatkan hot spring filaments reveal two new major (hyper)thermophilic lineages related to Thaumarchaeota. Res. Microbiol. 164, 425–438 (2013).
Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204–3223 (2011). This study represents the first genome reconstructed purely from metagenomic data and uncovered the existence of homologues of the eukaryotic ubiquitin system in archaea.
Guy, L. & Ettema, T. J. G. The archaeal “TACK” superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580–587 (2011). This opinion piece is the first extensive review of the evidence for a scenario in which the archaeal parent of eukaryotes emerged from within the TACK superphylum.
Guy, L., Saw, J. H. & Ettema, T. J. G. The archaeal legacy of eukaryotes: a phylogenomic perspective. Cold Spring Harb. Perspect. Biol. 6, a016022 (2014).
Petitjean, C., Deschamps, P., López-García, P. & Moreira, D. Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol. Evol. 7, 191–204 (2014).
Kelly, S., Wickstead, B. & Gull, K. Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc. Biol. Sci. 278, 1009–1018 (2011).
Williams, T. A., Foster, P. G., Cox, C. J. & Embley, T. M. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236 (2013).
Lasek-Nesselquist, E. & Gogarten, J. P. The effects of model choice and mitigating bias on the ribosomal tree of life. Mol. Phylogenet. Evol. 69, 17–38 (2013).
Williams, T. A. & Embley, T. M. Archaeal “dark matter” and the origin of eukaryotes. Genome Biol. Evol. 6, 474–481 (2014).
Raymann, K., Brochier-Armanet, C. & Gribaldo, S. The two-domain tree of life is linked to a new root for the Archaea. Proc. Natl Acad. Sci. USA 112, 6670–6675 (2015). This paper proposes an innovative strategy to increase the number of phylogenetic markers usable to investigate the tree of life and suggests a new position for the root of the tree of the Archaea.
Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R. & Embley, T. M. The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 20356–20361 (2008). This study reports the first convincing evidence for a two-domains tree of life by use of phylogenomic approaches that employed advanced evolutionary models.
Foster, P. G., Cox, C. J. & Embley, T. M. The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods. Philos. Trans. R. Soc. B Biol. Sci. 364, 2197–2207 (2009).
Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).
He, Y. et al. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat. Microbiol. 1, 16035 (2016).
Lazar, C. S. et al. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ. Microbiol. 18, 1200–1211 (2016).
Kozubal, M. A. et al. Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park. ISME J. 7, 622–634 (2013).
Guy, L., Spang, A., Saw, J. H. & Ettema, T. J. G. “Geoarchaeote NAG1” is a deeply rooting lineage of the archaeal order Thermoproteales rather than a new phylum. ISME J. 8, 1353–1357 (2014).
Vanwonterghem, I. et al. Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat. Microbiol. 1, 16170 (2016).
Baker, B. J. et al. Enigmatic, ultrasmall, uncultivated Archaea. Proc. Natl Acad. Sci. USA 107, 8806–8811 (2010).
Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).
Castelle, C. J. et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701 (2015).
Eme, L. & Doolittle, W. F. Microbial diversity: a bonanza of phyla. Curr. Biol. 25, R227–R230 (2015).
Spang, A., Caceres, E. F. & Ettema, T. J. G. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357, eaaf3883 (2017).
Adam, P. S., Borrel, G., Brochier-Armanet, C. & Gribaldo, S. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J. http://dx.doi.org/10.1038/ismej.2017.122 (2017).
Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015). This paper describes the discovery of Lokiarchaeota and provides evidence that they form a monophyletic group with eukaryotes and that their genomes encode an expanded repertoire of ESPs.
Pedersen, R. B. et al. Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge. Nat. Commun. 1, 126 (2010).
Hartman, H. & Fedorov, A. The origin of the eukaryotic cell: a genomic investigation. Proc. Natl Acad. Sci. USA 99, 1420–1425 (2002).
Da Cunha, V., Gaia, M., Gadelle, D., Nasir, A. & Forterre, P. Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet. 13, e1006810 (2017).
Spang, S. et al. Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genet. (in the press) (2017).
Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017). This work describes the Asgard superphylum and expands on the known repertoire of ESPs in archaea.
Knoll, A. H., Bambach, R. K., Canfield, D. E. & Grotzinger, J. P. Comparative Earth history and Late Permian mass extinction. Science 273, 452–457 (1996).
Eme, L., Sharpe, S. C., Brown, M. W. & Roger, A. J. On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb. Perspect. Biol. 6, a016139 (2014).
Koumandou, V. L. et al. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit. Rev. Biochem. Mol. Biol. 48, 373–396 (2013). This publication represents a comprehensive review of the inferred features of LECA.
Koonin, E. V. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11, 209 (2010).
Koreny, L. & Field, M. C. Ancient eukaryotic origin and evolutionary plasticity of nuclear lamina. Genome Biol. Evol. 8, 2663–2671 (2016).
Makarova, K. S., Wolf, Y. I., Mekhedov, S. L., Mirkin, B. G. & Koonin, E. V. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res. 33, 4626–4638 (2005).
Koonin, E. V. Preview. The incredible expanding ancestor of eukaryotes. Cell 140, 606–608 (2010).
Martin, W. & Koonin, E. V. Introns and the origin of nucleus-cytosol compartmentalization. Nature 440, 41–45 (2006).
Shabalina, S. A. & Koonin, E. V. Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 23, 578–587 (2008).
Collins, L. & Penny, D. Complex spliceosomal organization ancestral to extant eukaryotes. Mol. Biol. Evol. 22, 1053–1066 (2005).
Grau-Bové, X., Sebé-Pedrós, A. & Ruiz-Trillo, I. The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin. Mol. Biol. Evol. 32, 726–739 (2015).
Field, M. C. & Dacks, J. B. First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr. Opin. Cell Biol. 21, 4–13 (2009).
Schlacht, A., Herman, E. K., Klute, M. J., Field, M. C. & Dacks, J. B. Missing pieces of an ancient puzzle: evolution of the eukaryotic membrane-trafficking system. Cold Spring Harb. Perspect. Biol. 6, a016048 (2014).
Eme, L., Moreira, D., Talla, E. & Brochier-Armanet, C. A complex cell division machinery was present in the last common ancestor of eukaryotes. PLoS ONE 4, e5021 (2009).
Eme, L., Trilles, A., Moreira, D. & Brochier-Armanet, C. The phylogenomic analysis of the anaphase promoting complex and its targets points to complex and modern-like control of the cell cycle in the last common ancestor of eukaryotes. BMC Evol. Biol. 11, 265 (2011).
Speijer, D., Lukeš, J. & Eliáš, M. Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc. Natl Acad. Sci. USA 112, 8827–8834 (2015).
Lykidis, A. Comparative genomics and evolution of eukaryotic phospholipid biosynthesis. Prog. Lipid Res. 46, 171–199 (2007).
Desmond, E. & Gribaldo, S. Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature. Genome Biol. Evol. 1, 364–381 (2009).
Hannich, J. T., Umebayashi, K. & Riezman, H. Distribution and functions of sterols and sphingolipids. Cold Spring Harb. Perspect. Biol. 3, a004762 (2011).
Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).
Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J. & Woese, C. R. Mitochondrial origins. Proc. Natl Acad. Sci. USA 82, 4443–4447 (1985).
Gray, M. W. Organelle origins and ribosomal RNA. Biochem. Cell Biol. 66, 325–348 (1988).
Gray, M. W. Mitochondrial evolution. Cold Spring Harb. Perspect. Biol. 4, a011403 (2012).
Stairs, C. W., Leger, M. M. & Roger, A. J. Diversity and origins of anaerobic metabolism in mitochondria and related organelles. Philos. Trans. R. Soc. B Biol. Sci. 370, 20140326 (2015).
Müller, M. et al. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444–495 (2012).
Doolittle, W. F. How natural a kind is “eukaryote?”. Cold Spring Harb. Perspect. Biol. 6, a015974 (2014).
Boyd, R. Realism, anti-foundationalism and the enthusiasm for natural kinds. Philos. Stud. 61, 127–148 (1991).
Andersson, J. O. Gene transfer and diversification of microbial eukaryotes. Annu. Rev. Microbiol. 63, 177–193 (2009).
Soanes, D. & Richards, T. A. Horizontal gene transfer in eukaryotic plant pathogens. Annu. Rev. Phytopathol. 52, 583–614 (2014).
Eme, L., Gentekaki, E., Curtis, B., Archibald, J. M. & Roger, A. J. Lateral gene transfer in the adaptation of the anaerobic parasite blastocystis to the gut. Curr. Biol. 27, 807–820 (2017).
Alsmark, C. et al. Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol. 14, R19 (2013).
Jain, R., Rivera, M. C. & Lake, J. A. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl Acad. Sci. USA 96, 3801–3806 (1999).
Sibbald, S. J. & Archibald, J. M. More protist genomes needed. Nat. Ecol. Evol. 1, 145 (2017).
Bapteste, E. & Gribaldo, S. The genome reduction hypothesis and the phylogeny of eukaryotes. Trends Genet. 19, 696–700 (2003).
Thiergart, T., Landan, G., Schenk, M., Dagan, T. & Martin, W. F. An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol. Evol. 4, 466–485 (2012).
Rochette, N. C., Brochier-Armanet, C. & Gouy, M. Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes. Mol. Biol. Evol. 31, 832–845 (2014). This paper proposes a thorough systematic analysis of the phylogenetic relationships between ancestral eukaryotic genes and archaeal and bacterial genes.
Ku, C. et al. Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524, 427–432 (2015).
Pittis, A. A. & Gabaldón, T. Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 531, 101–104 (2016). This paper represents the first formal testing of the timing of acquisition of the mitochondrion by use of comparisons of phylogenetic distances between eukaryotic proteins and their closest prokaryotic relatives.
Yutin, N., Makarova, K. S., Mekhedov, S. L., Wolf, Y. I. & Koonin, E. V. The deep archaeal roots of eukaryotes. Mol. Biol. Evol. 25, 1619–1630 (2008).
Esser, C. et al. A genome phylogeny for mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 1643–1660 (2004).
Davidov, Y., Huchon, D., Koval, S. F. & Jurkevitch, E. A new α-proteobacterial clade of Bdellovibrio-like predators: implications for the mitochondrial endosymbiotic theory. Environ. Microbiol. 8, 2179–2188 (2006).
Fitzpatrick, D. A., Creevey, C. J. & McInerney, J. O. Genome phylogenies indicate a meaningful α-proteobacterial phylogeny and support a grouping of the mitochondria with the Rickettsiales. Mol. Biol. Evol. 23, 74–85 (2006).
Williams, K. P., Sobral, B. W. & Dickerman, A. W. A robust species tree for the alphaproteobacteria. J. Bacteriol. 189, 4578–4586 (2007).
Wu, M. et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2, E69 (2004).
Georgiades, K., Madoui, M.-A., Le, P., Robert, C. & Raoult, D. Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas americana mitochondrion. PLoS ONE 6, e24857 (2011).
Rodríguez-Ezpeleta, N. & Embley, T. M. The SAR11 group of alpha-proteobacteria is not related to the origin of mitochondria. PLoS ONE 7, e30520 (2012).
Thrash, J. C. et al. Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Sci. Rep. 1, 13 (2011).
Brindefalk, B., Ettema, T. J. G., Viklund, J., Thollesson, M. & Andersson, S. G. E. A phylometagenomic exploration of oceanic alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLoS ONE 6, e24457 (2011).
Wang, Z. & Wu, M. An integrated phylogenomic approach toward pinpointing the origin of mitochondria. Sci. Rep. 5, 7949 (2015).
Poole, A. M. & Penny, D. Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 74–84 (2007).
Keeling, P. J. The impact of history on our perception of evolutionary events: endosymbiosis and the origin of eukaryotic complexity. Cold Spring Harb. Perspect. Biol. 6, a016196 (2014).
McInerney, J. O., O'Connell, M. J. & Pisani, D. The hybrid nature of the Eukaryota and a consilient view of life on Earth. Nat. Rev. Microbiol. 12, 449–455 (2014).
Moreira, D. & Lopez-Garcia, P. Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47, 517–530 (1998). This publication details the syntrophy hypothesis, which proposes a detailed mechanism suggesting that eukaryotes evolved from a two-step symbiosis.
López-García, P. & Moreira, D. Open questions on the origin of eukaryotes. Trends Ecol. Evol. 30, 697–708 (2015). Among other topics, this review discusses the necessity to determine the mechanistic and selective forces explaining the origin of key eukaryotic features, such as the nucleus or the bacterial-like eukaryotic membrane system.
Dacks, J. B. et al. The changing view of eukaryogenesis — fossils, cells, lineages and how they all come together. J. Cell Sci. 129, 3695–3703 (2016).
Cavalier-Smith, T. Molecular phylogeny. Archaebacteria and Archezoa. Nature 339, 100–101 (1989).
Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998). This study proposes one of the first and most elaborate models of a symbiogenetic origin of eukaryotes.
Searcy, D. G. in The Origin and Evolution of the Cell (eds Hartmann, H. et al.) 47–78 (World Scientific, 1992).
Karnkowska, A. et al. A eukaryote without a mitochondrial organelle. Curr. Biol. 26, 1274–1284 (2016).
Martin, W. F. et al. Late mitochondrial origin is an artefact. Genome Biol. Evol. 9, 373–379 (2017).
Pittis, A. A. & Gabaldon, T. On phylogenetic branch lengths distribution and the late acquistion of mitochondria. Preprint at https://www.biorxiv.org/content/early/2016/07/20/064873.article-info (2016).
Ettema, T. J. G. Evolution: mitochondria in the second act. Nature 531, 39–40 (2016).
Wolf, Y. I., Makarova, K. S., Yutin, N. & Koonin, E. V. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol. Direct 7, 46 (2012).
Koonin, E. V. & Yutin, N. The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb. Perspect. Biol. 6, a016188 (2014).
Koonin, E. V., Makarova, K. S. & Elkins, J. G. Orthologs of the small RPB8 subunit of the eukaryotic RNA polymerases are conserved in hyperthermophilic Crenarchaeota and “Korarchaeota”. Biol. Direct 2, 38 (2007).
Zwickl, P. et al. Primary structure of the Thermoplasma proteasome and its implications for the structure, function, and evolution of the multicatalytic proteinase. Biochemistry 31, 964–972 (1992).
James, R. H. et al. Functional reconstruction of a eukaryotic-likeE1/E2/(RING) E3 ubiquitylation cascade from an uncultured archaeon. Nat Commun. (in the press).
Makarova, K. S. & Koonin, E. V. Archaeal ubiquitin-like proteins: functional versatility and putative ancestral involvement in tRNA modification revealed by comparative genomic analysis. Archaea 2010, 710303 (2010).
Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445–452 (2009).
Jékely, G. Origin and evolution of the self-organizing cytoskeleton in the network of eukaryotic organelles. Cold Spring Harb. Perspect. Biol. 6, a016030 (2014).
Ettema, T. J. G., Lindås, A.-C. & Bernander, R. An actin-based cytoskeleton in archaea. Mol. Microbiol. 80, 1052–1061 (2011).
Lindås, A. C., Chruszcz, M., Bernander, R. & Valegård, K. Structure of crenactin, an archaeal actin homologue active at 90 °C. Acta Crystallogr. D Biol. Crystallogr. 70, 492–500 (2014).
Izoré, T., Duman, R., Kureisaite-Ciziene, D. & Löwe, J. Crenactin from Pyrobaculum calidifontis is closely related to actin in structure and forms steep helical filaments. FEBS Lett. 588, 776–782 (2014).
Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009).
Yutin, N. & Koonin, E. V. Archaeal origin of tubulin. Biol. Direct 7, 10 (2012).
Makarova, K. S., Yutin, N., Bell, S. D. & Koonin, E. V. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8, 731–741 (2010).
Lindås, A.-C., Karlsson, E. A., Lindgren, M. T., Ettema, T. J. G. & Bernander, R. A unique cell division machinery in the Archaea. Proc. Natl Acad. Sci. USA 105, 18942–18946 (2008).
Samson, R. Y., Obita, T., Freund, S. M., Williams, R. L. & Bell, S. D. A role for the ESCRT system in cell division in archaea. Science 322, 1710–1713 (2008).
Pelve, E. A. et al. Cdv-based cell division and cell cycle organization in the thaumarchaeon Nitrosopumilus maritimus. Mol. Microbiol. 82, 555–566 (2011).
Saw, J. H. et al. Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140328 (2015).
Klinger, C. M., Spang, A., Dacks, J. B. & Ettema, T. J. G. Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol. Biol. Evol. 33, 1528–1541 (2016).
Brandizzi, F. & Barlowe, C. Organization of the ER-Golgi interface for membrane traffic control. Nat. Rev. Mol. Cell Biol. 14, 382–392 (2013).
Rout, M. P. & Field, M. C. The evolution of organellar coat complexes and organization of the eukaryotic cell. Annu. Rev. Biochem. 86, 637–657 (2017). This is an extensive review on the origin and early evolution of the eukaryotic endomembrane system.
Sousa, F. L., Neukirchen, S., Allen, J. F., Lane, N. & Martin, W. F. Lokiarchaeon is hydrogen dependent. Nat. Microbiol. 1, 16034 (2016).
Seitz, K. W., Lazar, C. S., Hinrichs, K.-U., Teske, A. P. & Baker, B. J. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J. 10, 1696–1705 (2016).
Mariotti, M. et al. Lokiarchaeota marks the transition between the archaeal and eukaryotic selenocysteine encoding systems. Mol. Biol. Evol. 33, 2441–2453 (2016).
Philippe, H. et al. Pitfalls in supermatrix phylogenomics. Eur. J. Taxon. 283, 1–25 (2017).
Lartillot, N. & Philippe, H. A. Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 1095–1109 (2004).
Foster, P. G. Modeling compositional heterogeneity. Syst. Biol. 53, 485–495 (2004).
Williams, T. A. et al. Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proc. Natl Acad. Sci. USA 114, E4602–E4611 (2017). This work investigates archaeal gene family evolution to find the root of the archaeal tree and to infer the metabolism of the archaeal ancestors.
Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).
Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208–211 (2015).
Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).
Woese, C. R., Magrum, L. J. & Fox, G. E. Archaebacteria. J. Mol. Evol. 11, 245–251 (1978).
Lombard, J., López-García, P. & Moreira, D. The early evolution of lipid membranes and the three domains of life. Nat. Rev. Microbiol. 10, 507–515 (2012).
Baum, D. A. & Baum, B. An inside-out origin for the eukaryotic cell. BMC Biol. 12, 76 (2014).
Gould, S. B., Garg, S. G. & Martin, W. F. Bacterial vesicle secretion and the evolutionary origin of the eukaryotic endomembrane system. Trends Microbiol. 24, 525–534 (2016).
Villanueva, L., Schouten, S. & Damsté, J. S. Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the 'lipid divide'. Environ. Microbiol. 19, 54–69 (2017).
Villanueva, L., Damsté, J. S. & Schouten, S. A re-evaluation of the archaeal membrane lipid biosynthetic pathway. Nat. Rev. Microbiol. 12, 438–448 (2014).
Lombard, J., López-García, P. & Moreira, D. An ACP-independent fatty acid synthesis pathway in archaea: implications for the origin of phospholipids. Mol. Biol. Evol. 29, 3261–3265 (2012).
Dibrova, D. V., Galperin, M. Y. & Mulkidjanian, A. Y. Phylogenomic reconstruction of archaeal fatty acid metabolism. Environ. Microbiol. 16, 907–918 (2014).
Yokobori, S.-I., Nakajima, Y., Akanuma, S. & Yamagishi, A. Birth of archaeal cells: molecular phylogenetic analyses of G1P dehydrogenase, G3P dehydrogenases, and glycerol kinase suggest derived features of archaeal membranes having G1P polar lipids. Archaea 2016, 1802675 (2016).
Brochier-Armanet, C., Forterre, P. & Gribaldo, S. Phylogeny and evolution of the Archaea: one hundred genomes later. Curr. Opin. Microbiol. 14, 274–281 (2011).
Narasingarao, P. et al. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 6, 81–93 (2012).
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).
The authors wish to thank A. Roger and W. F. Doolittle for fruitful discussions. L.E. is funded by the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 704263. J.L. is supported by a postdoctoral fellowship for foreign researchers from the Wenner-Gren Foundations in Stockholm (UPD2016-0072). C.W.S. is supported by a European Molecular Biology Organization long-term fellowship (ALTF-997-2015) and the Natural Sciences and Engineering Research Council of Canada postdoctoral research fellowship (PDF-487174-2016). This work is supported by grants of the European Research Council (ERC Starting Grant 310039-PUZZLE_CELL), the Swedish Foundation for Strategic Research (SSF-FFL5) and the Swedish Research Council (VR grant 2015–04959), awarded to T.J.G.E.
The authors declare no competing financial interests.
- Sister groups
Two descendants that split from the same node; the descendants are each other's closest relative.
- Monophyletic groups
A monophyletic group is a group of organisms that forms a clade, which consists of all the descendants of a common ancestor.
The whole sequence of evolutionary events occurring between the first eukaryotic common ancestor (FECA) and the last eukaryotic common ancestor (LECA) explaining the process by which eukaryotic cells evolved from prokaryotic ancestors.
The sequencing of genetic material extracted directly from environmental samples.
- Genome-resolved metagenomics
The assembly of complete or draft genomes exclusively from metagenomic sequencing data.
A proposed archaeal superphylum comprising Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanohaloarchaeota and Nanoarchaeota. More recently, it was suggested that additional candidate phyla such as Woesearchaeota, Pacearchaeota, Micrarchaeota and possibly Altiarchaeales are part of this group.
- Hydrothermal vents
Areas of the sea floor from which geothermally heated water issues.
- Eukaryotic signature proteins
(ESPs). Proteins involved in key eukaryotic processes and conserved across most eukaryotic diversity.
- First eukaryotic common ancestor
(FECA). The most ancient organism whose only living descendants are present-day eukaryotes.
- Last eukaryotic common ancestor
(LECA). The most recent ancestor of all present-day eukaryotes.
Repetitive nucleotide sequences located at the ends of the linear chromosomes of most eukaryotic organisms.
- Spliceosomal introns
Introns in the nuclear protein-coding genes of eukaryotes that are removed by spliceosomes.
A large protein complex responsible for regulated degradation of proteins as part of the ubiquitin system found in all eukaryotes.
- Horizontal gene transfer
(HGT). Exchange of genetic material between cells and/or organisms; sometimes called lateral gene transfer. This contrasts with the vertical inheritance of DNA from parent to offspring.
- Genomic streamlining
A form of genome evolution that occurs through size reduction and simplification in terms of gene content; particularly common among parasitic organisms.
- Phylogenetic signal
Information contained in homologous molecular sequences used to reconstruct the historical relationships between the sequences.
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Eme, L., Spang, A., Lombard, J. et al. Archaea and the origin of eukaryotes. Nat Rev Microbiol 15, 711–723 (2017). https://doi.org/10.1038/nrmicro.2017.133
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