Abstract
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.
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References
Adl, S. M. et al. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59, 429–493 (2012).
Lopez-Garcia, P. & Moreira, D. Open questions on the origin of eukaryotes. Trends Ecol. Evol. 30, 697–708 (2015).
Lopez-Garcia, P., Eme, L. & Moreira, D. Symbiosis in eukaryotic evolution. J. Theor. Biol. 434, 20–33 (2017).
Poole, A. M. & Penny, D. Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 74–84 (2007).
de Duve, C. The origin of eukaryotes: a reappraisal. Nat. Rev. Genet. 8, 395–403 (2007).
Eme, L., Spang, A., Lombard, J., Stairs, C. W. & Ettema, T. J. G. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723 (2017).
Embley, T. M. & Hirt, R. P. Early branching eukaryotes? Curr. Opin. Genet. Dev. 8, 624–629 (1998).
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).
Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).
Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).
Williams, T. A., Cox, C. J., Foster, P. G., Szöllősi, G. J. & Embley, T. M. Phylogenomics provides robust support for a two-domains tree of life. Nat. Ecol. Evol. 138–147 (2019).
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).
Koonin, E. V. Archaeal ancestors of eukaryotes: not so elusive any more. BMC Biol. 13, 84 (2015).
Williams, T. A. & Embley, T. M. Changing ideas about eukaryotic origins. Philos. Trans. R. Soc. Lond. B 370, 20140318 (2015).
Libby, E., Hebert-Dufresne, L., Hosseini, S. R. & Wagner, A. Syntrophy emerges spontaneously in complex metabolic systems. PLoS Comput. Biol. 15, e1007169 (2019).
Spang, A. et al. Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nat. Microbiol. 4, 1138–1148 (2019).
Lopez-Garcia, P. & Moreira, D. Eukaryogenesis, a syntrophy affair. Nat. Microbiol. 4, 1068–1070 (2019).
Imachi, H. et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577, 519–525 (2020).
López-García, P. & Moreira, D. Selective forces for the origin of the eukaryotic nucleus. Bioessays 28, 525–533 (2006).
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. Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier? Philos. Trans. R. Soc. Lond. B 370, 20140333 (2015).
Sagan, L. On the origin of mitosing cells. J. Theor. Biol. 14, 255–274 (1967).
Margulis, L. Origin of eukaryotic cells (Yale Univ. Press, 1970).
Margulis, L., Dolan, M. F. & Guerrero, R. The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc. Natl Acad. Sci. USA 97, 6954–6959 (2000).
Martin, W. & Muller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).
Moreira, D. & López-García, P. Symbiosis between methanogenic archaea and delta-Proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47, 517–530 (1998).
López-García, P. & Moreira, D. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24, 88–93 (1999).
Javaux, E. J. Challenges in evidencing the earliest traces of life. Nature 572, 451–460 (2019).
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).
Betts, H. C. et al. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nat. Ecol. Evol. 2, 1556–1562 (2018).
Martijn, J., Vosseberg, J., Guy, L., Offre, P. & Ettema, T. J. G. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557, 101–105 (2018).
Roger, A. J., Munoz-Gomez, S. A. & Kamikawa, R. The origin and diversification of mitochondria. Curr. Biol. 27, R1177–R1192 (2017).
Luo, G. et al. Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).
Knoll, A. H., Bergmann, K. D. & Strauss, J. V. Life: the first two billion years. Philos. Trans. R. Soc. Lond. B 371, 20150493 (2016).
El Albani, A. et al. Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago. Proc. Natl Acad. Sci. USA 116, 3431–3436 (2019).
Canfield, D. E., Habicht, K. S. & Thamdrup, B. The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288, 658–661 (2000).
Halevy, I., Johnston, D. T. & Schrag, D. P. Explaining the structure of the Archean mass-independent sulfur isotope record. Science 329, 204–207 (2010).
Shen, Y., Knoll, A. H. & Walter, M. R. Evidence for low sulphate and anoxia in a mid-Proterozoic marine basin. Nature 423, 632–635 (2003).
Poulton, S. W., Fralick, P. W. & Canfield, D. E. The transition to a sulphidic ocean approximately 1.84 billion years ago. Nature 431, 173–177 (2004).
Stolper, D. A. & Keller, C. B. A record of deep-ocean dissolved O2 from the oxidation state of iron in submarine basalts. Nature 553, 323 (2018).
Seitz, K. W. et al. Asgard archaea capable of anaerobic hydrocarbon cycling. Nat. Commun. 10, 1822–1822 (2019).
Saghaï, A. et al. Unveiling microbial interactions in stratified mat communities from a warm saline shallow pond. Environ. Microbiol. 19, 2405–2421 (2017).
Bulzu, P. A. et al. Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche. Nat. Microbiol. 4, 1129–1137 (2019).
Hamilton, T. L., Bryant, D. A. & Macalady, J. L. The role of biology in planetary evolution: cyanobacterial primary production in low-oxygen Proterozoic oceans. Environ. Microbiol. 18, 325–340 (2016).
Lenton, T. M. & Daines, S. J. Matworld - the biogeochemical effects of early life on land. New Phytol. 215, 531–537 (2017).
Bolhuis, H., Cretoiu, M. S. & Stal, L. J. Molecular ecology of microbial mats. FEMS Microbiol. Ecol. 90, 335–350 (2014).
Paerl, H. W., Pinckney, J. L. & Steppe, T. F. Cyanobacterial-bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments. Environ. Microbiol. 2, 11–26 (2000).
Martiny, J. B., Jones, S. E., Lennon, J. T. & Martiny, A. C. Microbiomes in light of traits: A phylogenetic perspective. Science 350, aac9323 (2015).
Gutierrez-Preciado, A. et al. Functional shifts in microbial mats recapitulate early Earth metabolic transitions. Nat. Ecol. Evol. 2, 1700–1708 (2018).
Harris, J. K. et al. Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat. ISME J. 7, 50–60 (2013).
Wong, H. L., Smith, D. L., Visscher, P. T. & Burns, B. P. Niche differentiation of bacterial communities at a millimeter scale in Shark Bay microbial mats. Sci. Rep. 5, 15607 (2015).
Dombrowski, N., Seitz, K. W., Teske, A. P. & Baker, B. J. Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments. Microbiome 5, 106 (2017).
Lovley, D. R. Syntrophy goes electric: direct interspecies electron transfer. Annu. Rev. Microbiol. 71, 643–664 (2017).
Fenchel, T. & Finlay, B. J. Ecology and Evolution in Anoxic Worlds (Oxford Univ. Press, 1995).
Lovley, D. R. Happy together: microbial communities that hook up to swap electrons. ISME J. 11, 327–336 (2016).
Mall, A. et al. Reversibility of citrate synthase allows autotrophic growth of a thermophilic bacterium. Science 359, 563–567 (2018).
Krukenberg, V. et al. Candidatus Desulfofervidus auxilii, a hydrogenotrophic sulfate-reducing bacterium involved in the thermophilic anaerobic oxidation of methane. Environ. Microbiol. 18, 3073–3091 (2016).
Oremland, R. S. & Stolz, J. F. The ecology of arsenic. Science 300, 939–944 (2003).
Muyzer, G. & Stams, A. J. The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6, 441–454 (2008).
Knittel, K. & Boetius, A. Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63, 311–334 (2009).
Hillesland, K. L. et al. Erosion of functional independence early in the evolution of a microbial mutualism. Proc. Natl Acad. Sci. USA 111, 14822–14827 (2014).
Hillesland, K. L. & Stahl, D. A. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl Acad. Sci. USA 107, 2124–2129 (2010).
Monteil, C. L. et al. Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist. Nat. Microbiol. 4, 1088–1095 (2019).
Wang, Y., Wegener, G., Hou, J., Wang, F. & Xiao, X. Expanding anaerobic alkane metabolism in the domain of Archaea. Nat. Microbiol. 4, 595–602 (2019).
Shi, T. & Falkowski, P. G. Genome evolution in cyanobacteria: The stable core and the variable shell. Proc. Natl Acad. Sci. USA 105, 2510–2515 (2008).
Shih, P. M. et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl Acad. Sci. USA 110, 1053–1058 (2013).
Martins, M. C. et al. How superoxide reductases and flavodiiron proteins combat oxidative stress in anaerobes. Free Radic. Biol. Med. 140, 36–60 (2019).
Slesak, I., Kula, M., Slesak, H., Miszalski, Z. & Strzalka, K. How to define obligatory anaerobiosis? An evolutionary view on the antioxidant response system and the early stages of the evolution of life on Earth. Free Radic. Biol. Med. 140, 61–73 (2019).
Fischer, W. W., Hemp, J. & Valentine, J. S. How did life survive Earth’s great oxygenation? Curr. Opin. Chem. Biol. 31, 166–178 (2016).
Neubeck, A. & Freund, F. Sulfur chemistry may have paved the way for evolution of antioxidants. Astrobiology (in the press).
Berghuis, B. A. et al. Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens. Proc. Natl Acad. Sci. USA 116, 5037–5044 (2019).
Borrel, G. et al. Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nat. Microbiol. 4, 603–613 (2019).
Evans, P. N. et al. An evolving view of methane metabolism in the Archaea. Nat. Rev. Microbiol. 17, 219–232 (2019).
McKay, L. J. et al. Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota. Nat. Microbiol. 4, 614–622 (2019).
Pittis, A. A. & Gabaldon, T. Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 531, 101–104 (2016).
Canfield, D. E. & Des Marais, D. J. Aerobic sulfate reduction in microbial mats. Science 251, 1471–1473 (1991).
Visscher, P. T. et al. Formation of lithified micritic laminae in modern marine stromatolites (Bahamas): The role of sulfur cycling. Am. Mineral. 83, 1482–1493 (1998).
Munoz-Gomez, S. A., Wideman, J. G., Roger, A. J. & Slamovits, C. H. The origin of mitochondrial cristae from Alphaproteobacteria. Mol. Biol. Evol. 34, 943–956 (2017).
Cavalier-Smith, T. Predation and eukaryote cell origins: a coevolutionary perspective. Int. J. Biochem. Cell Biol. 41, 307–322 (2009).
Martin, W. F., Garg, S. & Zimorski, V. Endosymbiotic theories for eukaryote origin. Philos. Trans. R. Soc. Lond. B 370, 20140330 (2015).
Martijn, J. & Ettema, T. J. From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem. Soc. Trans. 41, 451–457 (2013).
von Dohlen, C. D., Kohler, S., Alsop, S. T. & McManus, W. R. Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412, 433–436 (2001).
Sassera, D. et al. ‘Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int. J. Syst. Evol. Microbiol. 56, 2535–2540 (2006).
Wujek, D. E. Intracellular bacteria in the blue-green alga Pleurocapsa minor. Trans. Am. Microscop. Soc. 98, 143–145 (1979).
Larkin, J. M., Henk, M. C. & Burton, S. D. Occurrence of a Thiothrix sp. attached to mayfly larvae and presence of parasitic bacteria in the Thiothrix sp. Appl. Environ. Microbiol. 56, 357–361 (1990).
Larkin, J. M. & Henk, M. C. Filamentous sulfide-oxidizing bacteria at hydrocarbon seeps of the gulf of Mexico. Microsc. Res. Tech. 33, 23–31 (1996).
Yamaguchi, M. et al. Prokaryote or eukaryote? A unique microorganism from the deep sea. Microscopy 61, 423–431 (2012).
Shiratori, T., Suzuki, S., Kakizawa, Y. & Ishida, K.-I. Phagocytosis-like cell engulfment by a planctomycete bacterium. Nat. Commun. 10, 5529–5529 (2019).
Heimerl, T. et al. A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Front. Microbiol. 8, 1072 (2017).
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).
Jekely, G. Origin and evolution of the self-organizing cytoskeleton in the network of eukaryotic organelles. Cold Spring Harb. Perspect. Biol. 6, a016030 (2014).
Dacks, J. B. & Field, M. C. Evolutionary origins and specialisation of membrane transport. Curr. Opin. Cell Biol. 53, 70–76 (2018).
Dey, G., Thattai, M. & Baum, B. On the archaeal origins of eukaryotes and the challenges of inferring phenotype from genotype. Trends Cell Biol. 26, 476–485 (2016).
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).
Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009).
Lombard, J. The multiple evolutionary origins of the eukaryotic N-glycosylation pathway. Biol. Direct 11, 36 (2016).
Tromer, E. C., van Hooff, J. J. E., Kops, G. & Snel, B. Mosaic origin of the eukaryotic kinetochore. Proc. Natl Acad. Sci. USA 116, 12873–12882 (2019).
Akıl, C. & Robinson, R. C. Genomes of Asgard archaea encode profilins that regulate actin. Nature 562, 439–443 (2018).
Klinger, C. M., Spang, A., Dacks, J. B. & Ettema, T. J. Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol. Biol. Evol. 33, 1528–1541 (2016).
Jekely, G. Small GTPases and the evolution of the eukaryotic cell. Bioessays 25, 1129–1138 (2003).
Low, H. H. & Lowe, J. A bacterial dynamin-like protein. Nature 444, 766–769 (2006).
Santana-Molina, C., Rivas-Marin, E., Rojas, A. M. & Devos, D. P. Origin and evolution of polycyclic triterpene synthesis. Mol. Biol. Evol. (in the press).
Caforio, A. et al. Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane. Proc. Natl Acad. Sci. USA 115, 3704–3709 (2018).
Pogozheva, I. D., Tristram-Nagle, S., Mosberg, H. I. & Lomize, A. L. Structural adaptations of proteins to different biological membranes. Biochim. Biophys. Acta 1828, 2592–2608 (2013).
Makarova, M. et al. Delineating the rules for structural adaptation of membrane-associated proteins to evolutionary changes in membrane lipidome. Curr. Biol. 30, 367–380 (2020).
Shimada, H. & Yamagishi, A. Stability of heterochiral hybrid membrane made of bacterial sn-G3P lipids and archaeal sn-G1P lipids. Biochem. 50, 4114–4120 (2011).
Diekmann, Y. & Pereira-Leal, J. B. Evolution of intracellular compartmentalization. Biochem. J. 449, 319–331 (2013).
Greene, S. E. & Komeili, A. Biogenesis and subcellular organization of the magnetosome organelles of magnetotactic bacteria. Curr. Opin. Cell Biol. 24, 490–495 (2012).
van Niftrik, L. A. et al. The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol. Lett. 233, 7–13 (2004).
Jahn, M. T. et al. Shedding light on cell compartmentation in the candidate phylum Poribacteria by high resolution visualisation and transcriptional profiling. Sci. Rep. 6, 35860 (2016).
Fuerst, J. A. Intracellular compartmentation in planctomycetes. Annu. Rev. Microbiol. 59, 299–328 (2005).
Katayama, T. et al. Membrane-bounded nucleoid discovered in a cultivated bacterium of the candidate phylum ‘Atribacteria’. Preprint at https://www.biorxiv.org/content/10.1101/728279v1 (2019).
Borgnia, M. J., Subramaniam, S. & Milne, J. L. Three-dimensional imaging of the highly bent architecture of Bdellovibrio bacteriovorus by using cryo-electron tomography. J. Bacteriol. 190, 2588–2596 (2008).
Remis, J. P. et al. Bacterial social networks: structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environ. Microbiol. 16, 598–610 (2014).
Naor, A., Lapierre, P., Mevarech, M., Papke, R. T. & Gophna, U. Low species barriers in halophilic archaea and the formation of recombinant hybrids. Curr. Biol. 22, 1444–1448 (2012).
Nudleman, E., Wall, D. & Kaiser, D. Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309, 125–127 (2005).
Cao, P. & Wall, D. Direct visualization of a molecular handshake that governs kin recognition and tissue formation in myxobacteria. Nat. Commun. 10, 3073 (2019).
Jakobczak, B., Keilberg, D., Wuichet, K. & Sogaard-Andersen, L. Contact- and protein transfer-dependent stimulation of assembly of the gliding motility machinery in Myxococcus xanthus. PLoS Genet. 11, e1005341 (2015).
Wolgemuth, C. W. & Oster, G. The junctional pore complex and the propulsion of bacterial cells. J. Mol. Microbiol. Biotechnol. 7, 72–77 (2004).
Nan, B. & Zusman, D. R. Uncovering the mystery of gliding motility in the myxobacteria. Annu. Rev. Genet. 45, 21–39 (2011).
Munoz-Dorado, J., Marcos-Torres, F. J., Garcia-Bravo, E., Moraleda-Munoz, A. & Perez, J. Myxobacteria: moving, killing, feeding, and surviving together. Front. Microbiol. 7, 781 (2016).
Patron, N. J. & Waller, R. F. Transit peptide diversity and divergence: A global analysis of plastid targeting signals. Bioessays 29, 1048–1058 (2007).
Rogozin, I. B., Carmel, L., Csuros, M. & Koonin, E. V. Origin and evolution of spliceosomal introns. Biol. Direct 7, 11 (2012).
Catania, F., Gao, X. & Scofield, D. G. Endogenous mechanisms for the origins of spliceosomal introns. J. Hered. 100, 591–596 (2009).
Vosseberg, J. & Snel, B. Domestication of self-splicing introns during eukaryogenesis: the rise of the complex spliceosomal machinery. Biol. Direct 12, 30 (2017).
Martin, W. & Koonin, E. V. Introns and the origin of nucleus-cytosol compartmentalization. Nature 440, 41–45 (2006).
D’Angelo, M. A. Nuclear pore complexes as hubs for gene regulation. Nucleus 9, 142–148 (2018).
Peña, C., Hurt, E. & Panse, V. G. Eukaryotic ribosome assembly, transport and quality control. Nat. Struct. Mol. Biol. 24, 689 (2017).
Feng, J. M., Tian, H. F. & Wen, J. F. Origin and evolution of the eukaryotic SSU processome revealed by a comprehensive genomic analysis and implications for the origin of the nucleolus. Genome Biol. Evol. 5, 2255–2267 (2013).
Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 6239–6244 (1998).
Pisani, D., Cotton, J. A. & McInerney, J. O. Supertrees disentangle the chimerical origin of eukaryotic genomes. Mol. Biol. Evol. 24, 1752–1760 (2007).
Gabaldon, T. & Huynen, M. A. From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLoS Comput. Biol. 3, e219 (2007).
Gabaldon, T. Relative timing of mitochondrial endosymbiosis and the “pre-mitochondrial symbioses” hypothesis. IUBMB Life 70, 1188–1196 (2018).
Ku, C. et al. Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes. Proc. Natl Acad. Sci. USA 112, 10139–10146 (2015).
López-García, P., Zivanovic, Y., Deschamps, P. & Moreira, D. Bacterial gene import and mesophilic adaptation in archaea. Nat. Rev. Microbiol. 13, 447–456 (2015).
Larkum, A. W., Lockhart, P. J. & Howe, C. J. Shopping for plastids. Trends Plant. Sci. 12, 189–195 (2007).
Philippe, H. et al. Comparison of molecular and paleontological data in diatoms suggests a major gap in the fossil record. J. Evol. Biol. 7, 247–265 (1994).
Zhu, S. Evidence for myxobacterial origin of eukaryotic defensins. Immunogenetics 59, 949–954 (2007).
Perez, J., Castaneda-Garcia, A., Jenke-Kodama, H., Muller, R. & Munoz-Dorado, J. Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome. Proc. Natl Acad. Sci. USA 105, 15950–15955 (2008).
Kerk, D., Uhrig, R. G., Moorhead, G. B. & Bacterial-like, P. P. P. protein phosphatases: novel sequence alterations in pathogenic eukaryotes and peculiar features of bacterial sequence similarity. Plant Signal. Behav. 8, e27365 (2013).
Elias-Arnanz, M., Padmanabhan, S. & Murillo, F. J. The regulatory action of the myxobacterial CarD/CarG complex: a bacterial enhanceosome? FEMS Microbiol. Rev. 34, 764–778 (2010).
Bock, T., Kasten, J., Muller, R. & Blankenfeldt, W. Crystal structure of the HMG-CoA synthase MvaS from the gram-negative bacterium Myxococcus xanthus. Chembiochem. 17, 1257–1262 (2016).
Osborn, A. R. et al. Evolution and distribution of C7-cyclitol synthases in prokaryotes and eukaryotes. ACS Chem. Biol. 12, 979–988 (2017).
Pereto, J., Lopez-Garcia, P. & Moreira, D. Phylogenetic analysis of eukaryotic thiolases suggests multiple proteobacterial origins. J. Mol. Evol. 61, 65–74 (2005).
Schluter, A., Ruiz-Trillo, I. & Pujol, A. Phylogenomic evidence for a myxococcal contribution to the mitochondrial fatty acid beta-oxidation. PloS ONE 6, e21989 (2011).
Stairs, C. W., Leger, M. M. & Roger, A. J. Diversity and origins of anaerobic metabolism in mitochondria and related organelles. Philos. Trans. R. Soc. Lond. B 370, 20140326 (2015).
Baum, D. A. & Baum, B. An inside-out origin for the eukaryotic cell. BMC Biol. 12, 76 (2014).
Sousa, F. L., Neukirchen, S., Allen, J. F., Lane, N. & Martin, W. F. Lokiarchaeon is hydrogen dependent. Nat. Microbiol. 1, 16034 (2016).
Searcy, D. G. in The Origin and Evolution of the Cell (eds Hartman, H. & Matsuno, K.) 47–78 (World Scientific, 1992).
Searcy, D. G. Metabolic integration during the evolutionary origin of mitochondria. Cell Res. 13, 229–238 (2003).
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).
Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).
Field, M. C. & Rout, M. P. Pore timing: the evolutionary origins of the nucleus and nuclear pore complex. F1000 Res. 8, 369 (2019).
Acknowledgements
The authors acknowledge funding from the European Research Council (ERC) grants ProtistWorld (to P.L.-G.; agreement no. 322669) and Plast-Evol (to D.M.; agreement no. 787904), and the French Agence Nationale de la Recherche (to P.L.-G.; grant no. ANR-18-CE02-0013-1).
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P.L.-G. and D.M. conceived and discussed the ideas presented in the manuscript. P.L.-G. wrote the manuscript with critical input from D.M.
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López-García, P., Moreira, D. The Syntrophy hypothesis for the origin of eukaryotes revisited. Nat Microbiol 5, 655–667 (2020). https://doi.org/10.1038/s41564-020-0710-4
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DOI: https://doi.org/10.1038/s41564-020-0710-4
