An archaeal origin of eukaryotes supports only two primary domains of life
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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.
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The translational machinery was identified as one of the most ancient systems in biology and as part of the core of the hypothetical Last Universal Common Ancestor (LUCA).
“Thus, the translational machinery was identified as one of the most ancient of systems in biology and was forming part of the core of the (hypothetical) Last Universal Common Ancestor (LUCA)”
From The Emergence of Life (2019) · cites this paper as Williams et al. 2013
Cites
Woese, C. R. (1987) · Microbiological Reviews · doi:10.1128/mr.51.2.221-271.1987 · Cited by 5,042 · 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
Resolving difficult phylogenetic questions: Why more sequences are not enough
Philippe, H., Brinkmann, H., Lavrov, D. V., Littlewood, D. T. J., Manuel, M., Wörheide, G., & Baurain, D. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000602 · Cited by 1,129 · see citing works
Iwabe, N., Kuma, K., Hasegawa, M., Osawa, S., & Miyata, T. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.23.9355 · Cited by 902 · see citing works
Estimating 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
Self-citationLartillot, N., Brinkmann, H., & Philippe, H. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-s1-s4 · Cited by 705 · 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
Modeling compositional heterogeneity
Foster, P. G. (2004) · Systematic Biology · doi:10.1080/10635150490445779 · Cited by 474 · see citing works
Self-citationThe 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
Controls on development and diversity of Early Archean stromatolites
Allwood, A. C., Grotzinger, J. P., Knoll, A. H., Burch, I. W., Anderson, M. S., Coleman, M. L., & Kanik, I. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903323106 · Cited by 305 · see citing works
Mathematical Elegance with Biochemical Realism: The Covarion Model of Molecular Evolution
Penny, D., McComish, B. J., Charleston, M. A., & Hendy, M. D. (2001) · Journal of Molecular Evolution · doi:10.1007/s002390010258 · Cited by 287 · see citing works
Mapping the Tree of Life: Progress and Prospects
Pace, N. R. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00033-09 · Cited by 286 · see citing works
Pace, N. R. (2006) · Nature · doi:10.1038/441289a · Cited by 276 · see citing works
The Rooting of the Universal Tree of Life Is Not Reliable
Philippe, H., & Forterre, P. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006573 · Cited by 267 · see citing works
Evolution 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
Genome Networks Root the Tree of Life between Prokaryotic Domains
Dagan, T., Roettger, M., Bryant, D., & Martin, W. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq025 · Cited by 87 · see citing works
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Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life
Parks, D. H., Rinke, C., Chuvochina, M., Chaumeil, P.-A., Woodcroft, B. J., Evans, P. N., Hugenholtz, P., & Tyson, G. W. (2017) · Nature Microbiology · doi:10.1038/s41564-017-0012-7 · Cited by 1,882 · see citing works
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
Algae-bacteria interactions: Evolution, ecology and emerging applications
Ramanan, R., Kim, B.-H., Cho, D.-H., Oh, H.-M., & Kim, H.-S. (2016) · Biotechnology Advances · doi:10.1016/j.biotechadv.2015.12.003 · Cited by 1,301 · see citing works
Asgard archaea illuminate the origin of eukaryotic cellular complexity
Zaremba-Niedzwiedzka, K., Caceres, E. F., Saw, J. H., Bäckström, D., Juzokaite, L., Vancaester, E., Seitz, K. W., Anantharaman, K., Starnawski, P., Kjeldsen, K. U., et al. (2017) · Nature · doi:10.1038/nature21031 · Cited by 1,226 · see citing works
The physiology and habitat of the last universal common ancestor
Weiss, M. C., Sousa, F. L., Mrnjavac, N., Neukirchen, S., Roettger, M., Nelson-Sathi, S., & Martin, W. F. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.116 · Cited by 1,049 · see citing works
Endosymbiosis and Eukaryotic Cell Evolution
Archibald, J. M. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.055 · Cited by 654 · see citing works
Endosymbiotic theories for eukaryote origin
Martin, W. F., Garg, S., & Zimorski, V. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0330 · Cited by 583 · see citing works
Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin
Betts, H. C., Puttick, M. N., Clark, J. W., Williams, T. A., Donoghue, P. C. J., & Pisani, D. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0644-x · Cited by 437 · see citing works
Self-citationEndosymbiotic theory for organelle origins
Zimorski, V., Ku, C., Martin, W. F., & Gould, S. B. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.09.008 · Cited by 453 · see citing works
Archaea and the Human Gut: New Beginning of an Old Story
Gaci, N., Borrel, G., Tottey, W., O’Toole, P. W., & Brugère, J.-F. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i43.16062 · Cited by 422 · see citing works
Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life
Spang, A., Caceres, E. F., & Ettema, T. J. G. (2017) · Science · doi:10.1126/science.aaf3883 · Cited by 346 · see citing works
Phylogenomics provides robust support for a two-domains tree of life
Williams, T. A., Cox, C. J., Foster, P. G., Szöllősi, G. J., & Embley, T. M. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-1040-x · Cited by 274 · see citing works
Self-citationIntegrative modeling of gene and genome evolution roots the archaeal tree of life
Williams, T. A., Szöllősi, G. J., Spang, A., Foster, P. G., Heaps, S. E., Boussau, B., Ettema, T. J. G., & Embley, T. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1618463114 · Cited by 233 · see citing works
Self-citationSpang, A., Stairs, C. W., Dombrowski, N., Eme, L., Lombard, J., Caceres, E. F., Greening, C., Baker, B. J., & Ettema, T. J. G. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0406-9 · Cited by 200 · see citing works
The last universal common ancestor between ancient Earth chemistry and the onset of genetics
Weiss, M. C., Preiner, M., Xavier, J. C., Zimorski, V., & Martin, W. F. (2018) · PLOS Genetics · doi:10.1371/journal.pgen.1007518 · Cited by 186 · see citing works
Biosynthesis of polyamines and polyamine-containing molecules
Michael, A. J. (2016) · Biochemical Journal · doi:10.1042/bcj20160185 · Cited by 180 · see citing works
An origin-of-life reactor to simulate alkaline hydrothermal vents
Herschy, B., Whicher, A., Camprubi, E., Watson, C., Dartnell, L., Ward, J., Evans, J. R. G., & Lane, N. (2014) · Journal of Molecular Evolution · doi:10.1007/s00239-014-9658-4 · Cited by 194 · see citing works
Tan, D.-X., Zheng, X., Kong, J., Manchester, L., Hardeland, R., Kim, S., Xu, X., & Reiter, R. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150915858 · Cited by 188 · see citing works
A Bioenergetic Basis for Membrane Divergence in Archaea and Bacteria
Sojo, V., Pomiankowski, A., & Lane, N. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001926 · Cited by 154 · see citing works
Symbiosis in eukaryotic evolution
López-García, P., Eme, L., & Moreira, D. (2017) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2017.02.031 · Cited by 154 · see citing works
Koonin, E. V. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0333 · Cited by 145 · see citing works
Constraining the Time Interval for the Origin of Life on Earth
Pearce, B. K. D., Tupper, A. S., Pudritz, R. E., & Higgs, P. G. (2018) · Astrobiology · doi:10.1089/ast.2017.1674 · Cited by 140 · see citing works
Early Microbial Evolution: The Age of Anaerobes
Martin, W. F., & Sousa, F. L. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018127 · Cited by 129 · see citing works
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Judson, O. P. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0138 · Cited by 118 · see citing works
Proton gradients at the origin of life
Lane, N. (2017) · BioEssays · doi:10.1002/bies.201600217 · Cited by 115 · see citing works
Sousa, F. L., & Martin, W. F. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2014.02.001 · Cited by 100 · see citing works
Human TLR8 senses UR/URR motifs in bacterial and mitochondrial RNA
Krüger, A., Oldenburg, M., Chebrolu, C., Beisser, D., Kolter, J., Sigmund, A. M., Steinmann, J., Schäfer, S., Hochrein, H., Rahmann, S., et al. (2015) · The EMBO Reports · doi:10.15252/embr.201540861 · Cited by 99 · see citing works
Camprubí, E., de Leeuw, J. W., House, C. H., Raulin, F., Russell, M. J., Spang, A., Tirumalai, M. R., & Westall, F. (2019) · Space Science Reviews · doi:10.1007/s11214-019-0624-8 · Cited by 84 · see citing works
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Doolittle, W. F. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.010 · Cited by 75 · see citing works
New substitution models for rooting phylogenetic trees
Williams, T. A., Heaps, S. E., Cherlin, S., Nye, T. M. W., Boys, R. J., & Embley, T. M. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0336 · Cited by 61 · see citing works
“Based on recently published analyses of rRNA and protein-coding genes, this tree is currently thought to be incorrect [10,42,44,52,53], although it has historically received support from simpler stationary models (reviewed in [10]).”
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Archaeal Histone Contributions to the Origin of Eukaryotes
Brunk, C. F., & Martin, W. F. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.04.002 · Cited by 55 · see citing works
Late Mitochondrial Origin Is an Artifact
Martin, W. F., Roettger, M., Ku, C., Garg, S. G., Nelson-Sathi, S., & Landan, G. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx027 · Cited by 42 · see citing works
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Martin, H. S., Podolsky, K. A., & Devaraj, N. K. (2021) · ChemBioChem · doi:10.1002/cbic.202100232 · Cited by 36 · see citing works
Late Proterozoic Transitions in Climate, Oxygen, and Tectonics, and the Rise of Complex Life
Planavsky, N. J., Tarhan, L. G., Bellefroid, E. J., Evans, D. A. D., Reinhard, C. T., Love, G. D., & Lyons, T. W. (2015) · The Paleontological Society Papers · doi:10.1017/s1089332600002965 · Cited by 32 · see citing works
A structural phylogenetic tree of Rad52 and its annealase superfamily
Al-Fatlawi, A., Hossen, M. B., de Paula Lopes, S., Stewart, A. F., & Schroeder, M. (2025) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2024.12.012 · Cited by 3 · see citing works
- Authors
- Williams, T. A., Foster, P. G., Cox, C. J., & Embley, T. M.
- Affiliations
- Newcastle University (GB)
- Natural History Museum (GB)
- University of Algarve (PT)
- Corresponding author
- Embley, T. Martin
- Venue
- Nature
- Published
- 2013-12
- Volume
- 504
- Issue
- 7479
- Pages
- 231-236
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2049117477
- Cited by
- 519
- References
- 17
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 18 · 2023: 38 · 2022: 44 · 2021: 31 · 2020: 44 · 2019: 56 · 2018: 45 · 2017: 52 · 2016: 51 · 2015: 61 · 2014: 51
- FWCI
- 5.11
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- cc-by-nc
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Bristol Research (University of Bristol) (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion)
- Newcastle University ePrints (Newcastle Univesity) (cc-by-nc)
- Funders
- Wellcome Trust
- Biotechnology and Biological Sciences Research Council (BB/C006143/1, BB/C508777/1)
- 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 › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- eukaryotic origin, archaeal diversity, phylogenetic inference, mitochondrial endosymbiosis, ribosomal RNA phylogeny, cell evolution
- MeSH terms
- Archaea, Bacteria, Cell Membrane, Mitochondria, Models, Biological, Phylogeny, RNA, Ribosomal, Symbiosis, Eukaryota
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