Integrative modeling of gene and genome evolution roots the archaeal tree of life
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Significance: The Archaea represent a primary domain of cellular life, play major roles in modern-day biogeochemical cycles, and are central to debates about the origin of eukaryotic cells. However, understanding their origins and evolutionary history is challenging because of the immense time spans involved. Here we apply a new approach that harnesses the information in patterns of gene family evolution to find the root of the archaeal tree and to resolve the metabolism of the earliest archaeal cells. Our approach robustly distinguishes between published rooting hypotheses, suggests that the first Archaea were anaerobes that may have fixed carbon via the Wood–Ljungdahl pathway, and quantifies the cumulative impact of horizontal transfer on archaeal genome evolution.
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The last archaeal common ancestor (LACA) is likely to have encoded a CODH/ACS.
“Furthermore, the last archaeal common ancestor (LACA) is likely to have encoded a CODH/ACS (Williams et al. 2017).”
From The Emergence of Life (2019) · cites this paper as Williams et al. 2017
The Fig. 4 caption (Results and Discussion, p. 7) says the reconstruction supports a LACA that encoded cdhC, a subunit of CODH/ACS. It does not establish that LACA encoded the complete enzyme, as the citing sentence implies; the caption also notes that reconstructions at deep nodes are incomplete. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe ancestral physiology of archaea was likely hydrogen-dependent methanogenesis.
“Mei et al. (2023) and Williams et al. (2017) found that the ancestral physiology of archaea was likely hydrogen-dependent methanogenesis.”
From Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life (2023) · cites this paper as Williams et al., 2017
The Results and Discussion (pp. 6, 9) suggest that the last archaeal common ancestor was an anaerobe that may have fixed CO2 through the Wood–Ljungdahl pathway, but say its electron donor could not be determined. On p. 7, key methanogenesis enzymes map with high probability only to the base of Euryarchaeota. The paper therefore does not establish hydrogen-dependent methanogenesis as the ancestral physiology of all archaea. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe ancestors of Archaea were thermophilic or hyperthermophilic.
“while the ancestors of Bacteria and Archaea were thermophilic (Boussau et al. 2008) and thermophilic or hyperthermophilic (Groussin and Gouy 2011;Williams et al. 2017), respectively, LUCA may have been a mesophilic organism (Boussau et al. 2008).”
From The Emergence of Life (2019) · cites this paper as Williams et al. 2017
The cA1V1 and ncA1V1 subunits were present in LACA (PPs = 0.99-1) and the cF1 and ncF1 subunits were present in LBCA (PPs = 0.99-1).
“suggesting that the cA1V1 and ncA1V1 subunits were present in LACA (presence probability, PPs = 0.99–1)67 and the cF1 and ncF1 subunits were present in LBCA (PPs = 0.99–1)21.”
From ATP synthase evolution on a cross-braced dated tree of life (2023) · cites this paper as [67]
The Results and Discussion (p. 7) say that two V-type ATP synthase subunits were mapped to the DPANN common ancestor, not explicitly to LACA. Searches for cA1V1, ncA1V1, and their stated presence probabilities found no passage in our copy establishing the claim attributed to this source. The LBCA portion is attached to a different citation and is not assessed here. (LLM, conf=0.72)
Experimental — accuracy not yet measuredThe A/V-type ATP synthase was present in LACA and the F-type ATP synthase was in LBCA.
“The results of our analyses confirm that the A/V-type ATP synthase was present in LACA67 and the F-type ATP synthase was in LBCA19–22.”
From ATP synthase evolution on a cross-braced dated tree of life (2023) · cites this paper as [67]
Citation 67 is attached to the claim about A/V-type ATP synthase in LACA, not the separately cited claim about F-type ATP synthase in LBCA. The Results and Discussion (p. 7) maps two V-type ATP synthase subunits to the DPANN common ancestor, but does not establish that an A/V-type ATP synthase was present in LACA. Searches for A/V-type ATP synthase, V-type ATP synthase, and ATP synthase in LACA found no decisive passage. (LLM, conf=0.72)
Experimental — accuracy not yet measured
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Morgan, C. C., Foster, P. G., Webb, A. E., Pisani, D., McInerney, J. O., & O’Connell, M. J. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst117 · Cited by 123 · see citing works
Self-citationThe primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods
Foster, P. G., Cox, C. J., & Embley, T. M. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0034 · Cited by 120 · see citing works
Self-citationOrtiz‐Álvarez, R., & Casamayor, E. O. (2015) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12370 · Cited by 114 · see citing works
Bacterial gene import and mesophilic adaptation in archaea
López‐García, P., Zivanovic, Y., Deschamps, P., & Moreira, D. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3485 · Cited by 112 · see citing works
Podar, M., Makarova, K. S., Graham, D. E., Wolf, Y. I., Koonin, E. V., & Reysenbach, A. (2013) · Biology Direct · doi:10.1186/1745-6150-8-9 · Cited by 111 · see citing works
Genome-scale phylogenetic analysis finds extensive gene transfer among fungi
Szöllősi, G. J., Davín, A., Tannier, É., Daubin, V., & Boussau, B. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0335 · Cited by 101 · see citing works
Self-citationSousa, 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
Archaeal “Dark Matter” and the Origin of Eukaryotes
Williams, T. A., & Embley, T. M. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu031 · Cited by 100 · see citing works
Self-citationDeschamps, P., Zivanovic, Y., Moreira, D., Rodríguez‐Valera, F., & López‐García, P. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu127 · Cited by 100 · see citing works
Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the ‘lipid divide’
Villanueva, L., Stefan Schouten, A., & Damsté, J. S. S. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13361 · Cited by 98 · see citing works
Youssef, N. H., Rinke, C., Stepanauskas, R., Farag, I., Woyke, T., & Elshahed, M. S. (2014) · The ISME Journal · doi:10.1038/ismej.2014.141 · Cited by 97 · 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
The Problem of Rooting Rapid Radiations
Grievink, L. S., Penny, D., Hendy, M. D., & Holland, B. R. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm178 · Cited by 82 · see citing works
Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes
Saw, J. H. W., Spang, A., Zaremba-Niedźwiedzka, K., Juzokaite, L., Dodsworth, J. A., Murugapiran, S. K., Colman, D. R., Takacs‐Vesbach, C. D., Hedlund, B. P., Guy, L., et al. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0328 · Cited by 80 · see citing works
Self-citationAncient gene duplications and the root(s) of the tree of life
Zhaxybayeva, O., Lapierre, P., & Gogarten, J. P. (2005) · PROTOPLASMA · doi:10.1007/s00709-005-0135-1 · Cited by 75 · see citing works
Genome beginnings: rooting the tree of life
Lake, J. A., Skophammer, R. G., Herbold, C. W., & Servin, J. A. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0035 · Cited by 74 · see citing works
Inter-species interconnections in acid mine drainage microbial communities
Comolli, L. R., & Banfield, J. F. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00367 · Cited by 69 · see citing works
The effects of model choice and mitigating bias on the ribosomal tree of life
Lasek‐Nesselquist, E., & Gogarten, J. P. (2013) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2013.05.006 · Cited by 63 · 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 · cited 1× · see citing works
“under standard models of sequence evolution, which do not directly infer the root (55, 56).”
Self-citationOne step beyond a ribosome: The ancient anaerobic core
Sousa, F. L., Nelson-Sathi, S., & Martin, W. F. (2016) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2016.04.284 · Cited by 58 · see citing works
A Branch-Heterogeneous Model of Protein Evolution for Efficient Inference of Ancestral Sequences
Groussin, M., Boussau, B., & Gouy, M. (2013) · Systematic Biology · doi:10.1093/sysbio/syt016 · Cited by 56 · see citing works
Self-citationThe Estimation of Tree Posterior Probabilities Using Conditional Clade Probability Distributions
Larget, B. R. (2013) · Systematic Biology · doi:10.1093/sysbio/syt014 · Cited by 48 · see citing works
Gene Acquisitions from Bacteria at the Origins of Major Archaeal Clades Are Vastly Overestimated
Groussin, M., Boussau, B., Szöllősi, G. J., Eme, L., Gouy, M., Brochier‐Armanet, C., & Daubin, V. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv249 · Cited by 35 · see citing works
Self-citationClose Encounters of the Third Domain: The Emerging Genomic View of Archaeal Diversity and Evolution
Spang, A., Martijn, J., Saw, J. H. W., Lind, A. E., Guy, L., & Ettema, T. J. G. (2013) · Archaea · doi:10.1155/2013/202358 · Cited by 31 · see citing works
Self-citationThe molecular signal for the adaptation to cold temperature during early life on Earth
Groussin, M., Boussau, B., Charles, S., Blanquart, S., & Gouy, M. (2013) · Biology Letters · doi:10.1098/rsbl.2013.0608 · Cited by 29 · see citing works
Self-citationHorizontal Gene Transfer: Pitfalls and Promises
Gogarten, J. P., Murphey, R. D., & Olendzenski, L. (1999) · Biological Bulletin · doi:10.2307/1542970 · Cited by 27 · see citing works
Akanni, W. A., Siu-Ting, K., Creevey, C. J., McInerney, J. O., Wilkinson, M., Foster, P. G., & Pisani, D. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0337 · Cited by 27 · see citing works
Self-citationEvidence that the Root of the Tree of Life Is Not within the Archaea
Skophammer, R. G., Herbold, C. W., Rivera, M. C., Servin, J. A., & Lake, J. A. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl046 · Cited by 26 · see citing works
Bayesian modelling of compositional heterogeneity in molecular phylogenetics
Heaps, S. E., Nye, T. M. W., Boys, R. J., Williams, T. A., & Embley, T. M. (2014) · Statistical Applications in Genetics and Molecular Biology · doi:10.1515/sagmb-2013-0077 · Cited by 20 · see citing works
Self-citationStructural Basis for a Unique ATP Synthase Core Complex from Nanoarcheaum equitans
Mohanty, S., Jobichen, C., Chichili, V. P. R., Velázquez-Campoy, A., Low, B. C., Hogue, C. W. V., & Sivaraman, J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.677492 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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-citationGenomic 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
Self-citationA rooted phylogeny resolves early bacterial evolution
Coleman, G. A., Davín, A. A., Mahendrarajah, T. A., Szánthó, L. L., Spang, A., Hugenholtz, P., Szöllősi, G. J., & Williams, T. A. (2021) · Science · doi:10.1126/science.abe0511 · Cited by 285 · see citing works
Self-citationPhylogenomics 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-citationAdam, P. S., Borrel, G., & Gribaldo, S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716667115 · Cited by 226 · see citing works
Genomic diversity, lifestyles and evolutionary origins of DPANN archaea
Dombrowski, N., Lee, J.-H., Williams, T. A., Offre, P., & Spang, A. (2019) · FEMS Microbiology Letters · doi:10.1093/femsle/fnz008 · Cited by 230 · 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
Self-citationThe 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
An estimate of the deepest branches of the tree of life from ancient vertically evolving genes
Moody, E. R., Mahendrarajah, T. A., Dombrowski, N., Clark, J. W., Petitjean, C., Offre, P., Szöllősi, G. J., Spang, A., & Williams, T. A. (2022) · eLife · doi:10.7554/elife.66695 · Cited by 95 · see citing works
Self-citationSerpentinization: connecting geochemistry, ancient metabolism and industrial hydrogenation
Preiner, M., Xavier, J. C., Sousa, F. L., Zimorski, V., Neubeck, A., Lang, S. Q., Greenwell, H. C., Kleinermanns, K., Tüysüz, H., McCollom, T. M., et al. (2018) · Life · doi:10.3390/life8040041 · Cited by 97 · see citing works
Phylogenetic Signal, Congruence, and Uncertainty across Bacteria and Archaea
Martinez-Gutierrez, C. A., & Aylward, F. O. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab254 · Cited by 95 · see citing works
ATP synthase evolution on a cross-braced dated tree of life
Mahendrarajah, T. A., Moody, E. R. R., Schrempf, D., Szánthó, L. L., Dombrowski, N., Davín, A. A., Pisani, D., Donoghue, P. C. J., Szöllősi, G. J., Williams, T. A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42924-w · Cited by 86 · see citing works
Self-citationCamprubí, 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
Self-citationSchwander, L., Brabender, M., Mrnjavac, N., Wimmer, J. L. E., Preiner, M., & Martin, W. F. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1257597 · Cited by 65 · see citing works
“Mei et al. (2023) and Williams et al. (2017) found that the ancestral physiology of archaea was likely hydrogen-dependent methanogenesis.”
BackgroundThe metabolic network of the last bacterial common ancestor
Xavier, J. C., Gerhards, R. E., Wimmer, J. L. E., Brueckner, J., Tria, F. D. K., & Martin, W. F. (2021) · Communications Biology · doi:10.1038/s42003-021-01918-4 · Cited by 59 · see citing works
Hernandez, A. M., & Ryan, J. F. (2019) · doi:10.1101/729103 · Cited by 52 · see citing works
The origin and evolution of methanogenesis and <i>Archaea</i> are intertwined
Mei, R., Kaneko, M., Imachi, H., & Nobu, M. K. (2023) · PNAS Nexus · doi:10.1093/pnasnexus/pgad023 · Cited by 37 · see citing works
Hidden Concepts in the History and Philosophy of Origins-of-Life Studies: A Workshop Report
Mariscal, C., Barahona, A., Aubert-Kato, N., Aydinoglu, A. U., Bartlett, S., Cárdenas, M. L., Chandru, K., Cleland, C., Cocanougher, B. T., Comfort, N., et al. (2019) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-019-09580-x · Cited by 36 · see citing works
Small-molecule autocatalytic networks are universal metabolic fossils
Xavier, J. C., & Kauffman, S. (2022) · Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences · doi:10.1098/rsta.2021.0244 · Cited by 34 · see citing works
Relative Time Constraints Improve Molecular Dating
Szöllõsi, G. J., Höhna, S., Williams, T. A., Schrempf, D., Daubin, V., & Boussau, B. (2022) · Systematic Biology · doi:10.1093/sysbio/syab084 · Cited by 23 · see citing works
Self-citation
- Authors
- Williams, T. A., Szöllősi, G. J., Spang, A., Foster, P. G., Heaps, S. E., Boussau, B., Ettema, T. J. G., & Embley, T. M.
- Affiliations
- University of Bristol (GB)
- Eötvös Loránd University (HU)
- Uppsala University (SE)
- Natural History Museum (GB)
- Newcastle University (GB)
- Lyon 1 Université (FR)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2017-05-22
- Volume
- 114
- Issue
- 23
- Pages
- E4602-E4611
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5468678
- OpenAlex
- W2616865631
- Cited by
- 233
- References
- 115
- Citations by year
- 2026: 9 · 2025: 11 · 2024: 22 · 2023: 23 · 2022: 26 · 2021: 32 · 2020: 31 · 2019: 32 · 2018: 35 · 2017: 11
- FWCI
- 12.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Bristol Research (University of Bristol) (publishedVersion, other-oa)
- Socio-Environmental Systems Modeling (acceptedVersion)
- HAL (submittedVersion)
- Durham Research Online (Durham University) (submittedVersion, cc-by)
- Explore Bristol Research (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Royal Society (UF140626)
- Wellcome Trust (045404)
- EC | European Research Council (ERC- 2010-AdG-268701, 310039-PUZZLE_CELL)
- Swedish Foundation for Strategic Research (SSF-FFL5)
- Vetenskapsrådet (2015-04959)
- European Commission (Marie Curie 625521)
- Biotechnology and Biological Sciences Research Council (BB/G024707/1)
- Agence Nationale de la Recherche (ANR-10-BINF-01-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- 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
- Keywords
- archaea, gene family evolution, archaeal metabolism, Wood-Ljungdahl pathway, horizontal gene transfer, eukaryotic origin
- MeSH terms
- Algorithms, Archaea, Multigene Family, Models, Genetic, Phylogeny, Temperature, Evolution, Molecular, Gene Duplication, Genome, Archaeal, Gene Transfer, Horizontal, Metabolic Networks and Pathways, Eukaryota
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