Genome Networks Root the Tree of Life between Prokaryotic Domains
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Eukaryotes arose from prokaryotes, hence the root in the tree of life resides among the prokaryotic domains. The position of the root is still debated, although pinpointing it would aid our understanding of the early evolution of life. Because prokaryote evolution was long viewed as a tree-like process of lineage bifurcations, efforts to identify the most ancient microbial lineage split have traditionally focused on positioning a root on a phylogenetic tree constructed from one or several genes. Such studies have delivered widely conflicting results on the position of the root, this being mainly due to methodological problems inherent to deep gene phylogeny and the workings of lateral gene transfer among prokaryotes over evolutionary time. Here, we report the position of the root determined with whole genome data using network-based procedures that take into account both gene presence or absence and the level of sequence similarity among all individual gene families that are shared across genomes. On the basis of 562,321 protein-coding gene families distributed across 191 genomes, we find that the deepest divide in the prokaryotic world is interdomain, that is, separating the archaebacteria from the eubacteria. This result resonates with some older views but conflicts with the results of most studies over the last decade that have addressed the issue. In particular, several studies have suggested that the molecular distinctness of archaebacteria is not evidence for their antiquity relative to eubacteria but instead stems from some kind of inherently elevated rate of archaebacterial sequence change. Here, we specifically test for such a rate elevation across all prokaryotic lineages through the analysis of all possible quartets among eight genes duplicated in all prokaryotes, hence the last common ancestor thereof. The results show that neither the archaebacteria as a group nor the eubacteria as a group harbor evidence for elevated evolutionary rates in the sampled genes, either in the recent evolutionary past or in their common ancestor. The interdomain prokaryotic position of the root is thus not attributable to lineage-specific rate variation.
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The deepest, most ancient split in the prokaryotic world is that separating eubacteria from archaebacteria.
“That dichotomy is also mirrored by a number of other cellular, molecular and gene homology attributes, indicating that the deepest, most ancient split in the prokaryotic world is that separating eubacteria from archaebacteria [111,116,122].”
From Early bioenergetic evolution (2013) · cites this paper as [122]
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Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes
Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., Yu, R.-Y., van der Giezen, M., Tielens, A. G. M., & Martin, W. F. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05024-11 · Cited by 838 · see citing works
Self-citationAn archaeal origin of eukaryotes supports only two primary domains of life
Williams, T. A., Foster, P. G., Cox, C. J., & Embley, T. M. (2013) · Nature · doi:10.1038/nature12779 · Cited by 519 · see citing works
Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea
Zhu, Q.-Y., Mai, U., Pfeiffer, W., Janssen, S., Asnicar, F., Sanders, J. G., Belda-Ferre, P., Al-Ghalith, G., Kopylova, E., McDonald, D., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13443-4 · Cited by 309 · see citing works
Sousa, F. L., Thiergart, T., Landan, G., Nelson-Sathi, S., Pereira, I. A. C., Allen, J. F., Lane, N., & Martin, W. F. (2013) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0088 · Cited by 286 · see citing works
“by a number of other cellular, molecular and gene homology attributes, indicating that the deepest, most ancient split in the prokaryotic world is that separating eubacteria from archaebacteria [111,116,122].”
BackgroundSelf-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
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
Self-citationAn 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
Thiergart, T., Landan, G., Schenk, M., Dagan, T., & Martin, W. F. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs018 · Cited by 170 · see citing works
Self-citationKloesges, T., Popa, O., Martin, W. F., & Dagan, T. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq297 · Cited by 158 · see citing works
Self-citationA 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
The advantages and disadvantages of horizontal gene transfer and the emergence of the first species
Vogan, A. A., & Higgs, P. G. (2011) · Biology Direct · doi:10.1186/1745-6150-6-1 · Cited by 145 · see citing works
The hybrid nature of the Eukaryota and a consilient view of life on Earth
McInerney, J. O., O’Connell, M. J., & Pisani, D. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3271 · Cited by 138 · see citing works
Large-Scale Analysis of Plasmid Relationships through Gene-Sharing Networks
Tamminen, M. V., Virta, M., Fani, R., & Fondi, M. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr292 · Cited by 120 · 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
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
Rooting the tree of life: the phylogenetic jury is still out
Gouy, R., Baurain, D., & Philippe, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0329 · Cited by 96 · see citing works
Evolutionary aspects of lipoxygenases and genetic diversity of human leukotriene signaling
Horn, T. L., Adel, S., Schumann, R. R., Sur, S., Kakularam, K. R., Aparoy, P., Reddanna, P., Kühn, H., & Heydeck, D. (2014) · Progress in Lipid Research · doi:10.1016/j.plipres.2014.11.001 · Cited by 92 · see citing works
Supertrees Based on the Subtree Prune-and-Regraft Distance
Whidden, C., Zeh, N., & Beiko, R. G. (2014) · Systematic Biology · doi:10.1093/sysbio/syu023 · Cited by 82 · 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
Dagan, T. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.07.001 · Cited by 76 · see citing works
Self-citationGene similarity networks provide tools for understanding eukaryote origins and evolution
Alvarez‐Ponce, D., Lopez, P., Bapteste, E. P., & McInerney, J. O. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211371110 · Cited by 75 · see citing works
Early evolution without a tree of life
Martin, W. F. (2011) · Biology Direct · doi:10.1186/1745-6150-6-36 · Cited by 68 · see citing works
Self-citationCavalier‐Smith, T. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016006 · Cited by 66 · see citing works
Energy metabolism in anaerobic eukaryotes and Earth's late oxygenation
Zimorski, V., Mentel, M., Tielens, A. G. M., & Martin, W. F. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.03.030 · Cited by 66 · see citing works
Self-citationA catalogue of 136 microbial draft genomes from Red Sea metagenomes
Haroon, M. F., Thompson, L., Parks, D. H., Hugenholtz, P., & Stingl, U. (2016) · Scientific Data · doi:10.1038/sdata.2016.50 · Cited by 64 · 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
“The NR model favours a root on the branch separ-ating the Bacteria from all other cells, in agreement with traditional paralogue rooting approaches [11–13] and analyses of genome networks [54].”
Concatenated alignments and the case of the disappearing tree
Thiergart, T., Landan, G., & Martin, W. F. (2014) · BMC Evolutionary Biology · doi:10.1186/s12862-014-0266-0 · Cited by 59 · see citing works
Self-citationSeligmann, H., & Raoult, D. (2015) · Current Opinion in Microbiology · doi:10.1016/j.mib.2015.11.004 · Cited by 57 · see citing works
Telling the whole story in a 10,000-genome world
Beiko, R. G. (2011) · Biology Direct · doi:10.1186/1745-6150-6-34 · Cited by 52 · see citing works
Rooting Phylogenies and the Tree of Life While Minimizing Ad Hoc and Auxiliary Assumptions
Caetano‐Anollés, G., Nasir, A., Kim, K. M., & Caetano-Anollés, D. (2018) · Evolutionary Bioinformatics · doi:10.1177/1176934318805101 · Cited by 50 · see citing works
Genome size evolution in the Archaea
Kellner, S., Spang, A., Offre, P., Szöllősi, G. J., Petitjean, C., & Williams, T. A. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20180021 · Cited by 48 · see citing works
Investigating the Origins of Membrane Phospholipid Biosynthesis Genes Using Outgroup-Free Rooting
Coleman, G. A., Pancost, R. D., & Williams, T. A. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz034 · Cited by 47 · see citing works
Insights into thermoadaptation and the evolution of mesophily from the bacterial phylum Thermotogae
Pollo, S. M. J., Zhaxybayeva, O., & Nesbø, C. L. (2015) · Canadian Journal of Microbiology · doi:10.1139/cjm-2015-0073 · Cited by 46 · see citing works
Williams, D. F., Fournier, G. P., Lapierre, P., Swithers, K. S., Green, A. G., Andam, C. P., & Gogarten, J. P. (2011) · Biology Direct · doi:10.1186/1745-6150-6-45 · Cited by 44 · see citing works
Philosophy and Evolution: Minding the Gap Between Evolutionary Patterns and Tree-Like Patterns
Bapteste, E. P., Bouchard, F., & Burian, R. M. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-585-5_4 · Cited by 43 · see citing works
Initiation of DNA replication: functional and evolutionary aspects
Bryant, J. A., & Aves, S. J. (2011) · Annals of Botany · doi:10.1093/aob/mcr075 · Cited by 42 · see citing works
The Quest for a Universal Theory of Life
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893 · Cited by 122 · see citing works
Archaea: The First Domain of Diversified Life
Caetano‐Anollés, G., Nasir, A., Zhou, K., Caetano-Anollés, D., Mittenthal, J. E., Sun, F.-J., & Kim, K. M. (2014) · Archaea · doi:10.1155/2014/590214 · Cited by 37 · see citing works
Close 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
Being Aquifex aeolicus: Untangling a Hyperthermophile’s Checkered Past
Eveleigh, R. J. M., Meehan, C. J., Archibald, J. M., & Beiko, R. G. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt195 · Cited by 28 · see citing works
A Tree of Cellular Life Inferred from a Genomic Census of Molecular Functions
Kim, K. M., Nasir, A., Hwang, K., & Caetano‐Anollés, G. (2014) · Journal of Molecular Evolution · doi:10.1007/s00239-014-9637-9 · Cited by 27 · see citing works
Possible mechanisms of CO 2 reduction by H 2 via prebiotic vectorial electrochemistry
Vasiliadou, R., Dimov, N., Szita, N., Jordan, S. F., & Lane, N. J. (2019) · Interface Focus · doi:10.1098/rsfs.2019.0073 · Cited by 28 · see citing works
Changing ideas about eukaryotic origins
Williams, T. A., & Embley, T. M. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0318 · Cited by 26 · see citing works
Primal Eukaryogenesis: On the Communal Nature of Precellular States, Ancestral to Modern Life
Egel, R. (2012) · Life · doi:10.3390/life2010170 · Cited by 21 · see citing works
Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere
Spang, A., Mahendrarajah, T., Offre, P., & Stairs, C. W. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac034 · Cited by 19 · see citing works
How the virophage compels the need to readdress the classification of microbes
Raoult, D. (2014) · Virology · doi:10.1016/j.virol.2014.11.014 · Cited by 18 · see citing works
Arnoldt, H., Strogatz, S. H., & Timme, M. (2015) · Physical Review E · doi:10.1103/physreve.92.052909 · Cited by 17 · see citing works
The Methodology Behind Network Thinking: Graphs to Analyze Microbial Complexity and Evolution.
Watson, A. K., Lannes, R., Pathmanathan, J., Méheust, R., Karkar, S., Colson, P., Corel, E., Lopez, P., & Bapteste, É. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9074-0_9 · Cited by 8 · see citing works
Marine Microorganisms: perspectives for getting involved in cellulosic ethanol
Intriago, P. (2012) · AMB Express · doi:10.1186/2191-0855-2-46 · Cited by 13 · see citing works
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.004 · Cited by 11 · see citing works
Nathani, N. M., Dave, K. J., Vatsa, P. P., Mahajan, M. S., Sharma, P., & Chandrashekar, M. (2021) · Scientific Data · doi:10.1038/s41597-021-00957-0 · Cited by 11 · see citing works
Bapteste, E. P., Huneman, P., Keller, L., Teulière, J., Lopez, P., Teeling, E. C., Lindner, A. B., Baudisch, A., Ludington, W. B., & Franceschi, C. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101982 · Cited by 10 · see citing works
The performance of outgroup-free rooting under evolutionary radiations
Lamarca, A. P., Mello, B., & Schrago, C. G. (2022) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2022.107434 · Cited by 9 · see citing works
FUNGI | Classification of the Basidiomycota
Brondz, I. (2014) · Encyclopedia of Food Microbiology · doi:10.1016/b978-0-12-384730-0.00139-7 · Cited by 8 · see citing works
Microbial Diversity and Open Questions about the Deep Tree of Life
Eme, L., & Tamarit, D. (2024) · Genome Biology and Evolution · doi:10.1093/gbe/evae053 · Cited by 8 · see citing works
Diversity of Genome Organisation
Budd, A. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-582-4_2 · Cited by 8 · see citing works
Goode, O., Łapińska, U., Morimoto, J., Glover, G., Milner, D. S., Santoro, A. E., Pagliara, S., & Richards, T. A. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003155 · Cited by 6 · see citing works
Romance of the three domains: how cladistics transformed the classification of cellular organisms
Ho, C.-C., Lau, S. K. P., & Woo, P. C. Y. (2013) · Protein & Cell · doi:10.1007/s13238-013-3050-9 · Cited by 6 · see citing works
The power and limitations of species tree-aware phylogeneticsPreprint
Williams, T. A., Davín, A., Morel, B., Szánthó, L. L., Spang, A., Stamatakis, A., Hugenholtz, P., & Szöllősi, G. J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.17.533068 · Cited by 6 · see citing works
Dick, A. A., Harlow, T. J., & Gogarten, J. P. (2016) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2016.11.016 · Cited by 5 · see citing works
Phylogenomic Testing of Root Hypotheses
Tria, F. D. K., Landan, G., Picazo, D. R., & Dagan, T. (2023) · Genome Biology and Evolution · doi:10.1093/gbe/evad096 · Cited by 2 · see citing works
Self-citationReconstructing the Last Universal Common Ancestor
Poole, A. M. (2021) · Advances in astrobiology and biogeophysics · doi:10.1007/978-3-030-81039-9_9 · Cited by 3 · see citing works
Phylogenetic analysis of housekeeping Archaeal proteins and early stages of Archaea evolution
Владимирович, Г. К., Suslov, V. V., & Afonnikov, D. A. (2013) · Paleontological Journal · doi:10.1134/s0031030113090098 · Cited by 1 · see citing works
Searching for Extraterrestrial Life Without a Definition or Universal Theory of Life
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Challenges for a Universal Theory of Life
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.006 · Cited by 1 · see citing works
STORI: Selectable Taxon Ortholog Retrieval Iteratively
Stern, J. G. (2015) · SMARTech Repository (Georgia Institute of Technology) · doi:10.13140/rg.2.1.4458.0961 · Cited by 1 · see citing works
Resolving the origins of membrane phospholipid biosynthesis genes using outgroupfree rootingPreprint
Coleman, G. A., Pancost, R. D., & Williams, T. A. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/312991 · Cited by 1 · see citing works
Egel, R. (2024) · Preprints.org · doi:10.20944/preprints202405.0555.v1
Phylogenomic Networks of Microbial Genome Evolution
Dagan, T., Popa, O., Kloesges, T., & Landan, G. (2015) · ASM Press eBooks · doi:10.1128/9781555818821.ch4.1.1
Self-citationLópez, C. E., & Carrascal, L. (2011)
Membrane bioenergetics at major transitions in evolution
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Structural and functional advances in the evolutionary studies of cells and viruses
Nasir, A. (2015) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Short Branch Attraction, the Fundamental Bipartition in Cellular Life, and Eukaryogenesis
Dick, & Amanda, A. (2016)
A Shadow Biosphere: Alien Microbes on Earth?
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.010
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.002
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.003
How Scientific Theories Develop
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.005
Rethinking the Traditional Paradigm for Life: Lessons from the World of Microbes
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.007
Artificial Life: Could ALife Solve theN = 1N=1 Problem?
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.008
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.001
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.011
(2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.012
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.013
Joseph, A. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-95717-5.00011-6
- Authors
- Dagan, T., Roettger, M., Bryant, D., & Martin, W.
- Affiliations
- Heinrich Heine University Düsseldorf (DE)
- University of Auckland (NZ)
- Corresponding author
- Dagan, Tal
- Venue
- Genome Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-01-01
- Volume
- 2
- Pages
- 379-392
- ISSN
- 1759-6653 (ISSN-L)
- PMC
- PMC2997548
- OpenAlex
- W2130436157
- Cited by
- 87
- References
- 107
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 4 · 2022: 2 · 2021: 2 · 2019: 22 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 9 · 2014: 12 · 2013: 7 · 2012: 6
- FWCI
- 2.87
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc
- Locations
- Genome Biology and Evolution (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- Alexander von Humboldt-Stiftung
- Royal Society
- Royal Society Te Apārangi
- Deutsche Forschungsgemeinschaft
- 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 › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- archaea, bacteria, eukaryotic origin, horizontal gene transfer, phylogenetic networks, molecular clock, rate heterogeneity, last common ancestor
- MeSH terms
- Archaea, Bacteria, Multigene Family, Models, Genetic, Phylogeny, Prokaryotic Cells, Genome, Evolution, Molecular, Gene Regulatory Networks, INDEL Mutation
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