Horizontal gene transfer constrains the timing of methanogen evolution
Open accessPublished version of a preprint
Abstract
Microbial methanogenesis may have been a major component of Earth's carbon cycle during the Archaean eon, generating a methane greenhouse that increased global temperatures enough for a liquid hydrosphere, despite the Sun's lower luminosity at the time. Evaluation of potential solutions to the 'faint young Sun' hypothesis by determining the age of microbial methanogenesis has been limited by ambiguous geochemical evidence and the absence of a diagnostic fossil record. To overcome these challenges, we use a temporal constraint: a horizontal gene transfer event from within archaeal methanogens to the ancestor of Cyanobacteria, one of the few microbial clades with recognized crown-group fossils. Results of molecular clock analyses calibrated by this horizontal-gene-transfer-propagated constraint show methanogens diverging within Euryarchaeota no later than 3.51 billion years ago, with methanogenesis itself probably evolving earlier. This timing provides independent support for scenarios wherein microbial methane production was important in maintaining temperatures on the early Earth.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The Archean lower atmosphere is unlikely to have been H2-rich given the antiquity of methanogens.
“The Archean lower atmosphere is unlikely to have been H2-rich given the antiquity of methanogens (23, 51, 197), some of which convert H2 into methane through a net reaction”
From The Archean atmosphere (2020) · cites this paper as [23]
The Discussion (page unavailable) estimates that methanogens emerged by the early Archaean, supporting their antiquity. The paper does not assess whether the Archaean lower atmosphere was H2-rich or conclude that methanogens made it unlikely to be H2-rich. (LLM, conf=0.86)
Experimental — accuracy not yet measuredAn origin of life during ~4.3 to 4.0 Ga ago is consistent with phylogenetic inferences.
“An origin of life during the period ~4.3 to 4.0 Ga ago is consistent with phylogenetic inferences [e.g., (23)].”
From The Archean atmosphere (2020) · cites this paper as [23]
The Discussion (page unavailable) estimates the Euryarchaeota ancestor at 4.17 Ga ± 228 Myr and methanogens at 3.94 Ga ± 228 Myr, broadly consistent with life existing around the proposed period. These are dates for particular microbial lineages, however, not a phylogenetic estimate of when life originated. (LLM, conf=0.82)
Experimental — accuracy not yet measuredSome methanogens convert H2 into methane.
“The Archean lower atmosphere is unlikely to have been H2-rich given the antiquity of methanogens (23, 51, 197), some of which convert H2 into methane through a net reaction”
From The Archean atmosphere (2020) · cites this paper as [23]
The Introduction describes methanogens as methane-producing microbes, and the Discussion dates their emergence to the early Archaean. Neither passage says that some methanogens use H2 to produce methane, so the specific conversion attributed to this source is unsupported. (LLM, conf=0.82)
Experimental — accuracy not yet measuredPhylogenetically, methanogens date back to >3.5 Ga ago.
“Phylogenetically, methanogens date back to >3.5 Ga ago (23).”
From The Archean atmosphere (2020) · cites this paper as [23]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · see citing works
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
Stamatakis, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu033 · Cited by 32,291 · see citing works
Relaxed Phylogenetics and Dating with Confidence
Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040088 · Cited by 6,463 · see citing works
A new view of the tree of life
Hug, L. A., Baker, B. J., Anantharaman, K., Brown, C. T., Probst, A. J., Castelle, C. J., Butterfield, C. N., Hernsdorf, A. W., Amano, Y., Ise, K., et al. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.48 · Cited by 2,039 · see citing works
Oceanic Methane Biogeochemistry
Reeburgh, W. S. (2007) · Chemical Reviews · doi:10.1021/cr050362v · Cited by 1,588 · see citing works
Yang, Z., & Rannala, B. H. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj024 · Cited by 916 · see citing works
Lartillot, N., Rodrigue, N., Stubbs, D., & Richer, J. (2013) · Systematic Biology · doi:10.1093/sysbio/syt022 · Cited by 871 · see citing works
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics
Evans, P. N., Parks, D. H., Chadwick, G. L., Robbins, S. J., Orphan, V. J., Golding, S. D., & Tyson, G. W. (2015) · Science · doi:10.1126/science.aac7745 · Cited by 785 · see citing works
Best Practices for Justifying Fossil Calibrations
Parham, J. F., Donoghue, P. C. J., Bell, C. J., Calway, T. D., Head, J. J., Holroyd, P. A., Inoue, J. G., Irmis, R. B., Joyce, W. G., Ksepka, D. T., et al. (2012) · Systematic Biology · doi:10.1093/sysbio/syr107 · Cited by 780 · see citing works
GUIDANCE: a web server for assessing alignment confidence scores
Penn, O., Privman, E., Ashkenazy, H., Landan, G., Graur, D., & Pupko, T. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq443 · Cited by 626 · see citing works
Reassessing the first appearance of eukaryotes and cyanobacteria
Rasmussen, B., Fletcher, I. R., Brocks, J. J., & Kilburn, M. R. (2008) · Nature · doi:10.1038/nature07381 · Cited by 612 · see citing works
Battistuzzi, F. U., Feijao, A., & Hedges, S. B. (2004) · BMC Evolutionary Biology · doi:10.1186/1471-2148-4-44 · Cited by 581 · 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
Hadean age for a post-magma-ocean zircon confirmed by atom-probe tomography
Valley, J. W., Cavosie, A. J., Ushikubo, T., Reinhard, D. A., Lawrence, D. F., Larson, D. J., Clifton, P. H., Kelly, T. F., Wilde, S. A., Moser, D. E., et al. (2014) · Nature Geoscience · doi:10.1038/ngeo2075 · Cited by 549 · see citing works
FASconCAT: Convenient handling of data matrices
Kück, P., & Meusemann, K. (2010) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2010.04.024 · Cited by 539 · see citing works
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
Vanwonterghem, I., Evans, P. N., Parks, D. H., Jensen, P. D., Woodcroft, B. J., Hugenholtz, P., & Tyson, G. W. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.170 · Cited by 537 · see citing works
Tomitani, A., Knoll, A. H., Cavanaugh, C. M., & Ohno, T. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600999103 · Cited by 468 · see citing works
Rapid evolutionary innovation during an Archaean genetic expansion
David, L., & Alm, E. (2011) · Nature · doi:10.1038/nature09649 · Cited by 429 · see citing works
Sauquet, H., Ho, S. Y. W., Gandolfo, M. A., Jordan, G. J., Wilf, P., Cantrill, D. J., Bayly, M. J., Bromham, L. D., Brown, G. K., Carpenter, R. J., et al. (2011) · Systematic Biology · doi:10.1093/sysbio/syr116 · Cited by 425 · see citing works
Carbon isotope fractionation during microbial methane oxidation
Barker, J. F., & Fritz, P. (1981) · Nature · doi:10.1038/293289a0 · Cited by 405 · see citing works
Melby, T. E., Ciampaglio, C. N., Briscoe, G., & Erickson, H. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.6.1595 · Cited by 384 · see citing works
Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago
Luo, G., Ono, S., Beukes, N. J., Wang, D. T., Xie, S., & Summons, R. E. (2016) · Science Advances · doi:10.1126/sciadv.1600134 · Cited by 371 · see citing works
Schirrmeister, B. E., de Vos, J. M., Antonelli, A., & Bagheri, H. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209927110 · Cited by 357 · see citing works
A Revised, Hazy Methane Greenhouse for the Archean Earth
Haqq-Misra, J. D., Domagal-Goldman, S. D., Kasting, P. J., & Kasting, J. F. (2008) · Astrobiology · doi:10.1089/ast.2007.0197 · Cited by 357 · see citing works
A Major Clade of Prokaryotes with Ancient Adaptations to Life on Land
Battistuzzi, F. U., & Hedges, S. B. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn247 · Cited by 350 · see citing works
Empirical profile mixture models for phylogenetic reconstruction
Le, S. Q., Gascuel, O., & Lartillot, N. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn445 · Cited by 350 · see citing works
Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils
Schirrmeister, B. E., Gugger, M., & Donoghue, P. C. J. (2015) · Palaeontology · doi:10.1111/pala.12178 · Cited by 304 · see citing works
Tan, G., Muffato, M., Ledergerber, C., Herrero, J., Goldman, N., Gil, M., & Dessimoz, C. (2015) · Systematic Biology · doi:10.1093/sysbio/syv033 · Cited by 245 · see citing works
Exploring uncertainty in the calibration of the molecular clock
Warnock, R. C. M., Yang, Z., & Donoghue, P. C. J. (2012) · Biology Letters · doi:10.1098/rsbl.2011.0710 · Cited by 238 · see citing works
Modeling Protein Evolution with Several Amino Acid Replacement Matrices Depending on Site Rates
Le, S. Q., Dang, C. C., & Gascuel, O. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss112 · Cited by 226 · see citing works
Cunha, V. D., Gaïa, M., Gadelle, D., Nasir, A., & Forterre, P. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006810 · Cited by 212 · see citing works
Consequences of Secondary Calibrations on Divergence Time Estimates
Schenk, J. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148228 · Cited by 201 · see citing works
Szöllősi, G. J., Boussau, B., Abby, S. S., Tannier, É., & Daubin, V. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202997109 · Cited by 194 · see citing works
Building the Biomarker Tree of Life
Brocks, J. J. (2005) · Reviews in Mineralogy and Geochemistry · doi:10.2138/rmg.2005.59.10 · Cited by 180 · see citing works
Crown group Oxyphotobacteria postdate the rise of oxygen
Shih, P. M., Hemp, J., Ward, L. M., Matzke, N. J., & Fischer, W. W. (2016) · Geobiology · doi:10.1111/gbi.12200 · Cited by 173 · see citing works
Methanogenic burst in the end-Permian carbon cycle
Rothman, D. H., Fournier, G. P., French, K. L., Alm, E. J., Boyle, E. A., Cao, C., & Summons, R. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318106111 · Cited by 169 · see citing works
Self-citationCyanobacterial evolution during the Precambrian
Schirrmeister, B. E., Sánchez‐Baracaldo, P., & Wacey, D. (2016) · International Journal of Astrobiology · doi:10.1017/s1473550415000579 · Cited by 158 · see citing works
The impact of calibration and clock-model choice on molecular estimates of divergence times
Duchêne, S., Lanfear, R., & Ho, S. Y. W. (2014) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2014.05.032 · Cited by 156 · see citing works
Shih, P. M., & Matzke, N. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305813110 · Cited by 151 · see citing works
The Evolution of SMC Proteins: Phylogenetic Analysis and Structural Implications
Cobbe, N., & Heck, M. M. S. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh023 · Cited by 146 · see citing works
Microfossils from the Middle Proterozoic Dismal Lakes Groups, Arctic Canada
Horodyski, R. J., & Donaldson, J. A. (1980) · Precambrian Research · doi:10.1016/0301-9268(80)90043-1 · Cited by 137 · see citing works
Suda, K., Ueno, Y., Yoshizaki, M., Nakamura, H., Kurokawa, K., Nishiyama, E., Yoshino, K., Hongoh, Y., Kawachi, K., Omori, S., et al. (2013) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2013.11.001 · Cited by 135 · see citing works
Holler, T., Wegener, G., Knittel, K., Boëtius, A., Brunner, B., Kuypers, M. M. M., & Widdel, F. (2009) · Environmental Microbiology Reports · doi:10.1111/j.1758-2229.2009.00074.x · Cited by 124 · see citing works
Lateral Gene Transfer from the Dead
Szöllősi, G. J., Tannier, É., Lartillot, N., & Daubin, V. (2013) · Systematic Biology · doi:10.1093/sysbio/syt003 · Cited by 124 · see citing works
Proterozoic photosynthesis – a critical review
Butterfield, N. J. F. (2015) · Palaeontology · doi:10.1111/pala.12211 · Cited by 116 · see citing works
Estimated Minimal Divergence Times of the Major Bacterial and Archaeal Phyla
Sheridan, P. P., Freeman, K. H., & Brenchley, J. E. (2003) · Geomicrobiology Journal · doi:10.1080/01490450303891 · Cited by 110 · see citing works
Microbial fixation of methane carbon at 2.7 Ga: was an anaerobic mechanism possible?
Hinrichs, K. (2002) · Geochemistry Geophysics Geosystems · doi:10.1029/2001gc000286 · Cited by 106 · see citing works
Microfossils in 2000 Ma old cherty stromatolites of the Franceville Group, Gabon
Amard, B., & Bertrand-Sarfati, J. (1997) · Precambrian Research · doi:10.1016/s0301-9268(96)00035-6 · Cited by 101 · see citing works
The Timetree of Prokaryotes: New Insights into Their Evolution and Speciation
Marin, J., Battistuzzi, F. U., Brown, A. C., & Hedges, S. B. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw245 · Cited by 101 · see citing works
Do missing data influence the accuracy of divergence-time estimation with BEAST?
Zheng, Y., & Wiens, J. J. (2015) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2015.02.002 · Cited by 82 · see citing works
Gao, B., & Gupta, R. S. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-86 · Cited by 80 · see citing works
Uyeda, J. C., Harmon, L. J., & Blank, C. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162539 · Cited by 69 · see citing works
Not so old Archaea – the antiquity of biogeochemical processes in the archaeal domain of life
Blank, C. E. (2009) · Geobiology · doi:10.1111/j.1472-4669.2009.00219.x · Cited by 52 · see citing works
The Presence of a Haloarchaeal Type Tyrosyl-tRNA Synthetase Marks the Opisthokonts as Monophyletic
Huang, J., Xu, Y. C., & Gogarten, J. P. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi221 · Cited by 46 · see citing works
Petitjean, C., Moreira, D., López‐García, P., & Brochier‐Armanet, C. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-226 · Cited by 45 · see citing works
RelTime Rates Collapse to a Strict Clock When Estimating the Timeline of Animal Diversification
Lozano-Fernández, J., dos Reis, M., Donoghue, P. C. J., & Pisani, D. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx079 · Cited by 32 · see citing works
Phylogenomic Dating—The Relative Antiquity of Archaeal Metabolic and Physiological Traits
Blank, C. E. (2009) · Astrobiology · doi:10.1089/ast.2008.0248 · Cited by 31 · see citing works
Horizontal 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
Arbor: Comparative Analysis Workflows for the Tree of Life
Harmon, L. J., Baumes, J., Hughes, C. E., Soberón, J. M., Specht, C. D., Turner, W., Lisle, C. R., & THACKER, R. W. (2013) · PLoS Currents · doi:10.1371/currents.tol.099161de5eabdee073fd3d21a44518dc · Cited by 23 · see citing works
Toussaint, E. F. A., & Condamine, F. L. (2015) · Biological Journal of the Linnean Society · doi:10.1111/bij.12710 · Cited by 19 · see citing works
The routes of emergence of life from LUCA during the RNA and viral world
Jheeta, S. (2015) · International Journal of Astrobiology · doi:10.1017/s1473550415000361 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Paul, S., Bag, S. K., Das, S., Harvill, E. T. & Dutta, C. Molecular signature of hypersaline adaptation: insights from genome and proteome composition of halophilic prokaryotes. Genome Biol 9, R70 (2008).
Cited by
Sorted by citations
An evolving view of methane metabolism in the Archaea
Evans, P. N., Boyd, J. A., Leu, A. O., Woodcroft, B. J., Parks, D. H., Hugenholtz, P., & Tyson, G. W. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0136-7 · Cited by 614 · see citing works
Catling, D. C., & Zahnle, K. J. (2020) · Science Advances · doi:10.1126/sciadv.aax1420 · Cited by 568 · see citing works
“Hydrogen abundance The Archean lower atmosphere is unlikely to have been H2-rich given the antiquity of methanogens (23, 51, 197), some of which convert H2 into methane through a net reaction”
BackgroundLyu, Z., Shao, N., Akinyemi, T. S., & Whitman, W. B. (2018) · Current Biology · doi:10.1016/j.cub.2018.05.021 · Cited by 530 · 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
Exoplanet Biosignatures: A Framework for Their Assessment
Catling, D. C., Krissansen-Totton, J., Kiang, N. Y., Crisp, D., Robinson, T. D., DasSarma, S., Rushby, A. J., Del Genio, A., Bains, W., & Domagal-Goldman, S. (2018) · Astrobiology · doi:10.1089/ast.2017.1737 · Cited by 225 · see citing works
The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages
Fournier, G. P., Moore, K. R., Rangel, L. T., Payette, J. G., Momper, L., & Bosak, T. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0675 · Cited by 156 · see citing works
Self-citationKrissansen-Totton, J., Garland, R., Irwin, P., & Catling, D. C. (2018) · The Astronomical Journal · doi:10.3847/1538-3881/aad564 · Cited by 145 · see citing works
Phylogenomics suggests oxygen availability as a driving force in Thaumarchaeota evolution
Ren, M., Feng, X., Huang, Y., Wang, H., Hu, Z., Clingenpeel, S. R., Swan, B. K., Fonseca, M. M., Posada, D., Stepanauskas, R., et al. (2019) · The ISME Journal · doi:10.1038/s41396-019-0418-8 · Cited by 134 · see citing works
Co‐evolution of early Earth environments and microbial life
Lyons, T. W., Tino, C., Fournier, G. P., Anderson, R. E., Leavitt, W. D., Konhauser, K. O., & Stüeken, E. E. (2024) · Nature Reviews Microbiology · doi:10.1038/s41579-024-01044-y · Cited by 133 · see citing works
Self-citationDiversity and Evolution of Methane-Related Pathways in Archaea
Garcia, P. S., Gribaldo, S., & Borrel, G. (2022) · Annual Review of Microbiology · doi:10.1146/annurev-micro-041020-024935 · Cited by 113 · 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
The biogeochemistry of ferruginous lakes and past ferruginous oceans
Swanner, E. D., Lambrecht, N., Wittkop, C. A., Harding, C., Katsev, S., Torgeson, J. M., & Poulton, S. W. (2020) · Earth-Science Reviews · doi:10.1016/j.earscirev.2020.103430 · Cited by 99 · see citing works
Hou, J., Wang, Y., Zhu, P., Yang, N., Liang, L., Yu, T., Niu, M., Konhauser, K. O., Woodcroft, B. J., & Wang, F. (2023) · Science Advances · doi:10.1126/sciadv.adf5069 · Cited by 98 · see citing works
The case and context for atmospheric methane as an exoplanet biosignature
Thompson, M., Krissansen‐Totton, J., Wogan, N. F., Telus, M., & Fortney, J. J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2117933119 · Cited by 98 · see citing works
Dating phototrophic microbial lineages with reticulate gene histories
Magnabosco, C., Moore, K. R., Wolfe, J. M., & Fournier, G. P. (2018) · Geobiology · doi:10.1111/gbi.12273 · Cited by 83 · see citing works
Self-citationP-type ATPases: Many more enigmas left to solve
Palmgren, M. B. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105352 · Cited by 90 · 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
Gene transfers can date the tree of life
Davín, A., Tannier, É., Williams, T. A., Boussau, B., Daubin, V., & Szöllősi, G. J. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0525-3 · Cited by 80 · see citing works
Wang, Y., Wegener, G., Williams, T. A., Xie, R., Hou, J., Tian, C., Zhang, Y., Wang, F., & Xiao, X. (2021) · Science Advances · doi:10.1126/sciadv.abj1453 · Cited by 76 · see citing works
Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in Rhizobiales
Wang, S., Meade, A., Lam, H., & Luo, H. (2020) · mSystems · doi:10.1128/msystems.00438-20 · Cited by 74 · see citing works
How low can they go? Aerobic respiration by microorganisms under apparent anoxia
Berg, J. S., Ahmerkamp, S., Pjevac, P., Hausmann, B., Milucka, J., & Kuypers, M. M. M. (2022) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuac006 · Cited by 71 · see citing works
Horizontal Gene Transfer in Archaea—From Mechanisms to Genome Evolution
Gophna, U., & Altman‐Price, N. (2022) · Annual Review of Microbiology · doi:10.1146/annurev-micro-040820-124627 · Cited by 69 · see citing works
Cavalier‐Smith, T., & Chao, E. E. Y. (2020) · PROTOPLASMA · doi:10.1007/s00709-019-01442-7 · Cited by 68 · see citing works
Dating Alphaproteobacteria evolution with eukaryotic fossils
Wang, S., & Luo, H. (2021) · Nature Communications · doi:10.1038/s41467-021-23645-4 · Cited by 63 · see citing works
A geological timescale for bacterial evolution and oxygen adaptation.
Davín, A. A., Woodcroft, B., Soo, R. M., Morel, B., Murali, R., Schrempf, D., Clark, J. W., Álvarez-Carretero, S., Boussau, B., Moody, E. R., et al. (2025) · Science · doi:10.1126/science.adp1853 · Cited by 62 · see citing works
Large Interferometer For Exoplanets (LIFE)
Alei, E., Konrad, B. S., Angerhausen, D., Grenfell, J. L., Mollière, P., Quanz, S. P., Rugheimer, S., & Wunderlich, F. (2022) · Astronomy and Astrophysics · doi:10.1051/0004-6361/202243760 · Cited by 61 · see citing works
Comparative genomic analysis reveals metabolic flexibility of Woesearchaeota
Huang, W.-C., Liu, Y., Zhang, X., Zhang, C., Zou, D., Zheng, S., Xu, W., Luo, Z.-H., Liu, F., & Li, M. (2021) · Nature Communications · doi:10.1038/s41467-021-25565-9 · Cited by 59 · see citing works
Histone variants in archaea and the evolution of combinatorial chromatin complexity
Stevens, K. M., Swadling, J. B., Hocher, A., Bang, C., Gribaldo, S., Schmitz, R. A., & Warnecke, T. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2007056117 · Cited by 59 · see citing works
Berkemer, S. J., & McGlynn, S. E. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa089 · Cited by 52 · see citing works
Wang, Y., Wegener, G., Williams, T. A., Xie, R., Hou, J., Wang, F., & Xiao, X. (2021) · Science Advances · doi:10.1126/sciadv.abd7180 · Cited by 50 · see citing works
RetractedA consensus view of the proteome of the last universal common ancestor
Crapitto, A. J., Campbell, A. E., Harris, A., & Goldman, A. D. (2022) · Ecology and Evolution · doi:10.1002/ece3.8930 · 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
Methane formation driven by light and heat prior to the origin of life and beyond
Ernst, L., Barayeu, U., Hädeler, J., Dick, T. P., Klatt, J. M., Keppler, F., & Rebelein, J. G. (2023) · Nature Communications · doi:10.1038/s41467-023-39917-0 · Cited by 47 · see citing works
The evolution and spread of sulfur cycling enzymes reflect the redox state of the early Earth
Mateos, K., Chappell, G., Klos, A., Le, B., Boden, J., Stüeken, E., & Anderson, R. (2023) · Science Advances · doi:10.1126/sciadv.ade4847 · Cited by 43 · see citing works
Ngugi, D. K., Salcher, M. M., Andrei, A., Ghai, R., Klotz, F., Chiriac, M., Ionescu, D., Büsing, P., Grossart, H., Xing, P., et al. (2023) · Science Advances · doi:10.1126/sciadv.adc9392 · Cited by 36 · see citing works
Johnson, C., England, A. M., Munro-Ehrlich, M., Colman, D., DuBois, J., & Boyd, E. (2021) · Journal of Bacteriology · doi:10.1128/jb.00117-21 · Cited by 30 · see citing works
Krissansen‐Totton, J., Thompson, M., Galloway, M. L., & Fortney, J. J. (2022) · Nature Astronomy · doi:10.1038/s41550-021-01579-7 · Cited by 37 · see citing works
On the evolution of coenzyme biosynthesis
Kirschning, A. (2022) · Natural Product Reports · doi:10.1039/d2np00037g · Cited by 37 · see citing works
Wogan, N. F., & Catling, D. C. (2020) · The Astrophysical Journal · doi:10.3847/1538-4357/ab7b81 · Cited by 36 · see citing works
The deep history of Earth's biomass
McMahon, S., & Parnell, J. (2018) · Journal of the Geological Society · doi:10.1144/jgs2018-061 · Cited by 35 · see citing works
Zombi: a phylogenetic simulator of trees, genomes and sequences that accounts for dead linages
Davín, A., Tricou, T., Tannier, É., de Vienne, D. M., & Szöllősi, G. J. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz710 · Cited by 35 · see citing works
Microbial Diversity and Biosignatures: An Icy Moons Perspective
Jebbar, M., Hickman‐Lewis, K., Cavalazzi, B., Taubner, R.-S., Rittmann, S. K. ‐. R., & Antunes, A. (2020) · Space Science Reviews · doi:10.1007/s11214-019-0620-z · Cited by 35 · see citing works
Sholes, S., Krissansen‐Totton, J., & Catling, D. C. (2019) · Astrobiology · doi:10.1089/ast.2018.1835 · Cited by 36 · see citing works
Biogeochemical and physical controls on methane fluxes from two ferruginous meromictic lakes
Lambrecht, N., Katsev, S., Wittkop, C. A., Hall, S. J., Sheik, C. S., Picard, A., Fakhraee, M., & Swanner, E. D. (2019) · Geobiology · doi:10.1111/gbi.12365 · Cited by 34 · see citing works
Reductive biomining of pyrite by methanogens
Spietz, R. L., Payne, D., Szilagyi, R. K., & Boyd, E. S. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2022.05.005 · Cited by 33 · see citing works
Impact of the Dimethyl Sulfoxide Reductase Superfamily on the Evolution of Biogeochemical Cycles
Wells, M., Kim, M., Akob, D. M., Basu, P., & Stolz, J. F. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.04145-22 · Cited by 32 · see citing works
The Feasibility of Detecting Biosignatures in the TRAPPIST-1 Planetary System with JWST
Meadows, V., Lincowski, A., & Lustig‐Yaeger, J. (2023) · The Planetary Science Journal · doi:10.3847/psj/acf488 · Cited by 30 · see citing works
Quantifying the Error of Secondary vs. Distant Primary Calibrations in a Simulated Environment
Powell, C. L. E., Waskin, S., & Battistuzzi, F. U. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00252 · Cited by 29 · see citing works
Zinke, L., Evans, P. N., Santos‐Medellín, C., Schroeder, A. L., Parks, D. H., Varner, R. K., Rich, V. I., Tyson, G. W., & Emerson, J. (2020) · Environmental Microbiology · doi:10.1111/1462-2920.15316 · Cited by 29 · see citing works
Electron transport chains as a window into the earliest stages of evolution
Goldman, A. D., Weber, J. M., LaRowe, D. E., & Barge, L. M. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2210924120 · Cited by 30 · see citing works
Thermochronologic perspectives on the deep-time evolution of the deep biosphere
Drake, H., & Reiners, P. W. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2109609118 · Cited by 30 · see citing works
Methanogenesis on Early Stages of Life: Ancient but Not Primordial
Muñoz‐Velasco, I., García‐Ferris, C., Hernández-Morales, R., Lazcano, A., Peretó, J. G., & Becerra, A. (2018) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-018-9570-9 · Cited by 27 · see citing works
Payne, D., Shepard, E. M., Spietz, R. L., Steward, K. F., Brumfield, S., Young, M., Bothner, B. B., Broderick, W. E., Broderick, J. B., & Boyd, E. S. (2021) · Journal of Bacteriology · doi:10.1128/jb.00146-21 · Cited by 27 · see citing works
Expression of divergent methyl/alkyl coenzyme M reductases from uncultured archaea
Shao, N., Yu, F., Chou, C.-W., Yavari, S., Williams, R. V., Amster, I. J., Brown, S. M., Drake, I. J., Duin, E. C., Whitman, W. B., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-04057-6 · Cited by 26 · see citing works
Reconstructing Early Microbial Life
Kaçar, B. (2024) · Annual Review of Microbiology · doi:10.1146/annurev-micro-041522-103400 · Cited by 25 · see citing works
Reduced Late Bombardment on Rocky Exoplanets around M Dwarfs
Lichtenberg, T., & Clement, M. S. (2022) · The Astrophysical Journal Letters · doi:10.3847/2041-8213/ac9521 · Cited by 23 · see citing works
Dating Microbial Evolution with MCMCtree
dos Reis, M. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2691-7_1 · Cited by 20 · see citing works
Histone variants in archaea – An undiscovered country
Stevens, K. M., & Warnecke, T. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.02.016 · Cited by 21 · see citing works
Lynes, M. M., Jay, Z. J., Kohtz, A. J., & Hatzenpichler, R. (2024) · The ISME Journal · doi:10.1093/ismejo/wrae026 · Cited by 20 · 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
Prondzinsky, P., Toyoda, S., & McGlynn, S. E. (2022) · DNA Research · doi:10.1093/dnares/dsac048 · Cited by 19 · see citing works
Perspective: Microbial hydrogen metabolism in rock-hosted ecosystems
Boyd, E. S., Colman, D. R., & Templeton, A. S. (2024) · Frontiers in Energy Research · doi:10.3389/fenrg.2024.1340410 · Cited by 18 · see citing works
Microbial ecology of serpentinite-hosted ecosystems
Colman, D. R., Templeton, A. S., Spear, J. R., & Boyd, E. S. (2025) · The ISME Journal · doi:10.1093/ismejo/wraf029 · Cited by 21 · see citing works
Inaccurate fossil placement does not compromise tip‐dated divergence times
Koch, N. M., Garwood, R. J., & Parry, L. A. (2023) · Palaeontology · doi:10.1111/pala.12680 · Cited by 18 · see citing works
Respiratory Heme A-Containing Oxidases Originated in the Ancestors of Iron-Oxidizing Bacteria
Esposti, M. D., Garcia-Meza, V., Gómez, A. E. C., Moya-Beltrán, A., Quatrini, R., & Hederstedt, L. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.664216 · Cited by 18 · see citing works
The late Archaean to early Proterozoic origin and evolution of anaerobic methane‐oxidizing archaea
Wang, Y., Xie, R., Hou, J., Lv, Z., Li, L., Hu, Y., Huang, H., & Wang, F. (2022) · mLife · doi:10.1002/mlf2.12013 · Cited by 15 · see citing works
Paleozoic diversification of terrestrial chitin-degrading bacterial lineages
Gruen, D. S., Wolfe, J. M., & Fournier, G. P. (2019) · BMC Evolutionary Biology · doi:10.1186/s12862-019-1357-8 · Cited by 17 · see citing works
Self-citationConstraints on hydrogen levels in the Archean atmosphere based on detrital magnetite
Kadoya, S., & Catling, D. C. (2019) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2019.07.041 · Cited by 16 · see citing works
Resolving the History of Life on Earth by Seeking Life As We Know It on Mars
Carr, C. E. (2022) · Astrobiology · doi:10.1089/ast.2021.0043 · Cited by 16 · see citing works
Robinson, T. D. (2005) · University of Arizona Press eBooks · doi:10.2458/azu_uapress_9780816540068-ch015 · Cited by 20 · see citing works
Deep Conservation of Histone Variants in Thermococcales Archaea
Stevens, K. M., Hocher, A., & Warnecke, T. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evab274 · Cited by 13 · see citing works
Very early evolution from the perspective of microbial ecology
Goldman, A. D., & Kaçar, B. (2022) · Environmental Microbiology · doi:10.1111/1462-2920.16144 · Cited by 13 · see citing works
Sumner, D. Y. (2024) · Applied and Environmental Microbiology · doi:10.1128/aem.00093-24 · Cited by 11 · see citing works
A New View of the Last Universal Common Ancestor
Goldman, A. D., & Becerra, A. (2024) · Journal of Molecular Evolution · doi:10.1007/s00239-024-10193-w · Cited by 13 · 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
Payne, D., Keller, L. M., Larson, J. D., Bothner, B. B., Colman, D. R., & Boyd, E. S. (2024) · Communications Biology · doi:10.1038/s42003-024-07049-w · Cited by 10 · see citing works
Molecular clocks provide little information to date methanogenic Archaea
Roger, A. J., & Susko, E. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0687-z · Cited by 10 · see citing works
A naturalist perspective of microbiology: Examples from methanogenic archaea
Boyd, E. S., Spietz, R. L., Kour, M., & Colman, D. R. (2022) · Environmental Microbiology · doi:10.1111/1462-2920.16285 · Cited by 7 · see citing works
Fan, L., Xu, B., Chen, S., Liu, Y., Li, F., Xie, W., Prabhu, A., Zou, D., Wan, R., Li, H., et al. (2024) · PNAS Nexus · doi:10.1093/pnasnexus/pgae057 · Cited by 10 · see citing works
The emergence of metabolisms through Earth history and implications for biospheric evolution
Moody, E. R. R., Williams, T. A., Álvarez-Carretero, S., Szöllősi, G. J., Pisani, D., Lenton, T. M., & Donoghue, P. C. J. (2025) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2024.0097 · Cited by 12 · see citing works
Gülay, A., Fournier, G. P., Smets, B. F., & Girguis, P. R. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad161 · Cited by 8 · see citing works
Self-citationBentley, J. N., Ventura, G. T., Dalzell, C. J., Walters, C. C., Peters, C. A., Mennito, A. S., Nelson, R. K., Reddy, C. M., Seewald, J. S., & Sievert, S. M. (2021) · Organic Geochemistry · doi:10.1016/j.orggeochem.2021.104302 · Cited by 7 · see citing works
New approaches for archaeal genome-guided cultivation
Wang, Y., Kamagata, Y., Li, M., Han, F., Wang, F., & Xiao, X. (2021) · Science China Earth Sciences · doi:10.1007/s11430-020-9793-5 · Cited by 7 · see citing works
An Ancient Respiratory System in the Widespread Sedimentary Archaea Thermoprofundales
Zhang, X., Huang, Y., Liu, Y., Xu, W., Pan, J., Zheng, X., Du, H., Zhang, C., Lu, Z., Zou, D., et al. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac213 · Cited by 7 · see citing works
Relative time constraints improve molecular datingPreprint
Szöllősi, G. J., Höhna, S., Williams, T. A., Schrempf, D., Daubin, V., & Boussau, B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.17.343889 · Cited by 7 · see citing works
Comparative genomics reveals the adaptation of ammonia‐oxidising Thaumarchaeota to arid soils
Li, C., Liao, H., Xu, L., Wang, C., Yao, M., Wang, J., & Li, X. (2024) · Environmental Microbiology · doi:10.1111/1462-2920.16601 · Cited by 6 · see citing works
dos Reis, M. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0532-4 · Cited by 6 · see citing works
Reply to ‘Molecular clocks provide little information to date methanogenic Archaea’
Wolfe, J. M., & Fournier, G. P. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0685-1 · Cited by 6 · see citing works
Self-citationExo-Geoscience Perspectives Beyond Habitability
Spohn, T., Roberge, A., Way, M. J., Duarte, J. C., Miozzi, F., Baumeister, P., Byrne, P. K., & Lineweaver, C. H. (2026) · Space Science Reviews · doi:10.1007/s11214-026-01265-y · Cited by 5 · see citing works
Chemistry of Coenzyme F420 in Environment
Chauhan, S. M. S. (2024) · Journal of Molecular Chemistry. · doi:10.62110/sciencein.jmc.2024.696 · Cited by 5 · see citing works
Runge, E., Vulpius, S., Herwartz, D., Pack, A., Brachmann, C., & Noack, L. (2025) · Geo-Bio Interfaces · doi:10.1180/gbi.2025.10003 · Cited by 5 · see citing works
Sokolskyi, T., & DasSarma, S. (2023) · International Journal of Astrobiology · doi:10.1017/s1473550423000095 · Cited by 5 · see citing works
Pan, J., Zhang, X., Xu, W., Liu, Y., Liu, L., Luo, Z.-H., & Li, M. (2023) · mSystems · doi:10.1128/msystems.00305-23 · Cited by 5 · see citing works
An estimate of the deepest branches of the tree of life from ancient vertically-evolving genesPreprint
Moody, E. R. R., Mahendrarajah, T., Dombrowski, N., Clark, J., Petitjean, C., Offre, P., Szöllősi, G. J., Spang, A., & Williams, T. A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.19.427276 · Cited by 5 · see citing works
Editorial: The methane moment - Cross-boundary significance of methanogens: Preface
Lyu, Z., Rotaru, A., Pimentel, M., Zhang, C., & Rittmann, S. K. ‐. R. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1055494 · Cited by 5 · see citing works
Archaeology and the Construction of Artifact Lineages: From Culture History to Phylogenetics
O’Brien, M. J., Vidiella, B., Duran‐Nebreda, S., Bentley, R. A., & Valverde, S. (2025) · Biological Theory · doi:10.1007/s13752-025-00491-x · Cited by 4 · see citing works
Insights into the Evolutionary and Ecological Roles of Bathyarchaeia in Arsenic Detoxification
Wang, J., Duan, C., Feng, X., Qi, Y.-L., Lian, J., Wang, L., Li, M., & Hu, B. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.5c03342 · Cited by 4 · see citing works
Niche Partitioning and Intraspecific Variation of Thaumarchaeota in Deep Ocean Sediments
Liu, R., He, X., Ren, G., Li, D., Zhao, M., Lehtovirta‐Morley, L. E., Todd, J. D., Zhang, X., & Liu, J. (2025) · Environmental Microbiology · doi:10.1111/1462-2920.70018 · Cited by 4 · see citing works
Cultivation of Methanonezhaarchaeia, the third class of methanogens within the phylum Thermoproteota
Kohtz, A. J., Nupp, S., & Hatzenpichler, R. (2025) · Science Advances · doi:10.1126/sciadv.aea0936 · Cited by 4 · see citing works
Controls of Atmospheric Methane on Early Earth and Inhabited Earth-like Terrestrial Exoplanets
Akahori, A., Watanabe, Y., & Tajika, E. (2024) · The Astrophysical Journal · doi:10.3847/1538-4357/ad47f3 · Cited by 4 · see citing works
- Authors
- Wolfe, J. M., & Fournier, G. P.
- Affiliations
- Massachusetts Institute of Technology (US)
- Corresponding author
- Wolfe, Joanna M.
- Venue
- Nature Ecology & Evolution
- Published
- 2018-04-02
- Volume
- 2
- Issue
- 5
- Pages
- 897-903
- ISSN
- 2397-334X (ISSN-L)
- OpenAlex
- W2794637696
- Cited by
- 160
- References
- 62
- Citations by year
- 2026: 18 · 2025: 22 · 2024: 18 · 2023: 16 · 2022: 28 · 2021: 18 · 2020: 12 · 2019: 10 · 2018: 16
- FWCI
- 7.55
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Ecology & Evolution (publishedVersion)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Science Foundation (1615426)
- Massachusetts Green High Performance Computing Center
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Keywords
- horizontal gene transfer, methanogenesis, methanogenic archaea, archaea, cyanobacteria, molecular clock, divergence time estimation, Euryarchaeota, molecular phylogeny
- MeSH terms
- Cyanobacteria, Biological Evolution, Methane, Phylogeny, Temperature, Evolution, Planetary, Euryarchaeota, Gene Transfer, Horizontal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review