The DOI matches its Crossref record; 62 of the 62 references it cites were found in a registry or an index.
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.
Overview
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
Verification
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 source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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.
Citations
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
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
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
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
Oceanic Methane Biogeochemistry
Reeburgh, W. S. (2007) · Chemical Reviews · doi:10.1021/cr050362v · Cited by 1,588
Yang, Z., & Rannala, B. H. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj024 · Cited by 917
Lartillot, N., Rodrigue, N., Stubbs, D., & Richer, J. (2013) · Systematic Biology · doi:10.1093/sysbio/syt022 · Cited by 871
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 804
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
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 637
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
Battistuzzi, F. U., Feijao, A., & Hedges, S. B. (2004) · BMC Evolutionary Biology · doi:10.1186/1471-2148-4-44 · Cited by 609
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
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 550
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
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
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
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 422
Rapid evolutionary innovation during an Archaean genetic expansion
David, L. A., & Alm, E. J. (2010) · Nature · doi:10.1038/nature09649 · Cited by 420
Carbon isotope fractionation during microbial methane oxidation
Barker, J. F., & Fritz, P. (1981) · Nature · doi:10.1038/293289a0 · Cited by 405
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
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 372
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
Empirical profile mixture models for phylogenetic reconstruction
Le, S. Q., Gascuel, O., & Lartillot, N. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn445 · Cited by 362
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
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 355
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
Tan, G., Muffato, M., Ledergerber, C., Herrero, J., Goldman, N., Gil, M., & Dessimoz, C. (2015) · Systematic Biology · doi:10.1093/sysbio/syv033 · Cited by 261
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
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
Cunha, V. D., Gaïa, M., Gadelle, D., Nasir, A., & Forterre, P. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006810 · Cited by 216
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 202
Consequences of Secondary Calibrations on Divergence Time Estimates
Schenk, J. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148228 · Cited by 201
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
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 174
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
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 165
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 158
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
Shih, P. M., & Matzke, N. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305813110 · Cited by 151
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
Suda, K., Ueno, Y., Yoshizaki, M., Nakamura, H., Kurokawa, K., Nishiyama, E., Yoshino, K., Hongoh, Y., Kawachi, K., Omori, S., et al. (2014) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2013.11.001 · Cited by 130
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 127
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
Proterozoic photosynthesis – a critical review
Butterfield, N. J. F. (2015) · Palaeontology · doi:10.1111/pala.12211 · Cited by 120
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 111
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
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 104
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
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
Gao, B., & Gupta, R. S. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-86 · Cited by 81
Uyeda, J. C., Harmon, L. J., & Blank, C. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162539 · Cited by 73
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
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 47
Petitjean, C., Moreira, D., López‐García, P., & Brochier‐Armanet, C. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-226 · Cited by 45
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
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
Horizontal Gene Transfer: Pitfalls and Promises
Gogarten, J. P., Murphey, R. D., & Olendzenski, L. (1999) · Biological Bulletin · doi:10.2307/1542970 · Cited by 26
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
Toussaint, E. F. A., & Condamine, F. L. (2015) · Biological Journal of the Linnean Society · doi:10.1111/bij.12710 · Cited by 19
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
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 626
Catling, D. C., & Zahnle, K. J. (2020) · Science Advances · doi:10.1126/sciadv.aax1420 · Cited by 568
“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
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
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
Metadata
- 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 › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › 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
