The evolution and spread of sulfur cycling enzymes reflect the redox state of the early Earth
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Abstract
The biogeochemical sulfur cycle plays a central role in fueling microbial metabolisms, regulating the Earth’s redox state, and affecting climate. However, geochemical reconstructions of the ancient sulfur cycle are confounded by ambiguous isotopic signals. We use phylogenetic reconciliation to ascertain the timing of ancient sulfur cycling gene events across the tree of life. Our results suggest that metabolisms using sulfide oxidation emerged in the Archean, but those involving thiosulfate emerged only after the Great Oxidation Event. Our data reveal that observed geochemical signatures resulted not from the expansion of a single type of organism but were instead associated with genomic innovation across the biosphere. Moreover, our results provide the first indication of organic sulfur cycling from the Mid-Proterozoic onwards, with implications for climate regulation and atmospheric biosignatures. Overall, our results provide insights into how the biological sulfur cycle evolved in tandem with the redox state of the early Earth.
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The age of LUCA is sensitive to the root calibration used.
“This is consistent with previous work suggesting that the age of LUCA is sensitive to the root calibration used19,21,27,95,96.”
From ATP synthase evolution on a cross-braced dated tree of life (2023) · cites this paper as [95]
In Results (Construction of species tree and time-calibrated chronogram), LUCA age estimates differ substantially between the liberal and conservative calibration sets, and Table 1 shows that the LUCA root prior differs between those sets. However, the paper also changed several other calibration points at the same time, so it does not establish sensitivity to the root calibration alone. (LLM, conf=0.82)
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Nabhan, S., Marin‐Carbonne, J., Mason, P. R. D., & Heubeck, C. (2020) · Geobiology · doi:10.1111/gbi.12393 · Cited by 22 · see citing works
Biogeochemical cycling of sulfur, manganese and iron in ferruginous limnic analog of Archean ocean
Boyko, V., Avetisyan, K., Findlay, A., Guo, Q., Yang, X., Pellerin, A., & Kamyshny, A. (2021) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2020.12.020 · Cited by 22 · see citing works
Butterfield, N. J. F. (2000) · BioOne Complete (BioOne) · doi:10.1666/0094-8373(2000)026<0386:bpngns>2.0.co;2 · Cited by 15 · see citing works
Hoffman, P. F. (2018) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-053018-060145 · Cited by 11 · see citing works
Collins, A. G. (2000) · doi:10.1666/0094-8373(2000)026
Flagged first, then by citations
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Diversity and ecology of microbial sulfur metabolism
Zhou, Z., Tran, P. Q., Cowley, E. S., Trembath‐Reichert, E., & Anantharaman, K. (2024) · Nature Reviews Microbiology · doi:10.1038/s41579-024-01104-3 · Cited by 258 · 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-citationATP 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
“This is consistent with previous work suggesting that the age of LUCA is sensitive to the root calibration used 19,21,27,95,96 .”
BackgroundMethodResultInfluentialThe history of Earth’s sulfur cycle
Fakhraee, M., Crockford, P. W., Bauer, K. W., Pasquier, V., Sugiyama, I., Katsev, S., Raven, M. R., Gomes, M. L., Philippot, P., Crowe, S. A., et al. (2024) · Nature Reviews Earth & Environment · doi:10.1038/s43017-024-00615-0 · Cited by 69 · 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
Microbial iron oxide respiration coupled to sulfide oxidation
Chen, S., Li, X., Battisti, N., Guan, G., Montoya, M. A., Osvatic, J., Pjevac, P., Pollak, S., Richter, A. A., Schintlmeister, A., et al. (2025) · Nature · doi:10.1038/s41586-025-09467-0 · Cited by 57 · see citing works
Timing the evolution of phosphorus-cycling enzymes through geological time using phylogenomics
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Self-citationBiogenic Sulfur Gases as Biosignatures on Temperate Sub-Neptune Waterworlds
Tsai, S., Innes, H., Wogan, N. F., & Schwieterman, E. W. (2024) · The Astrophysical Journal Letters · doi:10.3847/2041-8213/ad3801 · Cited by 31 · see citing works
Williams, T., Davín, A. A., Szánthó, L. L., Stamatakis, A., Wahl, N. A., Woodcroft, B., Soo, R. M., Eme, L., Sheridan, P. O., Gubry-Rangin, C., et al. (2024) · The ISME Journal · doi:10.1093/ismejo/wrae129 · Cited by 30 · see citing works
Organic sulfur from source to sink in low‐sulfate Lake Superior
Phillips, A. A., Ulloa, I., Hyde, E., Agnich, J., Sharpnack, L., O'Malley, K. G., Webb, S. M., Schreiner, K. M., Sheik, C. S., Katsev, S., et al. (2023) · Limnology and Oceanography · doi:10.1002/lno.12454 · Cited by 22 · see citing works
Evolutionary history and origins of Dsr-mediated sulfur oxidation
Klier, K. M., Martin, C., Langwig, M. V., & Anantharaman, K. (2024) · The ISME Journal · doi:10.1093/ismejo/wrae167 · Cited by 20 · see citing works
Mansor, M., Duverger, A., Pasquier, V., Gorlas, A., Guyot, F., Berg, J. S., Marin‐Carbonne, J., Cosmidis, J., & Picard, A. (2025) · Geo-Bio Interfaces · doi:10.1180/gbi.2024.9 · Cited by 19 · see citing works
Jin, X., Wang, H., Wu, Q., Zhang, J., & Li, S. (2025) · Desalination and Water Treatment · doi:10.1016/j.dwt.2025.101100 · Cited by 12 · see citing works
Sumner, D. Y. (2024) · Applied and Environmental Microbiology · doi:10.1128/aem.00093-24 · Cited by 11 · see citing works
Patsis, A., Schuler, C. J., Toner, B. M., Santelli, C. M., & Sheik, C. S. (2025) · Nature Communications · doi:10.1038/s41467-025-59241-z · Cited by 11 · see citing works
An updated view of metabolic handoffs in microbiomes
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Boyle, R. A., Moody, E. R. R., Babcock, G., McShea, D. W., Álvarez-Carretero, S., Lenton, T. M., & Donoghue, P. C. J. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2406344122 · Cited by 9 · see citing works
Phylogeny and evolution of dissimilatory sulfite reduction in prokaryotes
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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
Moore, E. K., Diedolf, J., Morrison, S. M., & Hummer, D. R. (2024) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2024.05.024 · Cited by 7 · see citing works
DPANN Archaea and CPR Bacteria: insights into early cellular evolution?
Mahendrarajah, T., & Spang, A. (2025) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2024.0096 · Cited by 6 · see citing works
Cryptic sulfur cycling in the deep biosphere of ferruginous Lake Towuti, Indonesia
Ruiz-Blas, F., Bartholomäus, A., Henny, C., Russell, J. M., Kallmeyer, J., & Vuillemin, A. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1725877 · Cited by 4 · see citing works
Nisson, D. M., Mickol, R. L., Robinson, A., & Lloyd, K. G. (2026) · Astrobiology · doi:10.1177/15311074261464014 · Cited by 5 · see citing works
Biological use of molybdenum and tungsten stems back to 3.4 billion years ago
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Self-citationLi, K., & Pluth, M. D. (2026) · Chemical Reviews · doi:10.1021/acs.chemrev.5c00935 · Cited by 3 · see citing works
Chemosymbiotic trophic strategy in an Ediacaran tubular animal
Wang, Z., Peng, Y., Tang, Q., Schiffbauer, J. D., Xiao, S., Fike, D. A., Jia, Z., Feng, D., Crockford, P. W., Cai, Y., et al. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2526201123 · Cited by 2 · see citing works
Spangenberg, J. E., & Bosco‐Santos, A. (2024) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.9866 · Cited by 2 · see citing works
Transcriptional response to elemental sulfur in Geobacter sulfurreducens
Inoue, M., Fujita, D., Izu, Y., Aono, R., & Mihara, H. (2025) · Bioscience Biotechnology and Biochemistry · doi:10.1093/bbb/zbaf106 · Cited by 1 · see citing works
Boden, J. S., Ni, Z., Anderson, R. E., & Stüeken, E. E. (2026) · Science Advances · doi:10.1126/sciadv.aec4450 · Cited by 1 · see citing works
Self-citationTracing ancient life through the genomic record
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Bradley, A. S. (2026) · Springer geochemistry · doi:10.1007/978-3-032-07705-9_8 · Cited by 1 · see citing works
Ren, X.-Y., Lin, X., Tanabe, T. S., Loy, A., Hu, L., Zhu, Y., & Chen, S. (2026) · Nature Communications · doi:10.1038/s41467-026-75310-3 · Cited by 1 · see citing works
Timing the Evolution of Phosphorus-Cycling Enzymes Through Geological TimePreprint
Boden, J. S., Zhong, J., Anderson, R. E., & Stüeken, E. E. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.21.554175 · Cited by 1 · see citing works
Self-citationKlier, K. M., Martin, C., Langwig, M. V., & Anantharaman, K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.30.576480
Siess, J., & Nanda, V. (2025) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.70004
Correa, J. D. S., Sáyer, S.-M. G., Sepulveda, L. K. D., Cortés, J. S. A., Cuestas, C. I. C., Aristizábal, F., & Romero, I. A. G. (2025) · Cogent Food & Agriculture · doi:10.1080/23311932.2025.2548928
Sulphur metabolism as a key factor in the evolution of environmental adaptation of Acidihalobacter
Vergara, E., Khaleque, H. N., Neira, G., Watkin, E. L. J., Valdés, J. H., & Holmes, D. S. (2026) · Microbial Genomics · doi:10.1099/mgen.0.001732
Sun, J., Yang, Y., Yu, X., Zhang, X., Yang, P., Liu, B., Chen, Y., Wang, D., Peng, X., & Li, X. (2026) · Environmental Microbiology · doi:10.1111/1462-2920.70373
Impact of Chamaecrista rotundifolia cover cropping on soil elemental cycling in karst agroecosystems
Yue, Z., Sheng, S., Peng, L., Xu, W., Zhang, J., Wu, D., Liu, B., Li, Q., Dong, R., Cheng, H., et al. (2026) · Frontiers in Microbiology · doi:10.3389/fmicb.2026.1906173
Mammals produce cyclo -octasulfur to suppress lipid peroxidation and ferroptosis
Barayeu, U., Ogata, S., Takata, T., Jung, M., Matsunaga, T., Morita, M., Ida, T., Lange, M., Unno, Y., Boushehri, S., et al. (2026) · Science · doi:10.1126/science.aec5473
Aguilar, A., Perez, I. M., Nadel, O., Nayfach, S., Pestana, L. R., Segall, A. M., Rohwer, F. L., Roux, S., White, S. J., & Luque, A. (2026) · Nature Communications · doi:10.1038/s41467-026-78136-1 · Cited by 2 · see citing works
- Authors
- Mateos, K., Chappell, G., Klos, A., Le, B., Boden, J., Stüeken, E., & Anderson, R.
- Affiliations
- University of California, Santa Cruz (US)
- University of North Carolina at Chapel Hill (US)
- Carleton College (US)
- University of St Andrews (GB)
- Corresponding author
- Anderson, Rika
- Venue
- Science Advances
- Published
- 2023-07-07
- Volume
- 9
- Issue
- 27
- Pages
- eade4847-eade4847
- ISSN
- 2375-2548 (ISSN-L)
- PMC
- PMC10328410
- OpenAlex
- W4383499839
- Cited by
- 43
- References
- 97
- Citations by year
- 2026: 13 · 2025: 13 · 2024: 14 · 2023: 3
- FWCI
- 8.69
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Science Advances (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- St Andrews Research Repository (St Andrews Research Repository) (submittedVersion, cc-by)
- Funders
- National Aeronautics and Space Administration (80NSSC18K0829)
- Research Corporation for Science Advancement
- Carleton College
- Nuclear Safety and Security Commission
- Natural Environment Research Council (NE/V010824/1)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- sulfur cycling, sulfide oxidation, thiosulfate metabolism, Great Oxidation Event, Archean, phylogenetic reconciliation, genomic innovation, atmospheric biosignatures, climate regulation, sulfur isotopes
- MeSH terms
- Atmosphere, Climate, Oxidation-Reduction, Phylogeny, Sulfur
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.
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