The DOI matches its Crossref record; 59 of the 62 references it cites were found in a registry or an index.
Manganese-oxidizing photosynthesis before the rise of cyanobacteria
Open accessAbstract
The emergence of oxygen-producing (oxygenic) photosynthesis fundamentally transformed our planet; however, the processes that led to the evolution of biological water splitting have remained largely unknown. To illuminate this history, we examined the behavior of the ancient Mn cycle using newly obtained scientific drill cores through an early Paleoproterozoic succession (2.415 Ga) preserved in South Africa. These strata contain substantial Mn enrichments (up to ∼17 wt %) well before those associated with the rise of oxygen such as the ∼2.2 Ga Kalahari Mn deposit. Using microscale X-ray spectroscopic techniques coupled to optical and electron microscopy and carbon isotope ratios, we demonstrate that the Mn is hosted exclusively in carbonate mineral phases derived from reduction of Mn oxides during diagenesis of primary sediments. Additional observations of independent proxies for O2--multiple S isotopes (measured by isotope-ratio mass spectrometry and secondary ion mass spectrometry) and redox-sensitive detrital grains--reveal that the original Mn-oxide phases were not produced by reactions with O2, which points to a different high-potential oxidant. These results show that the oxidative branch of the Mn cycle predates the rise of oxygen, and provide strong support for the hypothesis that the water-oxidizing complex of photosystem II evolved from a former transitional photosystem capable of single-electron oxidation reactions of Mn.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“This interpretation of sediment manganese enrichments is robust regardless of the possibility of oxygen-free manganese oxidation-through UV photooxidation (Anbar & Holland 1992), photosynthetic oxidation ( Johnson et al. 2013), or oxidation with elemental sulfur (Daye et al. 2019)-given rapid manganese reduction under anoxic conditions (e.g., Busigny et al. 2014).”
From The History of Ocean Oxygenation (2022) · cites this paper as Johnson et al. 2013
Citations
Cites
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
Umena, Y., Kawakami, K., Shen, J., & Kamiya, N. (2011) · Nature · doi:10.1038/nature09913 · Cited by 3,920
Froelich, P. N., Klinkhammer, G. P., Bender, M. L., Luedtke, N. A., Heath, G. R., Cullen, D., Dauphin, P., Hammond, D., Hartman, B., & Maynard, V. (1979) · Geochimica et Cosmochimica Acta · doi:10.1016/0016-7037(79)90095-4 · Cited by 3,368
Architecture of the Photosynthetic Oxygen-Evolving Center
Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. P., & Iwata, S. (2004) · Science · doi:10.1126/science.1093087 · Cited by 3,330
Nitrite-driven anaerobic methane oxidation by oxygenic bacteria
Ettwig, K. F., Butler, M. K., Paslier, D. L., Pelletier, É., Mangenot, S., Kuypers, M. M. M., Schreiber, F., Dutilh, B. E., Zedelius, J., de Beer, D., et al. (2010) · Nature · doi:10.1038/nature08883 · Cited by 1,864
The Chemical Evolution of the Atmosphere and Oceans
Holland, H. D. (1984) · doi:10.1515/9780691220239 · Cited by 1,836
Atmospheric Influence of Earth's Earliest Sulfur Cycle
Farquhar, J., Bao, H., & Thiemens, M. (2000) · Science · doi:10.1126/science.289.5480.756 · Cited by 1,805
Water-Splitting Chemistry of Photosystem II
McEvoy, J. P., & Brudvig, G. W. (2006) · Chemical Reviews · doi:10.1021/cr0204294 · Cited by 1,542
Dating the rise of atmospheric oxygen
Bekker, A., Holland, H. D., Wang, P.-L., Rumble, D., Stein, H. J., Hannah, J. L., Coetzee, L. L., & Beukes, N. J. (2004) · Nature · doi:10.1038/nature02260 · Cited by 1,435 · cited 3×
“32 Ga (1, 2)—an interval supported by a broad range of geologic evidence (19, 25, 33).”
BackgroundArchean Molecular Fossils and the Early Rise of Eukaryotes
Brocks, J. J., Logan, G. A., Buick, R., & Summons, R. E. (1999) · Science · doi:10.1126/science.285.5430.1033 · Cited by 1,275
A Whiff of Oxygen Before the Great Oxidation Event?
Anbar, A. D., Duan, Y., Lyons, T. W., Arnold, G. L., Kendall, B., Creaser, R. A., Kaufman, A. J., Gordon, G. W., Scott, C., Garvin, J., et al. (2007) · Science · doi:10.1126/science.1140325 · Cited by 1,024
Klein, C. (2005) · American Mineralogist · doi:10.2138/am.2005.1871 · Cited by 969
Pavlov, A. A., & Kasting, J. F. (2002) · Astrobiology · doi:10.1089/153110702753621321 · Cited by 912
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
Kinetics of reaction between O2 and Mn(II) species in aqueous solutions
Morgan, J. J. (2004) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2004.06.013 · Cited by 568
Kopp, R. E., Kirschvink, J. L., Hilburn, I. A., & Nash, C. Z. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504878102 · Cited by 565
Self-citationMolecular Evidence for the Early Evolution of Photosynthesis
Xiong, J., Fischer, W. M., Inoue, K., Nakahara, M., & Bauer, C. E. (2000) · Science · doi:10.1126/science.289.5485.1724 · Cited by 513
Self-citationKirschvink, J. L., Gaidos, E. J., Bertani, L. E., Beukes, N. J., Gutzmer, J., Maepa, L. N., & Steinberger, R. E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.4.1400 · Cited by 456
Self-citationThe origin of atmospheric oxygen on Earth: The innovation of oxygenic photosynthesis
Dismukes, G. C., Klimov, V. V., Баранов, В. С., Kozlov, Y. N., Dasgupta, J., & Tyryshkin, A. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061514798 · Cited by 392
The origin and evolution of oxygenic photosynthesis
Blankenship, R. E., & Hartman, H. (1998) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(98)01186-4 · Cited by 382
New model for molybdenum behavior in euxinic waters
Helz, G. R., Bura-Nakić, E., Mikac, N., & Ciglenečki, I. (2011) · Chemical Geology · doi:10.1016/j.chemgeo.2011.03.012 · Cited by 358
Reconstructing Earth's surface oxidation across the Archean-Proterozoic transition
Guo, Q., Strauss, H., Kaufman, A. J., Schröder, S., Gutzmer, J., Wing, B., Baker, M. A., Bekker, A., Jin, Q., Kim, S.-T., et al. (2009) · Geology · doi:10.1130/g25423a.1 · Cited by 284
Biosynthesis of 2-methylbacteriohopanepolyols by an anoxygenic phototroph
Rashby, S. E., Sessions, A. L., Summons, R. E., & Newman, D. K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704912104 · Cited by 281
Beukes, N. J., & Gutzmer, J. (2008) · doi:10.5382/rev.15.01 · Cited by 275
A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning
Navarro-González, R., McKay, C. P., & Mvondo, D. N. (2001) · Nature · doi:10.1038/35083537 · Cited by 272
Sedimentary manganese metallogenesis in response to the evolution of the Earth system
Roy, S. (2006) · Earth-Science Reviews · doi:10.1016/j.earscirev.2006.03.004 · Cited by 246
Welander, P. V., Coleman, M. L., Sessions, A. L., Summons, R. E., & Newman, D. K. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912949107 · Cited by 242
Molybdenum isotope fractionation in pelagic euxinia: Evidence from the modern Black and Baltic Seas
Nägler, T. F., Neubert, N., Böttcher, M. E., Dellwig, O., & Schnetger, B. (2011) · Chemical Geology · doi:10.1016/j.chemgeo.2011.07.001 · Cited by 233
Geological constraints on the origin of oxygenic photosynthesis
Farquhar, J., Zerkle, A. L., & Bekker, A. (2011) · Photosynthesis Research · doi:10.1007/s11120-010-9594-0 · Cited by 223
Tamura, N., & Cheniae, G. M. (1987) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(87)90019-3 · Cited by 220
Bekker, A. (2001) · American Journal of Science · doi:10.2475/ajs.301.3.261 · Cited by 220
An iron shuttle for deepwater silica in Late Archean and early Paleoproterozoic iron formation
Fischer, W. W., & Knoll, A. H. (2006) · Geological Society of America Bulletin · doi:10.1130/b26328.1 · Cited by 196
Self-citationThe Evolution of Photosynthesis
Olson, J. M. (1970) · Science · doi:10.1126/science.168.3930.438 · Cited by 190
Allen, J. F., & Martin, W. F. (2007) · Nature · doi:10.1038/445610a · Cited by 178
Pufahl, P. K., & Hiatt, E. E. (2011) · Marine and Petroleum Geology · doi:10.1016/j.marpetgeo.2011.12.002 · Cited by 173
Okita, P. M., Maynard, J. B., Spiker, E. C., & Force, E. R. (1988) · Geochimica et Cosmochimica Acta · doi:10.1016/0016-7037(88)90036-1 · Cited by 159
Fischer, W. W., Schroeder, S., Lacassie, J. P., Beukes, N. J., Goldberg, T., Strauss, H., Horstmann, U. E., Schrag, D. P., & Knoll, A. H. (2009) · Precambrian Research · doi:10.1016/j.precamres.2008.10.010 · Cited by 139
Self-citationHofmann, A., Bekker, A., Rouxel, O. J., Rumble, D., III, & Master, S. (2009) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2009.07.008 · Cited by 127
Clement, B., Luther, G. W., & Tebo, B. M. (2009) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2008.12.023 · Cited by 124
Sauer, K., & Yachandra, V. K. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.132266199 · Cited by 122
Liang, M., Hartman, H., Kopp, R. E., Kirschvink, J. L., & Yung, Y. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608839103 · Cited by 119
Self-citationTsikos, H., Beukes, N. J., Moore, J. M., & Harris, C. (2003) · Economic Geology · doi:10.2113/gsecongeo.98.7.1449 · Cited by 108
Microaerobic steroid biosynthesis and the molecular fossil record of Archean life
Waldbauer, J., Newman, D. K., & Summons, R. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104160108 · Cited by 105
Genetic diversity of manganese deposition in the terrestrial geological record
Roy, S. (1996) · Geological Society London Special Publications · doi:10.1144/gsl.sp.1997.119.01.02 · Cited by 99
Origins of Life on the Earth and in the Cosmos
Zubay, G. (2000) · Elsevier eBooks · doi:10.1016/b978-0-12-781910-5.x5000-0 · Cited by 99
Komiya, T., Hirata, T., Kitajima, K., Yamamoto, S., Shibuya, T., Sawaki, Y., Ishikawa, T., Shu, D., Li, Y., & Han, J. (2007) · Gondwana Research · doi:10.1016/j.gr.2007.10.006 · Cited by 99
Schröder, S., Bedorf, D., Beukes, N. J., & Gutzmer, J. (2011) · Sedimentary Geology · doi:10.1016/j.sedgeo.2010.11.007 · Cited by 77
Mayhew, L. E., Webb, S. M., & Templeton, A. S. (2011) · Environmental Science & Technology · doi:10.1021/es104292n · Cited by 74
Self-citationAvailability of O 2 and H 2 O 2 on Pre-Photosynthetic Earth
Haqq-Misra, J., Kasting, J. F., & Lee, S. (2011) · Astrobiology · doi:10.1089/ast.2010.0572 · Cited by 73
Scheiderich, K., Zerkle, A. L., Helz, G. R., Farquhar, J. D., & Walker, R. J. (2010) · Chemical Geology · doi:10.1016/j.chemgeo.2010.10.015 · Cited by 66
Rhenium geochemical cycling: Insights from continental margins
Morford, J. L., Martin, W. R., & Carney, C. M. (2011) · Chemical Geology · doi:10.1016/j.chemgeo.2011.12.014 · Cited by 66
The evolution of Photosystem II: insights into the past and future
Williamson, A., Conlan, B., Hillier, W., & Wydrzynski, T. (2010) · Photosynthesis Research · doi:10.1007/s11120-010-9559-3 · Cited by 62
Manganese Ores of Supergene Zone: Geochemistry of Formation
Varentsov, I. M. (1996) · Springer eBooks · doi:10.1007/978-94-017-2174-5 · Cited by 57
Büchel, C., Barber, J., Ananyev, G., Eshaghi, S., Watt, R. K., & Dismukes, G. C. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.25.14288 · Cited by 47
The major early Proterozoic sedimentary iron and manganese deposits and their tectonic setting
Schissel, D., & Aro, P. (1992) · Economic Geology · doi:10.2113/gsecongeo.87.5.1367 · Cited by 29
Inorganic Complexes Enabled the Onset of Life and Oxygenic Photosynthesis
Russell, M. J., Allen, J. F., & Milner‐White, E. J. (2008) · Springer eBooks · doi:10.1007/978-1-4020-6709-9_259 · Cited by 23
Structure and composition of the Aleutian island arc and implications for continental crustal growth
Steven Holbrook, W., Lizarralde, D., McGeary, S., Bangs, N., & Diebold, J. (1999) · Geology · doi:10.1130/0091-7613(1999)027
Research works printed but not linked: 3
- Beukes N Klein C (1992) Models for iron-formation deposition. The Proterozoic Biosphere: A Multidisciplinary Study eds Schopf JW Klein C (Cambridge Univ Press) pp 147–156.
- T Miyano, NJ Beukes, Phase relations of stilpnomelane, ferri-annite, and riebeckite in very low-grade metamorphosed iron-formations. S Afr J Geol 87, 111–124 (1984).
- Kasting JF Holland HD Kump LR (1992) Atmospheric evolution: The rise of oxygen. The Proterozoic Biosphere: A Multidisciplinary Study eds Schopf WJ Klein C (Cambridge Univ Press Cambridge UK) pp 1185–1188.
Cited by
Sorted by citations
Mn4Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen
Yano, J., & Yachandra, V. K. (2014) · Chemical Reviews · doi:10.1021/cr4004874 · Cited by 685
Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event
Planavsky, N. J., Asael, D., Hofmann, A., Reinhard, C. T., Lalonde, S. V., Knudsen, A., Wang, X., Ossa Ossa, F., Pecoits, E., Smith, A. J. B., et al. (2014) · Nature Geoscience · doi:10.1038/ngeo2122 · Cited by 615
Timing and tempo of the great oxidation event
Gumsley, A. P., Chamberlain, K. R., Bleeker, W., Söderlund, U., de Kock, M. O., Larsson, E. R., & Bekker, A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1608824114 · Cited by 527
A critical review of mineral-microbe interaction and co-evolution: Mechanisms and applications
Dong, H., Huang, L., Zhao, L., Zeng, Q., Liu, X., Sheng, Y., Shi, L., Wu, G., Jiang, H., Li, F., et al. (2022) · National Science Review · doi:10.1093/nsr/nwac128 · Cited by 472
Evolution of Oxygenic Photosynthesis
Fischer, W. W., Hemp, J., & Johnson, J. E. (2016) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-060313-054810 · Cited by 438
Self-citation
Metadata
- Authors
- Johnson, J. E., Webb, S. M., Thomas, K., Ono, S., Kirschvink, J. L., & Fischer, W. W.
- Affiliations
- California Institute of Technology (US)
- Stanford Synchrotron Radiation Lightsource (US)
- Massachusetts Institute of Technology (US)
- Tokyo Institute of Technology (JP)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-06-24
- Volume
- 110
- Issue
- 28
- Pages
- 11238-11243
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3710856
- OpenAlex
- W2103118098
- Cited by
- 238
- References
- 62
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 24 · 2023: 22 · 2022: 19 · 2021: 20 · 2020: 21 · 2019: 25 · 2018: 16 · 2017: 17 · 2016: 15 · 2015: 13 · 2014: 19 · 2013: 5
- FWCI
- 11.79
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Science Foundation
- David and Lucile Packard Foundation
- U.S. Department of Energy
- National Aeronautics and Space Administration
- Agouron Institute
- Office of Science
- SLAC National Accelerator Laboratory
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Earth and Planetary Sciences › Geochemistry and Petrology › Geochemistry and Elemental Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Keywords
- manganese cycle, oxygen-evolving complex, Paleoproterozoic, manganese oxide, carbonate minerals, diagenesis, sulfur isotopes, carbon isotopes
- MeSH terms
- Cyanobacteria, Manganese, Oxidation-Reduction, Photosynthesis, Biomarkers
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
