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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

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Abstract

Several lines of geological and geochemical evidence indicate that the level of atmospheric oxygen was extremely low before 2.45 billion years (Gyr) ago, and that it had reached considerable levels by 2.22 Gyr ago. Here we present evidence that the rise of atmospheric oxygen had occurred by 2.32 Gyr ago. We found that syngenetic pyrite is present in organic-rich shales of the 2.32-Gyr-old Rooihoogte and Timeball Hill formations, South Africa. The range of the isotopic composition of sulphur in this pyrite is large and shows no evidence of mass-independent fractionation, indicating that atmospheric oxygen was present at significant levels (that is, greater than 10(-5) times that of the present atmospheric level) during the deposition of these units. The presence of rounded pebbles of sideritic iron formation at the base of the Rooihoogte Formation and an extensive and thick ironstone layer consisting of haematitic pisolites and oölites in the upper Timeball Hill Formation indicate that atmospheric oxygen rose significantly, perhaps for the first time, during the deposition of the Rooihoogte and Timeball Hill formations. These units were deposited between what are probably the second and third of the three Palaeoproterozoic glacial events.

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Voegelin, A., Nagler, T., Beukes, N., & Lacassie, J. P. (2010) · Precambrian Research · doi:10.1016/j.precamres.2010.07.001 · Cited by 106
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Biological activity and the Earth's surface evolution: Insights from carbon, sulfur, nitrogen and iron stable isotopes in the rock record
Thomazo, C., Pinti, D. L., Busigny, V., Ader, M., HASHIZUME, K., & Philippot, P. (2009) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2009.02.003 · Cited by 120
Long-term sedimentary recycling of rare sulphur isotope anomalies
Reinhard, C. T., Planavsky, N. J., & Lyons, T. W. (2013) · Nature · doi:10.1038/nature12021 · Cited by 113
A Hypothesis on the Origin and Evolution of Tubulin
Ludueña, R. F. (2013) · International review of cytology · doi:10.1016/b978-0-12-407699-0.00002-9 · Cited by 119
The Geologic History of Seawater
Lowenstein, T. K., Kendall, B., & Anbar, A. D. (2013) · Elsevier eBooks · doi:10.1016/b978-0-08-095975-7.00621-5 · Cited by 117
Chromium Isotope Geochemistry
Qin, L., & Wang, X. (2017) · Reviews in Mineralogy and Geochemistry · doi:10.2138/rmg.2017.82.10 · Cited by 113
“The interest in Earth’s redox evolution stems from its intimate relationship with the evolution of life, including oxygenic photosynthesizers and animals together with their subsequent proliferations and extinctions (e.g., Bekker et al. 2004; Lau et al. 2016).”
Background
Anaerobic endosymbiont generates energy for ciliate host by denitrification
Graf, J. S., Schorn, S., Kitzinger, K., Ahmerkamp, S., Woehle, C., Hüettel, B., Schubert, C. J., Kuypers, M. M. M., & Milucka, J. (2021) · Nature · doi:10.1038/s41586-021-03297-6 · Cited by 113
Archean mafic–ultramafic volcanic landmasses and their effect on ocean–atmosphere chemistry
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Coupled Fe and S isotope variations in pyrite nodules from Archean shale
Marin‐Carbonne, J., Rollion‐Bard, C., Bekker, A., Rouxel, O. J., Agangi, A., Cavalazzi, B., Wohlgemuth‐Ueberwasser, C. C., Hofmann, A., & McKeegan, K. D. (2014) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2014.02.009 · Cited by 112
“…composition of sedimentary pyrites have placed important constraints on the chemistry and redox evolution of the Earth's ocean and atmosphere over geological time (e.g. Bekker et al., 2004; Farquhar et al., 2000; Johnson et al., 2008; Rouxel et al., 2003; Rouxel et al., 2005; Strauss, 2003).”
BackgroundSelf-citation
Apoptotic Cell Death Under Hypoxia
Sendoel, A., & Hengartner, M. O. (2014) · Physiology · doi:10.1152/physiol.00016.2013 · Cited by 157
Timescales of Oxygenation Following the Evolution of Oxygenic Photosynthesis
Ward, L. M., Kirschvink, J. L., & Fischer, W. W. (2015) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-015-9460-3 · Cited by 112
“…2.4 and 2.35 billion years ago (Gya) the Earth experienced one of its largest and most significant changes, when free molecular oxygen first accumulated in the atmosphere (Bekker et al. 2004; Papineau et al. 2007; Guo et al. 2009; Hoffman 2013; Johnson et al. 2013a, 2014; Rasmussen et al. 2013a).”
BackgroundInfluential
Singularities: Landmarks on the Pathways of Life
de Duve, C. (2005) · doi:10.1017/cbo9780511614736 · Cited by 141
Trace sulfate in mid-Proterozoic carbonates and the sulfur isotope record of biospheric evolution
Gellatly, A. M., & Lyons, T. W. (2005) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2005.01.019 · Cited by 110
“4 Ga, the so-called Great Oxidation Event marked the transition from fundamentally reducing to oxidizing conditions at the Earth’s surface (Holland, 2002; Bekker et al., 2004).”
BackgroundInfluential
100th Anniversary Special Paper: Sedimentary Mineral Deposits and the Evolution of Earth's Near-Surface Environments
Holland, H. D. (2005) · Economic Geology · doi:10.2113/gsecongeo.100.8.1489 · Cited by 110
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Late Archean euxinic conditions before the rise of atmospheric oxygen
Scott, C. T., Bekker, A., Reinhard, C. T., Schnetger, B., Krapež, B., Rumble, D., & Lyons, T. W. (2011) · Geology · doi:10.1130/g31571.1 · Cited by 109
Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park
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“45Ga (Bekker et al., 2004) and perhaps before the evolution of oxygenic photosynthesis at B2.”
Background
Origin of two distinct multiple-sulfur isotope compositions of pyrite in the 2.5Ga Klein Naute Formation, Griqualand West Basin, South Africa
Ono, S., Beukes, N. J., & Rumble, D., III (2008) · Precambrian Research · doi:10.1016/j.precamres.2008.10.012 · Cited by 108
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NADPH-dependent and -independent disulfide reductase systems
Miller, C. G., Holmgren, A., Arnér, E. S. J., & Schmidt, E. E. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.03.051 · Cited by 110
“1) resulted eventually in a ~105-fold increase in the concentration of atmospheric oxygen on earth [26].”
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Global glaciations and atmospheric change at ca. 2.3 Ga
Tang, H., & Chen, Y. (2013) · Geoscience Frontiers · doi:10.1016/j.gsf.2013.02.003 · Cited by 110
“Removal of most of the CH4 by oxidation due to the rise of O2 at 2320 Ma (Farquhar et al., 2000; Pavlov and Kasting, 2002; Bekker et al., 2004; Frei et al., 2009; Konhauser et al., 2009) has been considered as a cause of the Palaeoproterozoic glacia-”
Influential
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Shaw, G. H. (2008) · Geochemistry · doi:10.1016/j.chemer.2008.05.001 · Cited by 114
High primary productivity and nitrogen cycling after the Paleoproterozoic phosphogenic event in the Aravalli Supergroup, India
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Pervasive aerobic nitrogen cycling in the surface ocean across the Paleoproterozoic Era
Kipp, M. A., Stüeken, E. E., Yun, M., Bekker, A., & Buick, R. (2018) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2018.08.007 · Cited by 107
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Great Oxidation and Lomagundi events linked by deep cycling and enhanced degassing of carbon
Eguchi, J., Seales, J., & Dasgupta, R. (2019) · Nature Geoscience · doi:10.1038/s41561-019-0492-6 · Cited by 113
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Early evolution of atmospheric oxygen from multiple-sulfur and carbon isotope records of the 2.9 Ga Mozaan Group of the Pongola Supergroup, Southern Africa
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Current developments in marine microbiology: high-pressure biotechnology and the genetic engineering of piezophiles
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Earth's First Redox Revolution
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Modern rather than Mesoarchaean oxidative weathering responsible for the heavy stable Cr isotopic signatures of the 2.95 Ga old Ijzermijn iron formation (South Africa)
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“Only clades 1, 2 and 5 derived prior to the Great Oxidation Event (GOE, 2.32–2.45 BYA; Bekker et al. 2004).”
BackgroundInfluential
Multiple oscillations in Neoarchaean atmospheric chemistry
Izon, G., Zerkle, A. L., Zhelezinskaia, I., Farquhar, J., Newton, R. J., Poulton, S. W., Eigenbrode, J. L., & Claire, M. W. (2015) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2015.09.018 · Cited by 99
“Taken together, these arguments make the presence of S-MIF the most robust evidence for an atmosphere devoid of significant oxygen prior to ∼2.45 Ga (Bekker et al., 2004; Guo et al., 2009).”
BackgroundInfluential
Constraining atmospheric oxygen and seawater sulfate concentrations during Paleoproterozoic glaciation: In situ sulfur three-isotope microanalysis of pyrite from the Turee Creek Group, Western Australia
Williford, K. H., Kranendonk, M. J. V., Ushikubo, T., Kozdon, R., & Valley, J. W. (2011) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2011.07.010 · Cited by 108
“, 2001) suggest that sulfate concentrations may have temporarily exceeded the 200 lM threshold in restricted basins, but the prevailing view is that enhanced oxidative weathering of continental sulfides due to rising atmospheric oxygen was required to elevate sulfate concentrations in the global ocean (Cameron, 1982;…”
BackgroundInfluential
Dating and Tracing the History of Ore Formation
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Vibronic origin of sulfur mass-independent isotope effect in photoexcitation of SO 2 and the implications to the early earth’s atmosphere
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“4 Ga (16, 17) signifies a fundamental change in the earth’s surface sulfur cycles, and generally is linked to the suppression of both SO2 photolysis and the formation of elemental sulfur aerosols by the rise of atmospheric oxygen levels (15, 18, 19).”
Background
Emergence of an aerobic biosphere during the Archean-Proterozoic transition: Challenges of future research
Melezhik, V. A., Fallick, A. E., Hanski, E., Kump, L. R., Lepland, A., Prave, A. R., & Strauß, H. (2005) · GSA Today · doi:10.1130/1052-5173(2005)015[4:eoaabd]2.0.co;2 · Cited by 99
A Mesoproterozoic iron formation
Canfield, D. E., Zhang, S., Wang, H., Wang, X., Zhao, W., Su, J., Bjerrum, C. J., Haxen, E. R., & Hammarlund, E. U. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720529115 · Cited by 100
“In the latter scenario, an increase in sulfate flux to the ocean followed the great oxidation of the atmosphere (GOE) some 2,300 Ma (5, 7, 8).”
Background
Singularities: landmarks on the pathways of life
(2006) · Choice Reviews Online · doi:10.5860/choice.43-5276 · Cited by 102
A model for the oceanic mass balance of rhenium and implications for the extent of Proterozoic ocean anoxia
Sheen, A. I., Kendall, B., Reinhard, C. T., Creaser, R. A., Lyons, T. W., Bekker, A., Poulton, S. W., & Anbar, A. D. (2018) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2018.01.036 · Cited by 99
“The riverine ﬂux of Re is assumed to have become largely independent of atmospheric O 2 levels at the early stage of the GOE, when atmospheric O 2 levels rose above the threshold (as low as <0.001% PAL) required to support subaerial oxidative dissolution of crustal sulﬁde minerals and delivery of the related products…”
InfluentialSelf-citation
Palaeoproterozoic evaporites in Fennoscandia: implications for seawater sulphate, the rise of atmospheric oxygen and local amplification of the δ13C excursion
Melezhik, V. A., Fallick, A. E., Rychanchik, D. V., & Kuznetsov, A. B. (2005) · Terra Nova · doi:10.1111/j.1365-3121.2005.00600.x · Cited by 99
“Interestingly, the 2100 Ma Tulomozero evaporites post-date the inferred 2330 Ma atmospheric oxygen rise (Bekker et al., 2004).”
BackgroundInfluential
Filling in the juvenile magmatic gap: Evidence for uninterrupted Paleoproterozoic plate tectonics
Partin, C. A., Bekker, A., Sylvester, P., Wodicka, N., Stern, R. A., Chacko, T., & Heaman, L. M. (2013) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2013.11.041 · Cited by 98
“001% present atmospheric levels (PAL) to as high as 1–10% PAL (Bekker et al., 2004; Kump, 2008).”
Self-citation
Mixotrophy in marine picocyanobacteria: use of organic compounds by Prochlorococcus and Synechococcus
Muñoz‐Marín, M. D. C., Gómez‐Baena, G., López‐Lozano, A., Moreno-Cabezuelo, J. Á., Díez, J., & Garcı́a-Fernández, J. M. (2020) · The ISME Journal · doi:10.1038/s41396-020-0603-9 · Cited by 96
Replacement origin for hematite in 2.5 Ga banded iron formation: Evidence for postdepositional oxidation of iron-bearing minerals
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187 Re- 187 Os geochronology of Precambrian organic-rich sedimentary rocks
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Evidence of magnetic isotope effects during thermochemical sulfate reduction
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“Na2SO4 þ nC → Na2Sþ COþ CO2: [3]”
Searching for travertines, calcretes and speleothems in deep time: Processes, appearances, predictions and the impact of plants
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Authors: Bekker, A., Holland, H. D., Wang, P.-L., Rumble, D., Stein, H. J., Hannah, J. L., Coetzee, L. L., & Beukes, N. J.
Affiliations: Harvard University (US)
Carnegie Institution for Science (US)
Colorado State University (US)
University of Johannesburg (ZA)
Corresponding author: Bekker, A.
ORCID: Bekker, A.
Wang, P.-L.
Hannah, J. L.
Beukes, N. J.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2004-01
Volume: 427
Issue: 6970
Pages: 117-120
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature02260
OpenAlex: W2090027771
Cited by: 1,435
References: 43
Citations by year: 2026: 39 · 2025: 61 · 2024: 59 · 2023: 60 · 2022: 55 · 2021: 76 · 2020: 79 · 2019: 80 · 2018: 78 · 2017: 73 · 2016: 58 · 2015: 70 · 2014: 72 · 2013: 99 · 2012: 69
FWCI: 53.34
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Science Foundation
Topics: Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
Physical Sciences › Earth and Planetary Sciences › Geochemistry and Petrology › Geological and Geochemical Analysis
Physical Sciences › Earth and Planetary Sciences › Geochemistry and Petrology › Geochemistry and Elemental Analysis
Keywords: Great Oxidation, atmospheric oxygen rise, sulfur isotopes, mass-independent fractionation, oolites, Neoproterozoic, Precambrian geochemistry
MeSH terms: Atmosphere, Carbonates, Cold Climate, Geography, Ice, Iron, Isotopes, Oxygen, South Africa, Sulfides, Sulfur, Time Factors, Geologic Sediments

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