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Isotopic Evidence for an Aerobic Nitrogen Cycle in the Latest Archean
Abstract
The nitrogen cycle provides essential nutrients to the biosphere, but its antiquity in modern form is unclear. In a drill core though homogeneous organic-rich shale in the 2.5-billion-year-old Mount McRae Shale, Australia, nitrogen isotope values vary from +1.0 to +7.5 per mil (per thousand) and back to +2.5 per thousand over approximately 30 meters. These changes evidently record a transient departure from a largely anaerobic to an aerobic nitrogen cycle complete with nitrification and denitrification. Complementary molybdenum abundance and sulfur isotopic values suggest that nitrification occurred in response to a small increase in surface-ocean oxygenation. These data imply that nitrifying and denitrifying microbes had already evolved by the late Archean and were present before oxygen first began to accumulate in the atmosphere.
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“The whiff is recorded by spikes in Mo and Re concentrations, elevated nitrogen isotope values, and iron speciation data (Anbar et al., 2007; Reinhard et al., 2009; Garvin et al., 2009);”
From Iron formations: A global record of Neoarchaean to Palaeoproterozoic environmental history (2017) · cites this paper as Garvin et al., 2009
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ResultTHE STABLE ISOTOPE GEOCHEMISTRY OF MOLYBDENUM
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BackgroundInfluentialThe cycling and redox state of nitrogen in the Archaean ocean
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“Hence, to reduce the potential post-depositional alterations in N isotopes, we specifically analysed the isotopic fractionation of the element in kerogen rather than bulk roc”
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BackgroundJohnson, B., & Goldblatt, C. (2015) · Earth-Science Reviews · doi:10.1016/j.earscirev.2015.05.006 · Cited by 224
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“…Precambrian evolution and radiation of organisms performing the main metabolic 105 pathways of the N cycle, such as NH4 + oxidation (Thomazo et al., 2011), denitrification 106 (Beaumont and Robert, 1999; Garvin et al., 2009; Godfrey and Falkowski, 2009) and N2-107 fixation (Stüeken et al., 2015a).”
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Self-citationOrigin and evolution of the atmospheres of early Venus, Earth and Mars
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“Small increases in sedimentary δ15N values alongside additional geochemical indicators of local oxygenation have been interpreted as evidence for the evolution of coupled nitrification-denitrification by ≈ 2.7 Gyr ago (Busigny and Bebout 2013; Garvin et al. 2009; Godfrey and Falkowski 2009).”
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InfluentialCoevolution of metal availability and nitrogen assimilation in cyanobacteria and algae
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A late methanogen origin for molybdenum-dependent nitrogenase
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BackgroundInfluentialSelf-citationReflections on O 2 as a Biosignature in Exoplanetary Atmospheres
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“7 Ga (Garvin et al., 2009; Thomazo et al., 2011), thereby favoring all heterotrophic microorganisms unable to fix N2.”
BackgroundInfluentialFully oxygenated water columns over continental shelves before the Great Oxidation Event
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Self-citationNitrogen isotope evidence for alkaline lakes on late Archean continents
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Onset of the aerobic nitrogen cycle during the Great Oxidation Event
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“The atomic ratio of particulate organic C to particulate organic N in RG sediment was 137, which is similar to organic C/N ratios in kerogen and cherts deposited during the Precambrian (2, 19) but which is elevated compared to organic C/N ratios of 10 to 20 commonly observed in shales deposited during the Devonian per…”
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BackgroundCo‐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 141
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Uranium isotope fractionation suggests oxidative uranium mobilization at 2.50 Ga
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“…2.5 Ga Mount McRae Shale of Western Australia (Anbar et al., 2007), in addition to changes in sedimentary sulfur (Kaufman et al., 2007), nitrogen (Garvin et al., 2009), andmolybdenum isotope compositions (Duan et al., 2010) that point to at least mild oxidative weathering conditions during the…”
BackgroundInfluentialA Chronostratigraphic Division of the Precambrian
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MethodThe Geologic History of Seawater
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Self-citationReactive Oxygen Species: Radical Factors in the Evolution of Animal Life
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“3) (Garvin et al. 2009; Godfrey and Falkowski 2009; Thomazo et al. 2011).”
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Microaerobic steroid biosynthesis and the molecular fossil record of Archean life
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Spotlight on the Thaumarchaeota
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“Therefore, it is tempting to speculate that the very ancient traces of nitrification recently suggested by isotopic records from the late Archaean (Garvin et al., 2009) may have been produced by the activity of ancient ammonia-oxidizing Thaumarchaeota.”
BackgroundPervasive 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
“The large isotopic variability seen in some Neoarchean facies is consistent with a small NO−3 reservoir (Garvin et al., 2009; Koehler et al., 2018), which could promote substantial inter-basinal variability and closed-system dynamics (discussed further in Section 5.3).”
BackgroundInfluentialSelf-citationEarth's First Redox Revolution
Ostrander, C. M., Johnson, A. C., & Anbar, A. D. (2021) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-072020-055249 · Cited by 102
Self-citationWilliford, 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
Möbius, J., Lahajnar, N., & Emeis, K. (2010) · Biogeosciences · doi:10.5194/bg-7-3901-2010 · Cited by 91
Geobiological feedbacks, oxygen, and the evolution of nitrogenase.
Mus, F., Colman, D., Peters, J., & Boyd, E. (2019) · Free Radical Biology & Medicine · doi:10.1016/j.freeradbiomed.2019.01.050 · Cited by 76
An anoxic, Fe(II)-rich, U-poor ocean 3.46 billion years ago
Li, W., Czaja, A. D., Kranendonk, M. J. V., Beard, B. L., Roden, E., & Johnson, C. M. (2013) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2013.06.033 · Cited by 94
The History of Ocean Oxygenation
Reinhard, C. T., & Planavsky, N. J. (2022) · Annual Review of Marine Science · doi:10.1146/annurev-marine-031721-104005 · Cited by 91
“…Group, South Africa), are consistent with the presence of coupled nitrification and denitrification (or anaerobic ammonium oxidation) reactions in some shallow marine environments (Garvin et al. 2009, Godfrey & Falkowski 2009, Koehler et al. 2018), strongly suggesting the presence of dissolved O2.”
BackgroundAtmospheric sulfur rearrangement 2.7 billion years ago: Evidence for oxygenic photosynthesis
Kurzweil, F., Claire, M., Thomazo, C., Peters, M., Hannington, M., & Strauss, H. (2013) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2013.01.028 · Cited by 91
Primary Productivity Was Limited by Electron Donors Prior to the Advent of Oxygenic Photosynthesis
Ward, L. M., Rasmussen, B., & Fischer, W. W. (2018) · Journal of Geophysical Research Biogeosciences · doi:10.1029/2018jg004679 · Cited by 95
“…efforts to develop a Precambrian nitrogen isotope record, little consensus has been reached about the nature of the Archean nitrogen cycle (e.g., Garvin et al., 2009; Zerkle et al., 2017), and even the N2 content of the Archean atmosphere is poorly constrained (e.g., Som et al., 2016; Zerkle &…”
BackgroundParsons, C., Stüeken, E. E., Rosen, C. J., Mateos, K., & Anderson, R. E. (2021) · Geobiology · doi:10.1111/gbi.12419 · Cited by 91
Selenium isotopes support free O2 in the latest Archean
Stüeken, E. E., Buick, R., & Anbar, A. D. (2015) · Geology · doi:10.1130/g36218.1 · Cited by 90
Self-citationKoehler, M. C., Stüeken, E. E., Kipp, M. A., Buick, R., & Knoll, A. H. (2016) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2016.10.050 · Cited by 90
“Heavy d15N(a) values, greater than those produced by biological N2 fixation alone and thus interpreted to represent aerobic nitrogen cycling, are known from the late Archean and early Paleoproterozoic before the Great Oxidation Event (Yamaguchi, 2002; Garvin et al., 2009; Godfrey and Falkowski, 2009; Busigny et al., 2…”
BackgroundInfluentialSelf-citationDifferential metamorphic effects on nitrogen isotopes in kerogen extracts and bulk rocks
Stüeken, E. E., Lima-Zaloumis, J., Meixnerová, J., & Buick, R. (2017) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2017.08.019 · Cited by 91
“…and +1‰, which is the canonical range of biological N2 fixation by Mo-nitrogenase and would be interpreted as such regardless of whether the interpretation is based on kerogen isolates or bulk rocks (e.g. Garvin et al., 2009; Godfrey and Falkowski, 2009; Stüeken et al., 2015a; Zerkle et al., 2017).”
BackgroundSelf-citationManganese oxides, Earth surface oxygenation, and the rise of oxygenic photosynthesis
Robbins, L. J., Fakhraee, M., Smith, A. J. B., Bishop, B., Swanner, E. D., Peacock, C. L., Wang, C., Planavsky, N. J., Reinhard, C. T., Crowe, S. A., et al. (2023) · Earth-Science Reviews · doi:10.1016/j.earscirev.2023.104368 · Cited by 96
“Perhaps more importantly, however, by 2.5 Ga there is evidence for the accumulation of nitrate in local environments within the Mt. McRae shale in western Australia and the Campbellrand-Malmani platform from South Africa (e.g., Garvin et al., 2009; Godfrey and Falkowski, 2009; Busigny et al., 2013).”
BackgroundInfluentialWang, D., Struck, U., Ling, H.-F., Guo, Q.-J., Shields-Zhou, G. A., Zhu, M.-Y., & Yao, S.-P. (2015) · Precambrian Research · doi:10.1016/j.precamres.2015.06.009 · Cited by 88
“…in the ratios range from 3.0 to 293.9 with a mean value of 61.5 in the Sancha section and from 35.8 to 133.5 with a mean value of 76.7 in the Yuanjia section, similar to other typically high Precambrian C/N ratios (>100) (Beaumont and Robert, 1999; Garvin et al., 2009; Papineau et al., 2009).”
BackgroundInfluentialSelenium isotopes record extensive marine suboxia during the Great Oxidation Event
Kipp, M. A., Stüeken, E. E., Bekker, A., & Buick, R. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1615867114 · Cited by 90
Self-citationKendall, B., Creaser, R. A., Reinhard, C. T., Lyons, T. W., & Anbar, A. D. (2015) · Science Advances · doi:10.1126/sciadv.1500777 · Cited by 86
Self-citationNitrogen isotope constraints on the early Ediacaran ocean redox structure
Wang, X., Jiang, G., Shi, X., Peng, Y., & Morales, D. C. (2018) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2018.08.034 · Cited by 84
Luo, G., Junium, C. K., Kump, L. R., Huang, J., Li, C., Feng, Q., Shi, X., Bai, X., & Xie, S. (2014) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2014.05.020 · Cited by 84
Biogeochemical Transformations in the History of the Ocean
Lenton, T. M., & Daines, S. J. (2016) · Annual Review of Marine Science · doi:10.1146/annurev-marine-010816-060521 · Cited by 80
Reexamination of 2.5-Ga “whiff” of oxygen interval points to anoxic ocean before GOE
Slotznick, S. P., Johnson, J. E., Rasmussen, B., Raub, T. D., Webb, S. M., Zi, J.-W., Kirschvink, J. L., & Fischer, W. W. (2022) · Science Advances · doi:10.1126/sciadv.abj7190 · Cited by 81
Kendall, B., Anbar, A. D., Kappler, A. A., & Konhauser, K. O. (2012) · Wiley eBooks · doi:10.1002/9781118280874.ch6 · Cited by 80
“…point to the presence of surface ocean O2 beneath a lowO2 atmosphere (<0.001% PAL based on MIF of sulfur isotopes; Anbar et al., 2007; Kaufman et al., 2007; Wille et al., 2007; Garvin et al., 2009; Godfrey and Falkowski, 2009; Reinhard et al., 2009; Duan et al., 2010a; Kendall et al., 2010).”
BackgroundInfluentialSelf-citationLimited oxygen production in the Mesoarchean ocean
Ossa, F. O., Hofmann, A., Spangenberg, J. E., Poulton, S. W., Stüeken, E. E., Schoenberg, R., Eickmann, B., Wille, M., Butler, M. J., & Bekker, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1818762116 · Cited by 74
“Since biological N2 fixation was evidently active in this environment, the growth and proliferation of O2-producing organisms were likely suppressed by nutrients other than nitrogen (e.g., phosphorus), which would have limited the expansion of oxygenated conditions during the Mesoarchean. oxygen oasis | nitrogen isoto…”
BackgroundInfluentialLuo, G., Junium, C. K., Izon, G., Ono, S., Beukes, N. J., Algeo, T. J., Cui, Y., Xie, S., & Summons, R. E. (2018) · Nature Communications · doi:10.1038/s41467-018-03361-2 · Cited by 75
The evolution of the global selenium cycle: Secular trends in Se isotopes and abundances
Stüeken, E. E., Buick, R., Bekker, A., Catling, D. C., Foriel, J., Guy, B. M., Kah, L. C., Machel, H. G., Montañez, I. P., & Poulton, S. W. (2015) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2015.04.033 · Cited by 74
“…al., 526 2006; Wille et al., 2007; Kendall et al., 2010) as well as other geochemical proxies including 527 sulfur (Stüeken et al., 2012), nitrogen (Garvin et al., 2009; Godfrey and Falkowski, 2009) and 528 organic carbon isotopes (Eigenbrode and Freeman, 2006) all support mildly or locally…”
BackgroundSelf-citationStüeken, E. E., Kipp, M. A., Koehler, M. C., Schwieterman, E. W., Johnson, B., & Buick, R. (2016) · Astrobiology · doi:10.1089/ast.2016.1537 · Cited by 73
“…greater degree than previously anticipated (Som et al. , 2016), (3) an aerobic nitrogen cycle arose before the Great Oxidation Event (GOE) at * 2.35 Ga (Garvin et al. , 2009; Godfrey and Falkowski, 2009), (4) during the mid-Proterozoic aerobic and anaerobic nitrogen cycling was spatially separated…”
InfluentialSelf-citationTransient surface ocean oxygenation recorded in the ∼2.66-Ga Jeerinah Formation, Australia
Koehler, M. C., Buick, R., Kipp, M. A., Stüeken, E. E., & Zaloumis, J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720820115 · Cited by 72
“Among the more salient features of this record is a proposed “whiff” of oxygen in surface environments at 2.5 Ga, well before the onset of the Great Oxidation Event (GOE) at ∼2.3–2.4 Ga (2, 3), which has been identified using combined trace metal and nitrogen isotope datasets collected at high stratigraphic resolution…”
BackgroundInfluentialSelf-citationPhylogeny of prokaryotes: does it exist and why should we care?
Gribaldo, S., & Brochier‐Armanet, C. (2009) · Research in Microbiology · doi:10.1016/j.resmic.2009.07.006 · Cited by 77
Nitrogen cycle in the Late Archean ferruginous ocean
Busigny, V., Lebeau, O., Ader, M., Krapež, B., & Bekker, A. (2013) · Chemical Geology · doi:10.1016/j.chemgeo.2013.06.023 · Cited by 71
“, 2011), and (3) quantitative oxidation of ammonium to nitrate, followed by partial denitrification in the water column (Garvin et al., 2009; Godfrey and Falkowski, 2009).”
BackgroundMethodInfluentialArchean Microbial Mat Communities
Tice, M. M., Thornton, D. C. O., Pope, M. C., Olszewski, T. D., & Gong, J. (2011) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-040809-152356 · Cited by 72
Mantle data imply a decline of oxidizable volcanic gases could have triggered the Great Oxidation
Kadoya, S., Catling, D. C., Nicklas, R. W., Puchtel, I. S., & Anbar, A. D. (2020) · Nature Communications · doi:10.1038/s41467-020-16493-1 · Cited by 72
Self-citationPapineau, D., Purohit, R., Fogel, M. L., & Shields, G. (2013) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2012.11.050 · Cited by 72
“, which preserve dNWR values between 0% and þ8% (Garvin et al., 2009).”
Schut, G. J., Zadvornyy, O. A., Wu, C.-H., Peters, J. W., Boyd, E. S., & Adams, M. W. W. (2016) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2016.01.010 · Cited by 69
“5 Ga) since the generation of this compound in substantial quantities is thought to also require molecular oxygen [32, 52].”
The Evolution Pathway of Ammonia-Oxidizing Archaea Shaped by Major Geological Events
Yang, Y., Zhang, C., Lenton, T. M., Yan, X., Zhu, M., Zhou, M., Tao, J., Phelps, T. J., & Cao, Z. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab129 · Cited by 66
The Geochemical Record of the Ancient Nitrogen Cycle, Nitrogen Isotopes, and Metal Cofactors
Godfrey, L., & Glass, J. B. (2010) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-381294-0.00022-5 · Cited by 70
“The greatest change in theN cycle occurred in the late Archean, following the onset of oxygenic photosynthesis by cyanobacteria (Anbar et al., 2007; Garvin et al., 2009; Godfrey and Falkowski, 2009; Waldbauer et al., 2009).”
BackgroundMethodCartigny, P., Farquhar, J. D., Thomassot, É., Harris, J. W., Wing, B., Masterson, A. L., McKeegan, K. D., & Stachel, T. (2009) · Lithos · doi:10.1016/j.lithos.2009.06.007 · Cited by 66
“The nitrogen isotopic composition of modern sediments thus shows average positive δ15N-values, of ~+2‰ for Archean and ~+5‰ for younger (recent) samples (Peters et al., 1976; Beaumont and Robert, 1999; Pinti et al., 2001; Garvin et al., 2009; review by Thomazo et al., in press).”
BackgroundMarine biogeochemical nitrogen cycling through Earth’s history
Stüeken, E. E., Pellerin, A., Thomazo, C., Johnson, B., Duncanson, S. P., & Schoepfer, S. D. (2024) · Nature Reviews Earth & Environment · doi:10.1038/s43017-024-00591-5 · Cited by 68
“Oxygenic photosynthesis probably arose and radiated around this time 69–73 , and therefore the increase in δ 15 N has been interpreted as evidence of nitrification coupled to O 2 , followed by denitrification in anoxic waters 74–76 .”
Revolutions in energy input and material cycling in Earth history and human history
Lenton, T. M., Pichler, P., & Weisz, H. (2016) · Earth System Dynamics · doi:10.5194/esd-7-353-2016 · Cited by 69
“Nitrogen would initially have been in the form of ammonium (rather than nitrate), but the advent of an oxygen source plausibly triggered the onset of nitrification and denitrification (Godfrey and Falkowski, 2009; Garvin et al., 2009).”
BackgroundReconciling evidence of oxidative weathering and atmospheric anoxia on Archean Earth
Johnson, A. C., Ostrander, C. M., Romaniello, S. J., Reinhard, C. T., Greaney, A. T., Lyons, T. W., & Anbar, A. D. (2021) · Science Advances · doi:10.1126/sciadv.abj0108 · Cited by 65
Self-citationOceanic redox evolution across the end-Permian mass extinction at Shangsi, South China
Xiang, L., Schoepfer, S. D., Zhang, H., Yuan, D., Cao, C., Zheng, Q.-F., Henderson, C. M., & Shen, S. (2015) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2015.10.046 · Cited by 62
Oxidative sulfide dissolution on the early Earth
Reinhard, C. T., Lalonde, S. V., & Lyons, T. W. (2013) · Chemical Geology · doi:10.1016/j.chemgeo.2013.10.006 · Cited by 60
Metadata
- Authors
- Garvin, J., Buick, R., Anbar, A. D., Arnold, G. L., & Kaufman, A. J.
- Affiliations
- University of Washington (US)
- Corresponding author
- Buick, Roger
- Venue
- Science
- Published
- 2009-02-20
- Volume
- 323
- Issue
- 5917
- Pages
- 1045-1048
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2000496027
- Cited by
- 260
- References
- 23
- Citations by year
- 2026: 6 · 2025: 21 · 2024: 14 · 2023: 11 · 2022: 18 · 2021: 18 · 2020: 13 · 2019: 14 · 2018: 20 · 2017: 17 · 2016: 8 · 2015: 11 · 2014: 12 · 2013: 23 · 2012: 18
- FWCI
- 13.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- 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 › Earth and Planetary Sciences › Geochemistry and Petrology › Geological and Geochemical Analysis
- Keywords
- nitrogen cycling, Archean, nitrogen isotopes, nitrification, denitrification, molybdenum, sulfur isotopes, ocean oxygenation, organic-rich shale, rock core
- MeSH terms
- Aerobiosis, Quaternary Ammonium Compounds, Anaerobiosis, Archaea, Australia, Bacteria, Biological Evolution, Nitrates, Nitrites, Nitrogen, Nitrogen Fixation, Nitrogen Isotopes, Oceans and Seas, Oxidation-Reduction, Oxygen, Time, Geologic Sediments
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