Review Article | Published:

The rise of oxygen in Earth’s early ocean and atmosphere

Nature volume 506, pages 307315 (20 February 2014) | Download Citation

Subjects

Abstract

The rapid increase of carbon dioxide concentration in Earth’s modern atmosphere is a matter of major concern. But for the atmosphere of roughly two-and-half billion years ago, interest centres on a different gas: free oxygen (O2) spawned by early biological production. The initial increase of O2 in the atmosphere, its delayed build-up in the ocean, its increase to near-modern levels in the sea and air two billion years later, and its cause-and-effect relationship with life are among the most compelling stories in Earth’s history.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Huronian rocks and uraniferous conglomerates in the Canadian Shield. Geol. Surv. Pap. Can. 68–40. (1969)

  2. 2.

    Volcanic gases, black smokers, and the Great Oxidation Event. Geochim. Cosmochim. Acta 66, 3811–3826 (2002)Formalized the notion of the GOE and highlighted the important balance between oxygen production and oxygen-buffering reactions, via reduced volatile compounds, in modulating the prevailing redox state at Earth’s surface.

  3. 3.

    The oxygenation of the atmosphere and oceans. Phil. Trans. R. Soc. B 361, 903–915 (2006)

  4. 4.

    The early history of atmospheric oxygen: Homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36 (2005)

  5. 5.

    , , , & Sulfur isotope evidence for an oxic Archaean atmosphere. Nature 442, 908–911 (2006)

  6. 6.

    , , & Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036 (1999)Essential organic biomarker study that provided the most-cited evidence for the earliest records of oxygen-producing photosynthesis, well before the GOE; the integrity of the biomarker data has been challenged in recent years.

  7. 7.

    Millimeter-scale concentration gradients of hydrocarbons in Archean shales: Live-oil escape or fingerprint of contamination? Geochim. Cosmochim. Acta 75, 3196–3213 (2011)

  8. 8.

    , , & Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1104 (2008)

  9. 9.

    et al. A whiff of oxygen before the Great Oxidation Event? Science 317, 1903–1906 (2007)Drew attention to the possibility of oxidative weathering of the continents—well before the GOE; recent challenges to the late Archaean organic biomarker record have elevated the value of the study’s inorganic data as likely signatures of pre-GOE oxygenesis.

  10. 10.

    , & Atmospheric oxygenation caused by a change in volcanic degassing pressure. Nature 478, 229–232 (2011)

  11. 11.

    & Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago. Nature 448, 1033–1036 (2007)

  12. 12.

    , & Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293, 839–843 (2001)Model exploring the consequences of atmospheric hydrogen escape for the redox budget of the evolving Earth; it has become a crucial lynchpin in the examination of Earth’s oxygenation within a planetary context.

  13. 13.

    , & Biogeochemical modelling of the rise in atmospheric oxygen. Geobiology 4, 239–269 (2006)

  14. 14.

    , & The rise of oxygen and the hydrogen hourglass. Chem. Geol (in the press)

  15. 15.

    & Paleoproterozic icehouses and the evolution of oxygen mediating enzymes: the case for a late origin of Photosystem-II. Phil. Trans. R. Soc. B 363, 2755–2765 (2008)

  16. 16.

    , & Atmospheric influence of Earth’s earliest sulfur cycle. Science 289, 756–758 (2000)Arguably the ‘smoking gun’ for the GOE—the loss of non-mass-dependent sulphur isotope fractionations—and thus launched a new wave of sulphur studies in Precambrian biogeochemistry and refined our understanding of early oxygenation.

  17. 17.

    & Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2, 27–41 (2002)

  18. 18.

    , & The loss of mass-independent fractionation in sulfur due to a Paleoproterozoic collapse of atmospheric methane. Geobiology 4, 271–283 (2006)

  19. 19.

    , , , & A bistable organic-rich atmosphere on the Neoarchaean Earth. Nature Geosci. 5, 359–363 (2012)

  20. 20.

    , & Explaining the structure of the Archean mass-independent sulfur isotope record. Science 329, 204–207 (2010)

  21. 21.

    A new model for Proterozoic ocean chemistry. Nature 396, 450–453 (1998)Spawned the concept of the ‘Canfield’ ocean by developing the idea that the ocean remained anoxic and probably euxinic for a billion years of the mid-Proterozoic, thus highlighting the essential lag between atmospheric and oceanic oxygenation and setting the stage for a generation of research in Precambrian oxygenation.

  22. 22.

    & U-rich Archaean sea-floor sediments from Greenland—indications of 3700 Ma oxygenic photosynthesis. Earth Planet. Sci. Lett. 217, 237–244 (2004)

  23. 23.

    Precambrian solution photochemistry, inverse segregation, and banded iron formations. Nature 276, 807–808 (1978)

  24. 24.

    et al. Photoferrotrophs thrive in an Archean ocean analogue. Proc. Natl Acad. Sci. USA 105, 15938–15943 (2008)

  25. 25.

    et al. Could bacteria have formed the Precambrian banded iron formations? Geology 30, 1079–1082 (2002)

  26. 26.

    , & The meaning of stromatolites. Annu. Rev. Earth Planet. Sci. 41, 21–44 (2013)

  27. 27.

    , & Microaerobic steroid biosynthesis and the molecular fossil record of Archean life. Proc. Natl Acad. Sci. USA 108, 13409–13414 (2011)

  28. 28.

    et al. Archean hydrocarbon biomarkers: Archean or not? Goldschmidt 2013 Conf. Abstr. (2013)

  29. 29.

    in The Proterozoic Biosphere (eds & ) Ch. 26.2 1185–1188 (Cambridge Univ. Press, 1992)

  30. 30.

    , & Geological constraints on the origin of oxygenic photosynthesis. Photosynth. Res. 107, 11–36 (2011)

  31. 31.

    , , & Re-Os and Mo isotope systematics of black shales from the Middle Proterozoic Velkerri and Wollogorang Formations, McArthur Basin, northern Australia. Geochim. Cosmochim. Acta 73, 2534–2558 (2009)

  32. 32.

    , , , & A late Archean sulfidic sea stimulated by early oxidative weathering of the continents. Science 326, 713–716 (2009)

  33. 33.

    , & Long-term sedimentary recycling of rare sulphur isotope anomalies. Nature 497, 100–103 (2013)

  34. 34.

    et al. Reconstructing Earth's surface oxidation across the Archean-Proterozoic transition. Geology 37, 399–402 (2009)

  35. 35.

    et al. Dating the rise of atmospheric oxygen. Nature 427, 117–120 (2004)First study to attempt to fingerprint the GOE precisely, using a tightly constrained stratigraphic record of the disappearance of NMD sulphur isotope fractionations, thus defining a temporal context for oxygenation models and major related climate events.

  36. 36.

    et al. Aerobic bacterial pyrite oxidation and acid rock drainage during the Great Oxidation Event. Nature 478, 369–373 (2011)

  37. 37.

    et al. Atmospheric oxygenation three billion years ago. Nature 501, 535–538 (2013)

  38. 38.

    The Phanerozoic Carbon Cycle (Oxford Univ. Press, 2004)

  39. 39.

    , & Bistability of atmospheric oxygen and the Great Oxidation. Nature 443, 683–686 (2006)

  40. 40.

    Vanadium in peridotites, mantle redox and tectonic environments: Archean to present. Earth Planet. Sci. Lett. 195, 75–90 (2002)

  41. 41.

    & The constancy of upper mantle fO2 through time inferred from V/Sc ratios in basalts. Earth Planet. Sci. Lett. 228, 483–493 (2004)

  42. 42.

    , & The oxidation state of Hadean magmas and implications for early Earth’s atmosphere. Nature 480, 79–82 (2011)

  43. 43.

    et al. Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458, 750–753 (2009)

  44. 44.

    , & Low-latitude glaciation in the Palaeoproterozoic era. Nature 386, 262–266 (1997)

  45. 45.

    , , , & Calibration of sulfate levels in the Archean ocean. Science 298, 2372–2374 (2002)

  46. 46.

    , , & A revised, hazy methane greenhouse for the Archean Earth. Astrobiology 8, 1127–1137 (2008)

  47. 47.

    , , & Neoarchaean seawater sulphate concentrations from sulphur isotopes in massive sulphide ore. Nature Geosci. 6, 61–64 (2013)

  48. 48.

    , & Greenhouse warming by CH4 in the atmosphere of early Earth. J. Geophys. Res. 105, 11981–11990 (2000)

  49. 49.

    & Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63, 311–334 (2009)

  50. 50.

    Solar interior structure and luminosity variations. Sol. Phys. 74, 21–34 (1981)

  51. 51.

    & Earth and Mars: evolution of atmospheres and surface temperatures. Science 177, 52–56 (1972)

  52. 52.

    & Carbon isotopes and the rise of atmospheric oxygen. Geology 24, 867–870 (1996)

  53. 53.

    , , , & Sulfur record of rising and falling marine oxygen and sulfate levels during the Lomagundi event. Proc. Natl Acad. Sci. USA 109, 18300–18305 (2012)

  54. 54.

    & The carbon cycle and associated redox processes through time. Phil. Trans. R. Soc. B 361, 931–950 (2006)

  55. 55.

    , , , & Rise in seawater sulphate concentration associated with the Paleoproterozoic positive carbon isotope excursion: evidence from sulphate evaporites in the 2.2–2.1 Gyr shallow-marine Lucknow Formation, South Africa. Terra Nova 20, 108–117 (2008)

  56. 56.

    et al. Large-scale fluctuations in Precambrian atmospheric and oceanic oxygen levels from the record of U in shales. Earth Planet. Sci. Lett. 369–370, 284–293 (2013)

  57. 57.

    & Oxygen overshoot and recovery during the early Paleoproterozoic. Earth Planet. Sci. Lett. 317–318, 295–304 (2012)

  58. 58.

    et al. Nitrogen cycle feedbacks as a control on euxinia in the mid-Proterozoic ocean. Nature Commun. 4, 1533 (2013)

  59. 59.

    et al. Tracing the stepwise oxygenation of the Proterozoic biosphere. Nature 452, 456–459 (2008)

  60. 60.

    et al. Proterozoic ocean redox and biogeochemical stasis. Proc. Natl Acad. Sci. USA 110, 5357–5362 (2013)State-of-the-art exploration of the redox landscape of the mid-Proterozoic ocean—with important implications for the mechanisms behind the persistently low levels of biospheric oxygen that defined the ‘boring billion’.

  61. 61.

    & Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137–1142 (2002)Building from the concept of the ‘Canfield’ ocean, this was the first paper to develop the idea of possible trace-metal limitations under assumed widespread euxinia in the mid-Proterozoic ocean as a throttle on early eukaryotic expansion.

  62. 62.

    , , , & History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc. Natl Acad. Sci. USA 107, 10567–10572 (2010)

  63. 63.

    , , & Molybdenum isotope evidence for widespread anoxia in Mid-Proterozoic oceans. Science 304, 87–90 (2004)

  64. 64.

    , , & The Sturgeon Falls paleosol and the composition of the atmosphere 1.1 Ga Bp. Precambr. Res. 42, 141–163 (1988)

  65. 65.

    , , & Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461, 250–253 (2009)

  66. 66.

    , & Rapid, oxygen-dependent microbial Mn(II) oxidation kinetics at sub-micromolar oxygen concentrations in the Black Sea suboxic zone. Geochim. Cosmochim. Acta 73, 1878–1889 (2009)

  67. 67.

    & Paleosols and the evolution of atmospheric oxygen: a critical review. Am. J. Sci. 298, 621–672 (1998)

  68. 68.

    , & Middle Proterozoic ocean chemistry: Evidence from McArthur Basin, Northern Australia. Am. J. Sci. 302, 81–109 (2002)

  69. 69.

    , , , & Tracking euxinia in the ancient ocean: A multiproxy perspective and Proterozoic case study. Annu. Rev. Earth Planet. Sci. 37, 507–534 (2009)

  70. 70.

    et al. Widespread iron-rich conditions in the mid-Proterozoic ocean. Nature 477, 448–451 (2011)

  71. 71.

    & Ferruginous conditions: a dominant feature of the ocean through Earth's history. Elements 7, 107–112 (2011)

  72. 72.

    , & Spatial variability in oceanic redox structure 1.8 billion years ago. Nature Geosci. 3, 486–490 (2010)

  73. 73.

    , , & Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age. Proc. Natl Acad. Sci. USA 106, 16925–16929 (2009)

  74. 74.

    , , , & Suboxic deep seawater in the late Paleoproterozoic: evidence from hematitic chert and iron formation related to seafloor-hydrothermal sulfide deposits, central Arizona, USA. Earth Planet. Sci. Lett. 255, 243–256 (2007)

  75. 75.

    , & Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae. Geobiology 7, 100–123 (2009)

  76. 76.

    et al. Iron formation: the sedimentary product of a complex interplay among mantle, tectonic, oceanic, and biospheric processes. Econ. Geol. 105, 467–508 (2010)

  77. 77.

    & Hydrothermal Fe fluxes during the Precambrian: effect of low oceanic sulfate concentrations and low hydrostatic pressure on the composition of black smokers. Earth Planet. Sci. Lett. 235, 654–662 (2005)

  78. 78.

    & The Neoproterozoic oxygenation event: Environmental perturbations and biogeochemical cycling. Earth Sci. Rev. 110, 26–57 (2012)

  79. 79.

    , & Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 92–95 (2007)

  80. 80.

    et al. Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489, 546–549 (2012)

  81. 81.

    , , & Oxidation of the Ediacaran ocean. Nature 444, 744–747 (2006)

  82. 82.

    , & Enigmatic origin of the largest-known carbon isotope excursion in Earth’s history. Nature Geosci. 4, 285–292 (2011)

  83. 83.

    & Does the global stratigraphic reproducibility of δ13C in Neoproterozoic carbonates require a marine origin? A Pliocene-Pleistocene comparison. Geology 40, 87–90 (2012)

  84. 84.

    et al. Ferruginous conditions dominated later Neoproterozoic deep-water chemistry. Science 321, 949–952 (2008)

  85. 85.

    , , & in Fundamentals of Geobiology (eds , & ) 371–402 (Blackwell, 2012)

  86. 86.

    et al. The evolution of the marine phosphate reservoir. Nature 467, 1088–1090 (2010)

  87. 87.

    et al. Cryogenian glaciation and the onset of carbon-isotope decoupling. Science 328, 608–611 (2010)

  88. 88.

    et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011)Essential overview of our present understanding of the cause-and-effect relationships among early animal evolution and diversification, increasing ecological complexity, and environmental change—particularly oxygenation of the ocean and atmosphere.

  89. 89.

    et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 (2009)

  90. 90.

    et al. Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nature Geosci. 3, 653–659 (2010)

  91. 91.

    Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7, 1–7 (2009)

  92. 92.

    Oxygen, ecology, and the Cambrian radiation of animals. Proc. Natl Acad. Sci. USA 110, 13446–13451 (2013)

  93. 93.

    , , & Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376, 53–56 (1995)

  94. 94.

    , , , & Mo isotopic composition of the mid-Neoproterozoic ocean: an iron formation perspective. Precambr. Res. 230, 168–178 (2013)

  95. 95.

    The rise of atmospheric oxygen. Nature 451, 277–278 (2008)

  96. 96.

    & A new model for atmospheric oxygen over Phanerozoic time. Am. J. Sci. 289, 333–361 (1989)

  97. 97.

    , & COPSE: A new model of biogeochemical cycling over Phanerozoic time. Am. J. Sci. 304, 397–437 (2004)

  98. 98.

    , & Causes of anoxia in the world ocean. Glob. Biogeochem. Cycles 2, 115–128 (1988)

  99. 99.

    , , & The sulfur cycle in the chemocline of a meromictic salt lake. Limnol. Oceanogr. 41, 147–156 (1996)

  100. 100.

    , & A global model for the early diagenesis of organic carbon and organic phosphorus in marine sediments. Geochim. Cosmochim. Acta 59, 1259–1284 (1995)

  101. 101.

    , & coupled atmosphere-ecosystem model of the early Archean Earth. Geobiology 3, 53–76 (2005)

  102. 102.

    et al. Organic carbon fluxes, degradation, and accumulation in an anoxic basin: Sediment trap results from the Cariaco Basin. Limnol. Oceanogr. 45, 300–308 (2000)

  103. 103.

    et al. Potential new production estimates in four eastern boundary upwelling ecosystems. Prog. Oceanogr. 83, 151–158 (2009)

  104. 104.

    & Mo–total organic carbon covariation in modern anoxic marine environments: Implications for analysis of paleoredox and paleohydrographic conditions. Paleoceanography 21, PA1016 (2006)

Download references

Acknowledgements

Funding from NSF-EAR, the NASA Exobiology Program, the NASA Astrobiology Institute, and the Agouron Institute supported this work. C.T.R. acknowledges support from an O. K. Earl Postdoctoral Fellowship in Geological and Planetary Sciences at the California Institute of Technology. N.J.P. acknowledges support from NSF-EAR-PDF. Comments and criticism from A. Bekker, D. Erwin, I. Halevy and D. Johnston improved the manuscript. A. Bekker was helpful in discussions about the GOE and suggested the acronym ‘GOT’.

Author information

Affiliations

  1. Department of Earth Sciences, University of California, Riverside, California 92521, USA

    • Timothy W. Lyons
    • , Christopher T. Reinhard
    •  & Noah J. Planavsky
  2. Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125, USA

    • Christopher T. Reinhard
  3. School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia 30332, USA

    • Christopher T. Reinhard
  4. Department of Geology and Geophysics, Yale University, New Haven, Connecticut 06511, USA

    • Noah J. Planavsky

Authors

  1. Search for Timothy W. Lyons in:

  2. Search for Christopher T. Reinhard in:

  3. Search for Noah J. Planavsky in:

Contributions

C.T.R. and N.J.P. designed the model for O2-producing photosynthesis and its relationship to Archaean organic carbon presented in Box 1. C.T.R. and N.J.P. compiled the database, and C.T.R. performed the modelling presented in Box 1. T.W.L. wrote the manuscript with major contributions from C.T.R. and N.J.P.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Timothy W. Lyons.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature13068

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.