Abstract

The macronutrient phosphorus is thought to limit primary productivity in the oceans on geological timescales1. Although there has been a sustained effort to reconstruct the dynamics of the phosphorus cycle over the past 3.5 billion years2,3,4,5, it remains uncertain whether phosphorus limitation persisted throughout Earth’s history and therefore whether the phosphorus cycle has consistently modulated biospheric productivity and ocean–atmosphere oxygen levels over time. Here we present a compilation of phosphorus abundances in marine sedimentary rocks spanning the past 3.5 billion years. We find evidence for relatively low authigenic phosphorus burial in shallow marine environments until about 800 to 700 million years ago. Our interpretation of the database leads us to propose that limited marginal phosphorus burial before that time was linked to phosphorus biolimitation, resulting in elemental stoichiometries in primary producers that diverged strongly from the Redfield ratio (the atomic ratio of carbon, nitrogen and phosphorus found in phytoplankton). We place our phosphorus record in a quantitative biogeochemical model framework and find that a combination of enhanced phosphorus scavenging in anoxic, iron-rich oceans6,7 and a nutrient-based bistability in atmospheric oxygen levels could have resulted in a stable low-oxygen world. The combination of these factors may explain the protracted oxygenation of Earth’s surface over the last 3.5 billion years of Earth history8. However, our analysis also suggests that a fundamental shift in the phosphorus cycle may have occurred during the late Proterozoic eon (between 800 and 635 million years ago), coincident with a previously inferred shift in marine redox states9, severe perturbations to Earth’s climate system10, and the emergence of animals11,12.

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References

  1. 1.

    The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999)

  2. 2.

    & Ocean productivity before about 1.9 Ga ago limited by phosphorus adsorption onto iron oxides. Nature 417, 159–162 (2002)

  3. 3.

    , , & Was there really an Archean phosphate crisis? Science 315, 1234 (2007)

  4. 4.

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

  5. 5.

    , , , & Iron oxides, divalent cations, silica, and the early earth phosphorus crisis. Geology 43, 135–138 (2015)

  6. 6.

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

  7. 7.

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

  8. 8.

    , & The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014)

  9. 9.

    & The case for a Neoproterozoic oxygenation event: geochemical evidence and biological consequences. GSA Today 21, 4–11 (2011)

  10. 10.

    & The Snowball Earth hypothesis: testing the limits of global change. Terra Nova 14, 129–155 (2002)

  11. 11.

    et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011)

  12. 12.

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

  13. 13.

    in Treatise on Geochemistry Vol. 8 (eds & ) 585–643 (Elsevier, 2003)

  14. 14.

    & The Continental Crust: its Composition and Evolution (Blackwell Science Publishing, 1985)

  15. 15.

    The Chemical Evolution of the Atmosphere and Ocean (Princeton Univ. Press, 1984)

  16. 16.

    The elements of marine life. Nat. Geosci. 7, 855–856 (2014)

  17. 17.

    Sedimentary mineral deposits and evolution of Earth’s near surface environments. Econ. Geol. 100, 1489–1509 (2005)

  18. 18.

    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)

  19. 19.

    et al. Potential influence of sulphur bacteria on Palaeoproterozoic phosphogenesis. Nat. Geosci. 7, 20–24 (2013)

  20. 20.

    & Evidence for enhanced phosphorus regeneration from marine sediments overlain by oxygen depleted waters. Geochim. Cosmochim. Acta 58, 2571–2575 (1994)

  21. 21.

    & in Treatise on Geochemistry Vol. 3 (eds & ) 1–64 (Elsevier, 2003)

  22. 22.

    et al. Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523, 451–454 (2015)

  23. 23.

    Causes and consequences of mid-Proterozoic anoxia. Geophys. Res. Lett. 42, 8538–8546 (2015)

  24. 24.

    et al. Green rust formation controls nutrient availability in a ferruginous water column. Geology 40, 599–602 (2012)

  25. 25.

    Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb. Perspect. Biol . 8, (2014)

  26. 26.

    , , & Flexible elemental stoichiomtery in Trichodesmium spp. and its ecological implications. Limnol. Oceanogr. 51, 1777–1790 (2006)

  27. 27.

    et al. Pore water fluoride in Peru continental margin sediments: uptake from seawater. Geochim. Cosmochim. Acta 47, 1605–1612 (1983)

  28. 28.

    , , & The present-day formation of apatite in Mexican continental-margin sediments. Geochim. Cosmochim. Acta 47, 259–266 (1983)

  29. 29.

    Reassessment of the oceanic residence time of phosphorus. Chem. Geol. 107, 405–409 (1993)

  30. 30.

    & Biogeochemical effects of atmospheric oxygen concentration, phosphorus weathering, and sea-level stand on oceanic redox chemistry: implications for greenhouse climates. Earth Planet. Sci. Lett. 373, 129–139 (2013)

  31. 31.

    , & The co-evolution of the nitrogen, carbon and oxygen cycles in the Proterozoic ocean. Am. J. Sci. 305, 526–545 (2005)

  32. 32.

    & Regulation of atmospheric oxygen during the Proterozoic. Earth Planet. Sci. Lett. 388, 81–91 (2014)

  33. 33.

    et al. Proterozoic ocean redox and biogeochemical stasis. Proc. Natl Acad. Sci. USA 110, 5357–5362 (2013)

  34. 34.

    The global phosphorus cycle. Rev. Mineral. Geochem. 48, 391–425 (2002)

  35. 35.

    The biogeochemical cycling of phosphorus in marine systems. Earth Sci. Rev. 51, 109–135 (2000)

  36. 36.

    Kinetic control of dissolved phosphate in natural rivers and estuaries—a primer on the phosphate buffer mechanism. Limnol. Oceanogr. 33, 649–668 (1988)

  37. 37.

    et al. The atmospheric input of trace species to the world ocean. Glob. Biogeochem. Cycles 5, 193–259 (1991)

  38. 38.

    , , & A chemical survey of the Mississippi estuary. Estuaries 10, 1–12 (1987)

  39. 39.

    , & The chemical control of soluble phosphorus in the Amazon estuary. Geochim. Cosmochim. Acta 50, 783–794 (1986)

  40. 40.

    Carbon, nitrogen, and phosphorus transport by world rivers. Am. J. Sci. 282, 401–450 (1982)

  41. 41.

    Controls on phosphorus concentration and accumulation in oceanic sediments. Mar. Geol. 139, 231–240 (1997)

  42. 42.

    & Phosphorus geochemistry of equatorial Pacific sediments. Geochim. Cosmochim. Acta 60, 1479–1495 (1996)

  43. 43.

    Phosphorus accumulation in marine sediments and the oceanic phosphorus cycle. Glob. Biogeochem. Cycles 12, 563–572 (1998)

  44. 44.

    & Authigenic apatite formation and burial in sediments from non-upwelling, continental-margin environments. Geochim. Cosmochim. Acta 57, 991–1007 (1993)

  45. 45.

    et al. Marine redox conditions in the middle Proterozoic ocean and isotopic constraints on authigenic carbonate formation: insights from the Chuanlinggou Formation, Yanshan Basin, North China. Geochim. Cosmochim. Acta 150, 90–105 (2015)

  46. 46.

    et al. Chromium isotope fractionation during subduction-related metamorphism, black shale weathering, and hydrothermal alteration. Chem. Geol. 423, 19–33 (2016)

  47. 47.

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

  48. 48.

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

  49. 49.

    , & Evidence for low sulfate and anoxia in a mid-Proterozoic marine basin. Nature 423, 632–635 (2003)

  50. 50.

    & Contrasting molybdenum cycling and isotopic properties in euxinic versus non-euxinic sediments and sedimentary rocks: refining the paleoproxies. Chem. Geol. 324/325, 19–27 (2012)

  51. 51.

    , , & Trace metals as paleoredox and paleoproductivity proxies: an update. Chem. Geol. 232, 12–32 (2006)

  52. 52.

    & Trace-metal covariation as a guide to water-mass conditions in ancient anoxic marine environments. Geosphere 4, 872–887 (2008)

  53. 53.

    & Trace-element behavior and redox facies in core shales of Upper Pennsylvanian Kansas-type cyclothems. Chem. Geol. 206, 289–318 (2004)

  54. 54.

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

  55. 55.

    et al. in Reading the Archive of Earth’s Oxygenation Vol. 3 (eds et al.) 1483–1492 (Springer, 2013)

  56. 56.

    & in Treatise on Geochemistry 2nd edn, Vol. 4 (eds & ) 1–51 (Elsevier, 2014)

  57. 57.

    & Geochemistry of Recent oxic and anoxic marine sediments: implications for the geological record. Mar. Geol. 113, 67–88 (1993)

  58. 58.

    , & Concentration, oxidation state, and particulate flux of uranium in the Black Sea. Geochim. Cosmochim. Acta 53, 2215–2224 (1989)

  59. 59.

    , , & Uranium deposition in Saanich Inlet sediments, Vancouver Island. Geochim. Cosmochim. Acta 53, 2205–2213 (1989)

  60. 60.

    , , , & Authigenic uranium: relationship to oxygen penetration depth and organic carbon rain. Geochim. Cosmochim. Acta 69, 95–108 (2005)

  61. 61.

    The synthesis and solubility of carbonate fluorapatite. Am. J. Sci. 284, 58–78 (1984)

  62. 62.

    in Early Life on Earth (ed ) Nobel Symposium No. 84, 245–258 (Columbia Univ. Press, 1994)

  63. 63.

    & in Carbonate Sedimentation and Diagenesis in the Evolving Precambrian World (eds & ) Special Publication 67, 1–20 (SEPM, 2000)

  64. 64.

    , & Evaporitic subtidal stromatolites produced by in situ precipitation: textures, facies associations, and temporal significance. J. Sediment. Res. 70, 1139–1151 (2000)

  65. 65.

    A mid Mesozoic revolution in the regulation of ocean chemistry. Mar. Geol. 217, 339–357 (2005)

  66. 66.

    & The role of the global carbonate cycle in the regulation and evolution of the Earth system. Earth Planet. Sci. Lett. 234, 299–315 (2005)

  67. 67.

    & A comparison of closed- and open-system models for porewater pH and calcite-saturation state. Geochim. Cosmochim. Acta 57, 317–334 (1993)

  68. 68.

    , & Oxygenation of the ocean and sediments: consequences for the seafloor carbonate factory. Earth Planet. Sci. Lett. 284, 25–33 (2009)

  69. 69.

    pH buffering of pore water of recent anoxic marine sediments. Limnol. Oceanogr. 18, 86–94 (1973)

  70. 70.

    , , & The relationship between P/Fe and V/Fe ratios in hydrothermal precipitates and dissolved phosphate in seawater. Geophys. Res. Lett. 25, 2253–2256 (1998)

  71. 71.

    & Co-diagenesis of iron and phosphorus in hydrothermal sediments from the southern East Pacific Rise: implications for the evaluation of paleoseawater phosphate concentrations. Geochim. Cosmochim. Acta 70, 5883–5898 (2006)

  72. 72.

    et al. Fe isotope and trace element geochemistry of the Neoproterozoic syn-glacial Rapitan iron formation. Earth Planet. Sci. Lett. 309, 100–112 (2011)

  73. 73.

    , , & A Cryogenian chronology: two long-lasting synchronous Neoproterozoic glaciations. Geology 43, 459–462 (2015)

  74. 74.

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

  75. 75.

    , & Surface charge and growth of sulphate and carbonate green rust in aqueous media. Geochim. Cosmochim. Acta 108, 141–153 (2013)

  76. 76.

    , , & Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003)

  77. 77.

    , & Model study on the ecosystem impact of a variable C:N:P ratio for cyanobacteria in the Baltic Proper. Ecol. Modell. 219, 107–114 (2008)

  78. 78.

    , , & Baltic Sea nitrogen fixation estimated from the summer increase in upper mixed layer total nitrogen. Limnol. Oceanogr. 46, 811–820 (2001)

  79. 79.

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

  80. 80.

    , , , & Controls on organic carbon and molybdenum accumulation in Cretaceous marine sediments from the Cenomanian-Turonian interval including Oceanic Anoxic Event 2. Chem. Geol. 324/325, 28–45 (2012)

  81. 81.

    & Relation between Sedimentation-Rate and Burial of Organic Phosphorus and Organic-Carbon in Marine-Sediments. Geochim. Cosmochim. Acta 54, 373–386 (1990)

  82. 82.

    , , , & A Late Archean Sulfidic Sea Stimulated by Early Oxidative Weathering of the Continents. Science 326, 713–716 (2009)

  83. 83.

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

  84. 84.

    , & Enhanced regeneration of phosphorus during formation of the most recent eastern Mediterranean sapropel (S1). Geochim. Cosmochim. Acta 66, 1171–1184 (2002)

  85. 85.

    & The global marine phosphorus cycle: sensitivity to oceanic circulation. Biogeosciences 4, 155–171 (2007)

  86. 86.

    , , & Microbial sequestration of phosphorus in anoxic upwelling sediments. Nat. Geosci. 3, 557–561 (2010)

  87. 87.

    & Sedimentary Corg:P ratios, paleocean ventilation, and Phanerozoic atmospheric pO2. Palaeogeogr. Palaeoclimatol. Palaeoecol. 256, 130–155 (2007)

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Acknowledgements

This research was supported by funds from from NSF-EAR and the NASA Astrobiology Institute. C.T.R. acknowledges support from the Alfred P. Sloan Foundation. K.O. acknowledges support from JSPS KAKENHI.

Author information

Author notes

    • Christopher T. Reinhard
    •  & Noah J. Planavsky

    These authors contributed equally to this work.

Affiliations

  1. School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia 30332, USA

    • Christopher T. Reinhard
    •  & Kazumi Ozaki
  2. Department of Geology and Geophysics, Yale University, New Haven, Connecticut 06511, USA

    • Noah J. Planavsky
    •  & Devon B. Cole
  3. Department of Geosciences, Virginia Tech, Blacksburg, Virginia 24061, USA

    • Benjamin C. Gill
  4. Center for Earth Surface System Dynamics, University of Tokyo, Kashiwanoha 277-8561, Japan

    • Kazumi Ozaki
  5. Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada

    • Leslie J. Robbins
    •  & Kurt O. Konhauser
  6. Department of Earth Science, University of California, Riverside, California 92521, USA

    • Timothy W. Lyons
  7. Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125, USA

    • Woodward W. Fischer
  8. State Key Laboratory of Petroleum Resources and Prospecting, China University of Petroleum, Beijing 102249, China

    • Chunjiang Wang

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Contributions

C.T.R., N.J.P. and B.C.G. designed the research. N.J.P., B.C.G., D.B.C. and C.W. generated new analytical data. C.T.R., N.J.P., B.C.G., L.J.R. and D.B.C. compiled and analysed the database. C.T.R., N.J.P. and K.O. designed the biogeochemical model. K.O. wrote code and performed model simulations. All authors contributed to data interpretation and the writing of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Christopher T. Reinhard or Noah J. Planavsky.

Reviewer Information

Nature thanks S. Crowe and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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