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.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Tyrrell, T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999)
Bjerrum, C. J. & Canfield, D. E. Ocean productivity before about 1.9 Ga ago limited by phosphorus adsorption onto iron oxides. Nature 417, 159–162 (2002)
Konhauser, K. O., Lalonde, S. V., Amskold, L. & Holland, H. D. Was there really an Archean phosphate crisis? Science 315, 1234 (2007)
Planavsky, N. et al. The evolution of the marine phosphate reservoir. Nature 467, 1088–1090 (2010)
Jones, C., Nomosatryo, S., Crowe, S. A., Bjerrum, C. J. & Canfield, D. E. Iron oxides, divalent cations, silica, and the early earth phosphorus crisis. Geology 43, 135–138 (2015)
Poulton, S. W. & Canfield, D. E. Ferruginous conditions: a dominant feature of the ocean through Earth’s history. Elements 7, 107–112 (2011)
Planavsky, N. J. et al. Widespread iron-rich conditions in the mid-Proterozoic ocean. Nature 477, 448–451 (2011)
Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014)
Shields-Zhou, G. & Och, L. The case for a Neoproterozoic oxygenation event: geochemical evidence and biological consequences. GSA Today 21, 4–11 (2011)
Hoffman, P. F. & Schrag, D. P. The Snowball Earth hypothesis: testing the limits of global change. Terra Nova 14, 129–155 (2002)
Erwin, D. H. et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011)
Love, G. D. et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 (2009)
Ruttenberg, K. C. in Treatise on Geochemistry Vol. 8 (eds Holland, H. D. & Turekian, K. K. ) 585–643 (Elsevier, 2003)
Taylor, R. & McLennan, S. M. The Continental Crust: its Composition and Evolution (Blackwell Science Publishing, 1985)
Holland, H. D. The Chemical Evolution of the Atmosphere and Ocean (Princeton Univ. Press, 1984)
Planavsky, N. J. The elements of marine life. Nat. Geosci. 7, 855–856 (2014)
Holland, H. D. Sedimentary mineral deposits and evolution of Earth’s near surface environments. Econ. Geol. 100, 1489–1509 (2005)
Partin, C. A. 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)
Lepland, A. et al. Potential influence of sulphur bacteria on Palaeoproterozoic phosphogenesis. Nat. Geosci. 7, 20–24 (2013)
Ingall, E. D. & Jahnke, R. Evidence for enhanced phosphorus regeneration from marine sediments overlain by oxygen depleted waters. Geochim. Cosmochim. Acta 58, 2571–2575 (1994)
Rudnick, R. L. & Gao, S. in Treatise on Geochemistry Vol. 3 (eds Holland, H. D. & Turekian, K. K. ) 1–64 (Elsevier, 2003)
Sperling, E. A. et al. Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523, 451–454 (2015)
Derry, L. A. Causes and consequences of mid-Proterozoic anoxia. Geophys. Res. Lett. 42, 8538–8546 (2015)
Zegeye, A. et al. Green rust formation controls nutrient availability in a ferruginous water column. Geology 40, 599–602 (2012)
Knoll, A. H. Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb. Perspect. Biol . 8, http://dx.doi.org/10.1101/cshperspect.a016121 (2014)
White, A. E., Spitz, Y. H., Karl, D. M. & Letelier, R. M. Flexible elemental stoichiomtery in Trichodesmium spp. and its ecological implications. Limnol. Oceanogr. 51, 1777–1790 (2006)
Frolich, P. N. et al. Pore water fluoride in Peru continental margin sediments: uptake from seawater. Geochim. Cosmochim. Acta 47, 1605–1612 (1983)
Jahnke, R. A., Emerson, S. R., Roe, K. K. & Burnett, W. C. The present-day formation of apatite in Mexican continental-margin sediments. Geochim. Cosmochim. Acta 47, 259–266 (1983)
Ruttenberg, K. C. Reassessment of the oceanic residence time of phosphorus. Chem. Geol. 107, 405–409 (1993)
Ozaki, K. & Tajika, E. 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)
Fennel, K., Follows, M. & Falkowski, P. G. The co-evolution of the nitrogen, carbon and oxygen cycles in the Proterozoic ocean. Am. J. Sci. 305, 526–545 (2005)
Laakso, T. A. & Schrag, D. P. Regulation of atmospheric oxygen during the Proterozoic. Earth Planet. Sci. Lett. 388, 81–91 (2014)
Reinhard, C. T. et al. Proterozoic ocean redox and biogeochemical stasis. Proc. Natl Acad. Sci. USA 110, 5357–5362 (2013)
Filippelli, G. M. The global phosphorus cycle. Rev. Mineral. Geochem. 48, 391–425 (2002)
Benitez-Nelson, C. R. The biogeochemical cycling of phosphorus in marine systems. Earth Sci. Rev. 51, 109–135 (2000)
Froelich, P. N. Kinetic control of dissolved phosphate in natural rivers and estuaries—a primer on the phosphate buffer mechanism. Limnol. Oceanogr. 33, 649–668 (1988)
Duce, R. A. et al. The atmospheric input of trace species to the world ocean. Glob. Biogeochem. Cycles 5, 193–259 (1991)
Fox, L. E., Lipschultz, F., Kerkhof, L. & Wofsy, S. C. A chemical survey of the Mississippi estuary. Estuaries 10, 1–12 (1987)
Fox, L. E., Sager, S. L. & Wofsy, S. C. The chemical control of soluble phosphorus in the Amazon estuary. Geochim. Cosmochim. Acta 50, 783–794 (1986)
Meybeck, M. Carbon, nitrogen, and phosphorus transport by world rivers. Am. J. Sci. 282, 401–450 (1982)
Filippelli, G. M. Controls on phosphorus concentration and accumulation in oceanic sediments. Mar. Geol. 139, 231–240 (1997)
Filippelli, G. M. & Delaney, M. L. Phosphorus geochemistry of equatorial Pacific sediments. Geochim. Cosmochim. Acta 60, 1479–1495 (1996)
Delaney, M. L. Phosphorus accumulation in marine sediments and the oceanic phosphorus cycle. Glob. Biogeochem. Cycles 12, 563–572 (1998)
Ruttenberg, K. C. & Berner, R. A. Authigenic apatite formation and burial in sediments from non-upwelling, continental-margin environments. Geochim. Cosmochim. Acta 57, 991–1007 (1993)
Li, C. 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)
Wang, X. et al. Chromium isotope fractionation during subduction-related metamorphism, black shale weathering, and hydrothermal alteration. Chem. Geol. 423, 19–33 (2016)
Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic biosphere. Nature 452, 456–459 (2008)
Shen, Y., Canfield, D. E. & Knoll, A. H. Middle Proterozoic ocean chemistry: evidence from McArthur Basin, Northern Australia. Am. J. Sci. 302, 81–109 (2002)
Shen, Y., Knoll, A. H. & Walter, M. A. Evidence for low sulfate and anoxia in a mid-Proterozoic marine basin. Nature 423, 632–635 (2003)
Scott, C. & Lyons, T. W. 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)
Tribovillard, N., Algeo, T. J., Lyons, T. & Riboulleau, A. Trace metals as paleoredox and paleoproductivity proxies: an update. Chem. Geol. 232, 12–32 (2006)
Algeo, T. J. & Maynard, J. B. Trace-metal covariation as a guide to water-mass conditions in ancient anoxic marine environments. Geosphere 4, 872–887 (2008)
Algeo, T. J. & Maynard, B. Trace-element behavior and redox facies in core shales of Upper Pennsylvanian Kansas-type cyclothems. Chem. Geol. 206, 289–318 (2004)
Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008)
Reinhard, C. T. et al. in Reading the Archive of Earth’s Oxygenation Vol. 3 (eds V. A. Melezhik et al.) 1483–1492 (Springer, 2013)
Rudnick, R. & Gao, S. in Treatise on Geochemistry 2nd edn, Vol. 4 (eds Holland, H. D. & Turekian, K. K. ) 1–51 (Elsevier, 2014)
Calvert, S. E. & Pederson, T. F. Geochemistry of Recent oxic and anoxic marine sediments: implications for the geological record. Mar. Geol. 113, 67–88 (1993)
Anderson, R. F., Fleischer, M. Q. & LeHuray, A. P. Concentration, oxidation state, and particulate flux of uranium in the Black Sea. Geochim. Cosmochim. Acta 53, 2215–2224 (1989)
Anderson, R. F., LeHuray, A. P., Fleisher, M. Q. & Murray, J. W. Uranium deposition in Saanich Inlet sediments, Vancouver Island. Geochim. Cosmochim. Acta 53, 2205–2213 (1989)
McManus, J., Berelson, W. M., Klinkhammer, G. P., Hammond, D. E. & Holm, C. Authigenic uranium: relationship to oxygen penetration depth and organic carbon rain. Geochim. Cosmochim. Acta 69, 95–108 (2005)
Jahnke, R. A. The synthesis and solubility of carbonate fluorapatite. Am. J. Sci. 284, 58–78 (1984)
Grotzinger, J. P. in Early Life on Earth (ed Bengston, S. ) Nobel Symposium No. 84, 245–258 (Columbia Univ. Press, 1994)
Grotzinger, J. P. & James, N. P. in Carbonate Sedimentation and Diagenesis in the Evolving Precambrian World (eds Grotzinger, J. P. & James, N. P. ) Special Publication 67, 1–20 (SEPM, 2000)
Pope, M. C., Grotzinger, J. P. & Schreiber, B. C. Evaporitic subtidal stromatolites produced by in situ precipitation: textures, facies associations, and temporal significance. J. Sediment. Res. 70, 1139–1151 (2000)
Ridgwell, A. A mid Mesozoic revolution in the regulation of ocean chemistry. Mar. Geol. 217, 339–357 (2005)
Ridgwell, A. & Zeebe, R. E. The role of the global carbonate cycle in the regulation and evolution of the Earth system. Earth Planet. Sci. Lett. 234, 299–315 (2005)
Boudreau, B. P. & Canfield, D. E. A comparison of closed- and open-system models for porewater pH and calcite-saturation state. Geochim. Cosmochim. Acta 57, 317–334 (1993)
Higgins, J. A., Fischer, W. W. & Schrag, D. P. Oxygenation of the ocean and sediments: consequences for the seafloor carbonate factory. Earth Planet. Sci. Lett. 284, 25–33 (2009)
Ben-Yaakov, S. pH buffering of pore water of recent anoxic marine sediments. Limnol. Oceanogr. 18, 86–94 (1973)
Feely, R. A., Trefry, J. H., Lebon, G. T. & German, C. R. The relationship between P/Fe and V/Fe ratios in hydrothermal precipitates and dissolved phosphate in seawater. Geophys. Res. Lett. 25, 2253–2256 (1998)
Poulton, S. W. & Canfield, D. E. 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)
Halverson, G. P. et al. Fe isotope and trace element geochemistry of the Neoproterozoic syn-glacial Rapitan iron formation. Earth Planet. Sci. Lett. 309, 100–112 (2011)
Rooney, A. D., Strauss, J. V., Brandon, A. D. & Macdonald, F. A. A Cryogenian chronology: two long-lasting synchronous Neoproterozoic glaciations. Geology 43, 459–462 (2015)
Canfield, D. E. et al. Ferruginous conditions dominated later Neoproterozoic deep-water chemistry. Science 321, 949–952 (2008)
Guilbaud, R., White, M. L. & Poulton, S. W. Surface charge and growth of sulphate and carbonate green rust in aqueous media. Geochim. Cosmochim. Acta 108, 141–153 (2013)
Bertilsson, S., Berglund, O., Karl, D. M. & Chisholm, S. W. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003)
Kuznetsov, I., Neumann, T. & Burchard, H. 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)
Larsson, U., Hajdu, S., Walve, J. & Elmgren, R. Baltic Sea nitrogen fixation estimated from the summer increase in upper mixed layer total nitrogen. Limnol. Oceanogr. 46, 811–820 (2001)
Tromp, T. K., Vancappellen, P. & Key, R. M. A global model for the early diagenesis of organic carbon and organic phosphorus in marine sediments. Geochim. Cosmochim. Acta 59, 1259–1284 (1995)
Dale, A. W., Meyers, S. R., Aguilera, D. R., Arndt, S. & Wallmann, K. 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)
Ingall, E. D. & Vancappellen, P. Relation between Sedimentation-Rate and Burial of Organic Phosphorus and Organic-Carbon in Marine-Sediments. Geochim. Cosmochim. Acta 54, 373–386 (1990)
Reinhard, C. T., Raiswell, R., Scott, C., Anbar, A. D. & Lyons, T. W. A Late Archean Sulfidic Sea Stimulated by Early Oxidative Weathering of the Continents. Science 326, 713–716 (2009)
Poulton, S. W., Fralick, P. W. & Canfield, D. E. Spatial variability in oceanic redox structure 1.8 billion years ago. Nat. Geosci. 3, 486–490 (2010)
Slomp, C. P., Thomson, J. & de Lange, G. J. Enhanced regeneration of phosphorus during formation of the most recent eastern Mediterranean sapropel (S1). Geochim. Cosmochim. Acta 66, 1171–1184 (2002)
Slomp, C. P. & Van Cappellen, P. The global marine phosphorus cycle: sensitivity to oceanic circulation. Biogeosciences 4, 155–171 (2007)
Goldhammer, T., Brüchert, V., Ferdelman, T. G. & Zabel, M. Microbial sequestration of phosphorus in anoxic upwelling sediments. Nat. Geosci. 3, 557–561 (2010)
Algeo, T. J. & Ingall, E. Sedimentary Corg:P ratios, paleocean ventilation, and Phanerozoic atmospheric pO2 . Palaeogeogr. Palaeoclimatol. Palaeoecol. 256, 130–155 (2007)
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.
The authors declare no competing financial interests.
Nature thanks S. Crowe and the other anonymous reviewer(s) for their contribution to the peer review of this work.
Extended data figures and tables
Extended Data Figure 1 Comparison of bulk P content and Corg content in marine siliciclastic sedimentary rocks.
There are large differences in bulk P content despite statistically indistinguishable Corg content (see main text). The crossplot shows bulk concentrations, and the histograms show bootstrap resampled mean values for each parameter. Note the differing scales between the raw data plot and resampled mean histograms.
Extended Data Figure 2 Distributions of P content in marine siliciclastic sedimentary rocks from our database.
On the left, from top to bottom, are pre-Cryogenian samples, anoxic Phanerozoic samples, and oxic Phanerozoic samples. For the Phanerozoic data, oxic and anoxic samples were delineated on the basis of sedimentary Mo enrichments (see main text). The shaded box denotes values greater than 0.2 wt%. On the right are cumulative frequency distributions (top) and bootstrap resampled mean P concentrations (bottom) for the same subsampled data sets.
Extended Data Figure 3 Distributions of P content in marine siliciclastic sedimentary rocks from our database.
On the left, from top to bottom, are pre-Cryogenian samples, anoxic Phanerozoic samples and oxic Phanerozoic samples. For the Phanerozoic data, oxic and anoxic samples were delineated on the basis of sedimentary uranium (U) enrichments (see main text). The shaded box denotes values greater than 0.2 wt%. On the right are cumulative frequency distributions (top) and bootstrap resampled mean P concentrations (bottom) for the same subsampled data sets. A single outlier containing 33 wt% P was removed during bootstrap resampling based on U content.
Extended Data Figure 4 Distributions of P content in marine siliciclastic sedimentary rocks from our database.
On the left, from top to bottom, are pre-Cryogenian samples, anoxic Phanerozoic samples and oxic Phanerozoic samples. For the Phanerozoic data, oxic and anoxic samples were delineated on the basis of sedimentary vanadium (V) enrichments (see main text). The shaded box denotes values greater than 0.2 wt%. On the right are cumulative frequency distributions (top) and bootstrap resampled mean P concentrations (bottom) for the same subsampled data sets.
a, Major P burial fluxes in a well oxygenated ocean–atmosphere system, where relatively high nutrient P availability and low phytoplankton C/P ratios facilitate extensive P burial in marginal marine sediments as authigenic CFA. b, P burial fluxes in a ferruginous ocean, in which scavenging of P by Fe mineral phases (a water-column Fe–P trap) leads to surface ocean P scarcity, high phytoplankton C/P ratios, and greatly decreased P burial in marginal marine sediments.
Extended Data Figure 6 Function used in the modified CANOPS model specifying dynamic primary producer biomass stoichiometry (C/P) as a function of ambient phosphate level, [PO43−].
The plot is based on the flexible stoichiometry model employed by ref. 58. The red dashed line shows the canonical Redfield ratio, whereas the green dashed line shows the default maximum C/P ratio for biomass, [C:P]max. The grey curve shows the function implemented in the model (see main text): f(PO43−).
a–d, Steady-state P removal fluxes from the model as a function of atmospheric for a range of net scavenging efficiencies, σscav. The Fe-bound, organic, authigenic, and scavenged P fluxes are denoted as ‘Fe’, ‘org’, ‘auth’ and ‘scav’, respectively.
Extended Data Figure 8 Illustrative results of output from the ocean-sediment biogeochemical model discussed in the text.
a–c, All panels show a given P burial flux (in mmol P m−2 yr−1) contoured as a function of steady-state atmospheric and ocean depth. a, The organic P burial flux; b, the Fe-bound P burial flux; and c, the authigenic P burial flux.
About this article
Cite this article
Reinhard, C., Planavsky, N., Gill, B. et al. Evolution of the global phosphorus cycle. Nature 541, 386–389 (2017). https://doi.org/10.1038/nature20772
Communications Earth & Environment (2022)
Nature Geoscience (2022)
Authigenic clay mineral evidence for restricted, evaporitic conditions during the emergence of the Ediacaran Doushantuo Biota
Communications Earth & Environment (2022)
Geochemical speciation and spatial distributions of phosphorus in surface sediments from the basin of the Marcus-Wake seamounts in the western Pacific Ocean
Acta Oceanologica Sinica (2022)