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Evolution of the global phosphorus cycle

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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Figure 1: P content of fine-grained, marine siliciclastic sedimentary rocks through time.
Figure 2: Results from the global ocean-sediment biogeochemical model.
Figure 3: Results from the global ocean-sediment biogeochemical model.

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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.

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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.

Corresponding authors

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

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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.

Extended Data Figure 5 Proposed conceptual model for P cycling.

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−).

Extended Data Figure 7 Illustrative results of output from the ocean-sediment biogeochemical model.

ad, 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.

ac, 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.

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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

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