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Uncovering the Ediacaran phosphorus cycle

Nature volume 618, pages 974–980 (2023)Cite this article

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Abstract

Phosphorus is a limiting nutrient that is thought to control oceanic oxygen levels to a large extent1,2,3. A possible increase in marine phosphorus concentrations during the Ediacaran Period (about 635–539 million years ago) has been proposed as a driver for increasing oxygen levels4,5,6. However, little is known about the nature and evolution of phosphorus cycling during this time4. Here we use carbonate-associated phosphate (CAP) from six globally distributed sections to reconstruct oceanic phosphorus concentrations during a large negative carbon-isotope excursion—the Shuram excursion (SE)—which co-occurred with global oceanic oxygenation7,8,9. Our data suggest pulsed increases in oceanic phosphorus concentrations during the falling and rising limbs of the SE. Using a quantitative biogeochemical model, we propose that this observation could be explained by carbon dioxide and phosphorus release from marine organic-matter oxidation primarily by sulfate, with further phosphorus release from carbon-dioxide-driven weathering on land. Collectively, this may have resulted in elevated organic-pyrite burial and ocean oxygenation. Our CAP data also seem to suggest equivalent oceanic phosphorus concentrations under maximum and minimum extents of ocean anoxia across the SE. This observation may reflect decoupled phosphorus and ocean anoxia cycles, as opposed to their coupled nature in the modern ocean. Our findings point to external stimuli such as sulfate weathering rather than internal oceanic phosphorus–oxygen cycling alone as a possible control on oceanic oxygenation in the Ediacaran. In turn, this may help explain the prolonged rise of atmospheric oxygen levels.

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Fig. 1: CAP (given as CAP/(Ca+Mg)) and accompanying key geochemical records in six globally distributed sections that record the SE, the largest known negative C-isotope excursion in carbonate (δ13Ccarb) from the geological record.
Fig. 2: Conceptual model illustrating the coevolution of the phosphorus cycle and DOM oxidation during the SE (see text for detailed description of the panels).
Fig. 3: Biogeochemical quantitative model results that best replicate the observed CAP and C-, U-, S- and Sr-isotope records in Fig. 1.

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Data availability

All data generated or analysed during this study are available at https://figshare.com/articles/dataset/Dodd_et_al_2023_xlsx/22274293 and included with the published article (and its Supplementary Information files). Source data are provided with this paper.

Code availability

MATLAB code for COPSE is freely available at https://github.com/bjwmills/COPSE.

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Acknowledgements

We thank B. Shen and R. Wang for generously providing samples from the Mochia-Khutuk section and L. Zheng for assistance in obtaining the Sishang section samples. This study was supported by the NSFC (grant nos. 41825019, 42130208 and 41821001) and the National Key Research and Development Program of China (2022YFF0800100) for funding. M.S.D. acknowledges support from the International Exchange Program for Postdoctors of China and funding from the China Postdoctoral Science Foundation, the Forrest Research Foundation and the University of Western Australia School of Earth Sciences. A.vS.H. and M.W. acknowledge support from the ARC (DE190100988 and DP210103715). Further funding through the NASA Astrobiology Institute under Cooperative Agreement No. NNA15BB03A issued through the Science Mission Directorate and the Interdisciplinary Consortia for Astrobiology Research (T.W.L.).

Author information

Authors and Affiliations

  1. State Key Laboratory of Oil and Gas Reservoir Geology and Exploitation, Institute of Sedimentary Geology, Chengdu University of Technology, Chengdu, China

    Matthew S. Dodd, Wei Shi, Chao Li, Zihu Zhang & Meng Cheng

  2. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, China

    Matthew S. Dodd, Chao Li & Haodong Gu

  3. International Center for Sedimentary Geochemistry and Biogeochemistry Research, Chengdu University of Technology, Chengdu, China

    Matthew S. Dodd, Wei Shi, Chao Li, Zihu Zhang & Meng Cheng

  4. School of Earth Sciences, University of Western Australia, Perth, Western Australia, Australia

    Matthew S. Dodd

  5. Forrest Research Foundation, Perth, Western Australia, Australia

    Matthew S. Dodd

  6. Department of Earth and Environmental Sciences, Michigan State University, East Lansing, MI, USA

    Dalton S. Hardisty

  7. Department of Geological Sciences, California State University, Fullerton, CA, USA

    Sean J. Loyd

  8. School of Geography, Earth and Atmospheric Sciences, University of Melbourne, Parkville, Victoria, Australia

    Malcolm W. Wallace, Ashleigh vS. Hood & Kelsey Lamothe

  9. School of Earth and Environment, University of Leeds, Leeds, UK

    Benjamin J. W. Mills & Simon W. Poulton

  10. Department of Earth and Planetary Sciences, University of California, Riverside, Riverside, CA, USA

    Timothy W. Lyons

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  1. Matthew S. Dodd
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Contributions

C.L. led the research. C.L. and M.S.D. designed the research. M.S.D., Z.Z., M.C. and H.G. performed analyses. W.S. and B.J.W.M. conducted modelling work. C.L., T.W.L., D.S.H., S.J.L., M.W.W., A.vS.H., K.L., M.C. and H.G. provided samples and assistance in the field. S.W.P. provided analytical assistance. M.S.D., C.L. and W.S. wrote the manuscript, with important discussion and contributions from all authors.

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Correspondence to Chao Li.

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Extended data figures and tables

Extended Data Fig. 1 Open-system diagenetic evolution fluid–rock interaction model.

a–c, Fluid–rock alteration models showing the relative order of alteration for CAP, CAS, Fe, Mn, IO3, δ13C, δ34SCAS, δ238U, δ44/40Ca and 87Sr/86Sr. Several curves are presented for δ13C and δ34SCAS under varying DIC and sulfate concentrations in the diagenetic fluid. d, Fluid–rock alteration model showing the predicted trends between CAP and δ13C. Grey points are CAP and δ13C data from all study sections. Solid and dashed lines represent different pore-water DIC concentration and δ13C compositions. Dotted line is trendline through data points with R value. See Supplementary Information for model description. Yellow stars mark the point at which 50% of the CAP value has been altered. Red stars mark the point at which 50% of the element of interest has been altered.

Extended Data Fig. 2 COPSE model results comparing different hypotheses (DOM oxidation by sulfate only, elevated organic-matter recycling, elevated weathering by uplift, elevated weathering by volcanism) for the observed changes in ocean P during the SE.

a,A,I,i, Relative increase in sulfate addition versus background flux. b,B,II,ii, Phosphorus concentration in seawater ([P]sw). c,C,III,iii, Relative atmospheric oxygen concentration (pO2). d,D,IV,iv, Degree of ocean anoxia (Anoxia). e,E,V,v, Modelled marine carbonate carbon-isotope composition (δ13Ccarb). Note that in panel E, the δ13Ccarb reflects the δ13C of pore water DIC, not oceanic δ13C. f,F,VI,vi, Modelled marine sulfate sulfur-isotope composition (δ34Ssulfate). g,G,VII,vii, Modelled marine carbonate uranium-isotope composition (δ238Ucarb). For the DOM oxidation hypothesis, we run the COPSE model with a DOM reservoir 30 times the size of the modern marine DIC reservoir and the C:P of the DOM reservoir is 1,000, whereas the C:P of organic matter in the organic-matter recycle model is 250 (see Supplementary Information 6 for more details). PAL, present atmospheric level.

Extended Data Fig. 3 COPSE model results comparing the oxidation of a DOM reservoir using sulfate, free oxygen (Shields et al.37) and sulfate + free oxygen, respectively.

a,A,I, Relative increase in sulfate addition versus background flux (the varying colour shades of the model lines reflect the varying magnitudes of the sulfate pulse for different model runs). b,B,II, Phosphorus concentration in seawater ([P]sw). c,C,III, Relative atmospheric oxygen concentration (pO2). d,D,IV, Degree of ocean anoxia (Anoxia). e,E,V, Modelled marine carbonate carbon-isotope composition (δ13Ccarb). f,F,VI, Modelled marine sulfate sulfur-isotope composition (δ34Ssulfate). The C:P of the DOM reservoir is set to 1,000 in all model runs. The magnitude of the sulfate pulses for each model is variable because higher additional sulfate fluxes are required for models in which DOM is oxidized by O2 resulting from pyrite burial in comparison with models in which DOM is oxidized only by sulfate (see Supplementary Information 7 for details).

Extended Data Fig. 4 COPSE model results with varying sizes (A–F) and variable P content (a–d) of an initial DOM reservoir and higher initial steady-state pO2 of 20% present atmospheric level (PAL), with C:P of DOM = 250 (a–d) (no Fe2+-P burial) (I–IV).

A, Size of DOM reservoir in moles of carbon. B, Phosphorus concentration in seawater ([P]sw). C, Relative atmospheric oxygen concentration (pO2). D, Degree of ocean anoxia (Anoxia). E, Modelled marine carbonate carbon-isotope composition (δ13Ccarb). F, Modelled marine carbonate uranium-isotope composition (δ238Ucarb). In panels A–F, we choose a sulfate pulse of four times that of the background flux and the C:P of the DOM reservoir is 1,000. a,I, Size of DOM reservoir in moles of carbon. b,II, Phosphorus concentration in seawater ([P]sw). c,III, Relative atmospheric oxygen concentration (pO2). d,IV, Degree of ocean anoxia. In panels a–d, we choose a sulfate input of four times the background flux and the size of the DOM reservoir is 30 times that of the size of the modern marine DIC reservoir. For panels I–IV, the DOM reservoir is 30 times that of the size of the modern marine DIC. Higher steady-state pO2 was achieved by adjusting the model terrestrial P-input flux and gypsum burial.

Extended Data Fig. 5 COPSE model results varying the magnitude of a further sulfate pulse for DOM oxidation by sulfate only (no Fe2+-P burial) (a–h), burying all the extra sulfate pulse as pyrite (I–VIII) and setting gypsum burial to a constant rate (i–viii).

a, Size of DOM reservoir in moles of carbon. b, Modelled marine carbonate carbon-isotope composition (δ13Ccarb). c, Phosphorus concentration in seawater ([P]sw). d, Modelled marine carbonate uranium-isotope composition (δ238Ucarb). e, Relative atmospheric oxygen concentration (pO2). f, Degree of ocean anoxia. g, Modelled marine sulfate sulfur-isotope composition (δ34Ssulfate). h, Modelled marine carbonate strontium-isotope composition (87Sr/86Sr). The blue line, grey line and dashed grey line are sulfate pulses of three, four and five times the background flux, respectively. I,i, Relative atmospheric oxygen concentration (pO2). II,ii, Phosphorus concentration in seawater ([P]sw). III,iii, Modelled marine carbonate carbon-isotope composition (δ13Ccarb). VI,vi, Evolution of ocean anoxia. V,v, Modelled marine carbonate uranium-isotope composition (δ238Ucarb). VI,vi, Modelled marine sulfate sulfur-isotope composition (δ34Ssulfate). VII,vii, Sulfate concentration in seawater ([SO4]sw). VIII,viii, Oceanic gypsum burial rate (mgsb). Here we used a DOM reservoir size that is 30 times that of the size of the modern marine DIC reservoir. PAL, present atmospheric level; POL, present oceanic level.

Extended Data Fig. 6 Full COPSE model outputs for DOM oxidation by sulfate with constant Fe2+-bound phosphorus burial, using a sulfate pulse of four times the background flux, DOM C:P of 1,000 and the size of the DOM reservoir is 30 times the size of the modern marine DIC reservoir.

a, Weathering sulfate pulse versus background flux. b, DOM oxidation flux (DOMox) in moles of carbon per year. c, DOM reservoir (DOMpool) in moles of carbon. d, P concentration in seawater ([P]sw). e, Relative atmospheric oxygen concentration (pO2) to present atmospheric level (PAL). f, Degree of marine anoxia (Anoxia). g, Modelled marine carbonate carbon-isotope composition (δ13Ccarb). h, Modelled marine sulfate sulfur-isotope composition (δ34Ssulfate). i, Silicate weathering flux (silw) in moles of carbon per year. j, Modelled marine carbonate strontium-isotope composition (87Sr/86Sr). k, Relative marine sulfate concentration ([SO42−]sw) to present oceanic level (POL). l, Relative marine new primary productivity (newp) to POL. m, Relative atmospheric carbon dioxide concentration (pCO2) to PAL. n, Average global temperature (Temp) in °C. o, Organic carbon weathering flux (oxidw) in moles of carbon per year. p, Marine organic carbon burial flux (mocb) in moles of carbon. q, Gypsum sulfur weathering flux (gypw) in moles of sulfur. r, Pyrite sulfur weathering flux (pyrw) in moles of sulfur. s, Marine pyrite sulfur burial flux (mpsb) in moles of sulfur. t, Marine gypsum sulfur burial flux (mgsb) in moles of sulfur. u, Phosphorus releasing flux from DOM oxidation (DOMOX_P) in moles of phosphorus. v, Flux of weathered phosphorus reaching the sea (psea) in moles of phosphorus. w, Total iron-bound phosphorus burial flux (fepb) in moles of phosphorus. x, Carbonate-bound phosphorus burial flux (capb) in moles of phosphorus. y, Marine organic phosphorus burial flux (mopb) in moles of phosphorus. z, Ferric iron Fe3+-bound phosphorus burial [fepb(Fe3+)] in moles of phosphorus. aa, Ferrous iron Fe2+-bound phosphorus burial [fepb(Fe2+)] in moles of phosphorus.

Extended Data Fig. 7 Comparison of COPSE model results for ocean P cycling with and without P burial by Fe2+ scavenging.

a, Ocean inorganic carbon isotopic composition (δ13Ccarb). b, Ocean P concentration ([P]sw). c, Ocean uranium isotopic composition recorded in carbonates (δ238Ucarb). d, Ocean sulfur isotopic composition recorded in carbonate-associated sulfate (δ34SCAS). e, Ocean strontium isotopic composition (87Sr/86Sr). f, Ediacaran fossil record adapted after Darroch et al.19. Stages I–IV are defined as the SE intervals of falling limb, plateau, rising limb and post-SE, respectively, as in Fig. 1, which are matched with modelled ocean P reservoir shifts. Model parameters for outputs are the same as detailed in Fig. 3 and Extended Data Fig. 6, except for the red line, which excludes P burial by Fe2+ scavenging (that is, a modern-style P and O2 cycle). P-1st and P-2nd refer to CAP peaks in Fig. 1.

Extended Data Fig. 8 Model output of a quantitative four-box ocean P cycle model.

Output from Figs. 4a and 5a in Alcott et al.13 with the P concentrations in the respective boxes (proximal shelf, distal shelf, deep ocean) plotted. This shows the relative concentration of soluble reactive phosphorus in each ocean box during a model solution in which P levels are oscillating on a large scale. These results show that, even under substantial changes in P concentration, the distal shelf (that is, the area of the shelf that is not dominated by riverine input) is expected to be strongly linked to the deep-ocean P concentration. See Alcott et al.13 for full model details.

Extended Data Fig. 9 Experimental constraints on the effects of alkalinity (a) and carbonate precipitation rate (b) on CAP values in carbonate.

a, CAP uptake increases with progressively lower [CO32−] and alkalinity concentrations. b, CAP uptake decreases with increasing precipitation rate. The changes in CAP over the observed ranges in alkalinity and precipitation rate are small compared with the effects of phosphate concentration and solution pH (Dodd et al.29). All trendlines are linear fits. Error bars are ±5% for CAP and ±0.1 for Ca/ALK.

Extended Data Table 1 Statistics for CAP extraction and diagenetic measures
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Dodd, M.S., Shi, W., Li, C. et al. Uncovering the Ediacaran phosphorus cycle. Nature 618, 974–980 (2023). https://doi.org/10.1038/s41586-023-06077-6

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