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      Ediacaran reorganization of the marine phosphorus cycle

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          Significance

          The evolution of macroscopic animals in the latest Proterozoic Eon is associated with many changes in the geochemical environment, but the sequence of cause and effect remains a topic of intense research and debate. In this study, we use two apparently paradoxical observations—that massively phosphorus-rich rocks first appear at this time, and that the median P content of rocks does not change—to argue for a change in internal marine P cycling associated with rising sulfate levels. We argue that this change was self-sustaining, setting in motion a cascade of biogeochemical transformations that led to conditions favorable for major ecological and evolutionary change.

          Abstract

          The Ediacaran Period (635 to 541 Ma) marks the global transition to a more productive biosphere, evidenced by increased availability of food and oxidants, the appearance of macroscopic animals, significant populations of eukaryotic phytoplankton, and the onset of massive phosphorite deposition. We propose this entire suite of changes results from an increase in the size of the deep-water marine phosphorus reservoir, associated with rising sulfate concentrations and increased remineralization of organic P by sulfate-reducing bacteria. Simple mass balance calculations, constrained by modern anoxic basins, suggest that deep-water phosphate concentrations may have increased by an order of magnitude without any increase in the rate of P input from the continents. Strikingly, despite a major shift in phosphorite deposition, a new compilation of the phosphorus content of Neoproterozoic and early Paleozoic shows little secular change in median values, supporting the view that changes in remineralization and not erosional P fluxes were the principal drivers of observed shifts in phosphorite accumulation. The trigger for these changes may have been transient Neoproterozoic weathering events whose biogeochemical consequences were sustained by a set of positive feedbacks, mediated by the oxygen and sulfur cycles, that led to permanent state change in biogeochemical cycling, primary production, and biological diversity by the end of the Ediacaran Period.

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          A negative feedback mechanism for the long-term stabilization of Earth's surface temperature

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            Evolution of the global phosphorus cycle

            The macronutrient phosphorus is thought to limit primary productivity in the oceans on geological timescales. Although there has been a sustained effort to reconstruct the dynamics of the phosphorus cycle over the past 3.5 billion years, 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 oceans 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 history. 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 states, severe perturbations to Earth’s climate system, and the emergence of animals.
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              The rise of algae in Cryogenian oceans and the emergence of animals

              The transition from dominant bacterial to eukaryotic marine primary productivity was one of the most profound ecological revolutions in the Earth’s history, reorganizing the distribution of carbon and nutrients in the water column and increasing energy flow to higher trophic levels. But the causes and geological timing of this transition, as well as possible links with rising atmospheric oxygen levels and the evolution of animals, remain obscure. Here we present a molecular fossil record of eukaryotic steroids demonstrating that bacteria were the only notable primary producers in the oceans before the Cryogenian period (720–635 million years ago). Increasing steroid diversity and abundance marks the rapid rise of marine planktonic algae (Archaeplastida) in the narrow time interval between the Sturtian and Marinoan ‘snowball Earth’ glaciations, 659–645 million years ago. We propose that the incumbency of cyanobacteria was broken by a surge of nutrients supplied by the Sturtian deglaciation. The ‘Rise of Algae’ created food webs with more efficient nutrient and energy transfers, driving ecosystems towards larger and increasingly complex organisms. This effect is recorded by the concomitant appearance of biomarkers for sponges and predatory rhizarians, and the subsequent radiation of eumetazoans in the Ediacaran period.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                2 June 2020
                18 May 2020
                18 May 2020
                : 117
                : 22
                : 11961-11967
                Affiliations
                [1] aDepartment of Earth and Planetary Sciences, Harvard University , Cambridge, MA 20138;
                [2] bDepartment of Geological Sciences, Stanford University , Stanford, CA 94305;
                [3] cDepartment of Organismic and Evolutionary Biology, Harvard University , Cambridge, MA 20138
                Author notes
                1To whom correspondence may be addressed. Email: laakso@ 123456fas.harvard.edu or aknoll@ 123456oeb.harvard.edu .

                Contributed by Andrew H. Knoll, March 25, 2020 (sent for review September 26, 2019; reviewed by Kurt O. Konhauser and Lee R. Kump)

                Author contributions: T.A.L., D.T.J., and A.H.K. designed research; T.A.L., E.A.S., D.T.J., and A.H.K. performed research; T.A.L., E.A.S., D.T.J., and A.H.K. analyzed data; and T.A.L., E.A.S., D.T.J., and A.H.K. wrote the paper.

                Reviewers: K.O.K., University of Alberta; and L.R.K., Pennsylvania State University.

                Author information
                https://orcid.org/0000-0002-2755-8050
                https://orcid.org/0000-0002-2487-1084
                https://orcid.org/0000-0003-1308-8585
                Article
                201916738
                10.1073/pnas.1916738117
                7275700
                32424088
                4f892415-576a-4c48-9411-2199268ee809
                Copyright © 2020 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 7
                Categories
                Physical Sciences
                Earth, Atmospheric, and Planetary Sciences
                Biological Sciences
                Evolution

                ediacaran,biosphere,sulfate,phopshorus,phosphorite
                ediacaran, biosphere, sulfate, phopshorus, phosphorite

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