Abstract
Phosphorus (P) is critical to modern biochemical functions and can control ecosystem growth. It was presumably important as a reagent in prebiotic chemistry. However, on the early Earth, P sources may have consisted primarily of poorly soluble calcium phosphates, which may have rendered phosphate as a minimally available nutrient or reagent if these minerals were the sole source. Here, we review aqueous P availability on the early Earth (>2.5 Gyr ago), considering both mineral sources and geochemical sinks relevant to its solvation, and activation by abiotic and biological pathways. Phosphorus on Earth’s early surface would have been present as a mixture of phosphate minerals, as a minor element in silicate minerals, and in reactive, reduced phases from accreted dust, meteorites and asteroids. These P sources would have weathered and plausibly furnished the prebiotic Earth with abundant and potentially reactive P. After the origin of a biosphere, life evolved to draw on not just reactive available P sources, but also insoluble and unreactive sources. The rise of an ecosystem dependent on this element at some point forged a P-limited biosphere, with evolutionary stress forcing the efficient extraction and recycling of P from both abiotic and biotic sources and sinks.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Change history
22 May 2023
A Correction to this paper has been published: https://doi.org/10.1038/s41561-023-01209-z
References
Westheimer, F. H. Why nature chose phosphates. Science 235, 1173–1178 (1987).
Schroeder, G. K., Lad, C., Wyman, P., Williams, N. H. & Wolfenden, R. The time required for water attack at the phosphorus atom of simple phosphodiesters and of DNA. Proc. Natl Acad. Sci. USA 103, 4052–4055 (2006).
Dürr-Mayer, T. et al. The chemistry of branched condensed phosphates. Nat. Commun. 12, 5368 (2021).
Bowlin, M. Q. & Gray, M. J. Inorganic polyphosphate in host and microbe biology. Trends Microbiol. 29, 1013–1023 (2021).
Lang, C., Lago, J. & Pasek, M. A. in Handbook of Astrobiology (Ed. Kolb, V. M) 361–369 (CRC Press, 2018).
Pasek, M. A. in Prebiotic Chemistry and Chemical Evolution of Nucleic Acids (Ed. Menor-Salván, C.) 175–197 (Springer, 2018).
Goldford, J. E., Hartman, H., Smith, T. F. & Segrè, D. Remnants of an ancient metabolism without phosphate. Cell 168, 1126–1134.e1129 (2017).
Cafferty, B. J., Fialho, D. M., Khanam, J., Krishnamurthy, R. & Hud, N. V. Spontaneous formation and base pairing of plausible prebiotic nucleotides in water. Nat. Commun. 7, 11328 (2016).
Pasek, M. A. Thermodynamics of prebiotic phosphorylation. Chem. Rev. 120, 4690–4706 (2019).
Hao, J. et al. Cycling phosphorus on the Archean Earth: Part II. Phosphorus limitation on primary production in Archean ecosystems. Geochim. Cosmochim. Acta 280, 360–377 (2020).
Herschy, B. et al. Archean phosphorus liberation induced by iron redox geochemistry. Nat. Commun. 9, 1346 (2018).
Hess, B. L., Piazolo, S. & Harvey, J. Lightning strikes as a major facilitator of prebiotic phosphorus reduction on early Earth. Nat. Commun. 12, 1535 (2021).
Plane, J. M., Feng, W. & Douglas, K. M. Phosphorus chemistry in the Earth’s upper atmosphere. J. Geophys. Res. Space Phys. 126, e2021JA029881 (2021).
Lodders, K. Solar System abundances and condensation temperatures of the elements. Astrophys. J. 591, 1220 (2003).
Wood, B. J., Smythe, D. J. & Harrison, T. The condensation temperatures of the elements: a reappraisal. Am. Miner. 104, 844–856 (2019).
Mezger, K., Schönbächler, M. & Bouvier, A. Accretion of the Earth—missing components? Space Sci. Rev. 216, 27 (2020).
Righter, K., Pando, K., Danielson, L. & Lee, C.-T. Partitioning of Mo, P and other siderophile elements (Cu, Ga, Sn, Ni, Co, Cr, Mn, V, and W) between metal and silicate melt as a function of temperature and silicate melt composition. Earth Planet. Sci. Lett. 291, 1–9 (2010).
Gu, T., Stagno, V. & Fei, Y. Partition coefficient of phosphorus between liquid metal and silicate melt with implications for the Martian magma ocean. Phys. Earth Planet. Inter. 295, 106298 (2019).
Cox, G. M., Lyons, T. W., Mitchell, R. N., Hasterok, D. & Gard, M. Linking the rise of atmospheric oxygen to growth in the continental phosphorus inventory. Earth Planet Sci. Lett. 489, 28–36 (2018).
Pasek, M. A., Harnmeijer, J. P., Buick, R., Gull, M. & Atlas, Z. Evidence for reactive reduced phosphorus species in the early Archean ocean. Proc. Natl Acad. Sci. USA 110, 10089–10094 (2013).
Dhuime, B., Hawkesworth, C. J., Delavault, H. & Cawood, P. A. Rates of generation and destruction of the continental crust: implications for continental growth. Phil. Trans. R. Soc. A 376, 20170403 (2018).
Korenaga, J. Hadean geodynamics and the nature of early continental crust. Precambrian Res. 359, 106178 (2021).
McCoy-West, A. J. et al. Extensive crustal extraction in Earth’s early history inferred from molybdenum isotopes. Nat. Geosci. 12, 946–951 (2019).
Paytan, A. & McLaughlin, K. The oceanic phosphorus cycle. Chem. Rev. 107, 563–576 (2007).
Green, T. & Watson, E. Crystallization of apatite in natural magmas under high pressure, hydrous conditions, with particular reference to ‘orogenic’ rock series. Contrib. Mineral. Petrol. 79, 96–105 (1982).
Haggerty, S. E., Fung, A. T. & Burt, D. M. Apatite, phosphorus and titanium in eclogitic garnet from the upper mantle. Geophys. Res. Lett. 21, 1699–1702 (1994).
Walton, C. R. et al. Phosphorus mineral evolution and prebiotic chemistry: from minerals to microbes. Earth-Sci. Rev. 221, 103806 (2021).
Greber, N. D. et al. Titanium isotopic evidence for felsic crust and plate tectonics 3.5 billion years ago. Science 357, 1271–1274 (2017).
Greber, N. D. & Dauphas, N. The chemistry of fine-grained terrigenous sediments reveals a chemically evolved Paleoarchean emerged crust. Geochim. Cosmochim. Acta 255, 247–264 (2019).
Tang, M., Chen, K. & Rudnick, R. L. Archean upper crust transition from mafic to felsic marks the onset of plate tectonics. Science 351, 372–375 (2016).
Wilde, S. A., Valley, J. W., Peck, W. H. & Graham, C. M. Evidence from detrital zircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago. Nature 409, 175–178 (2001).
Zahnle, K., Schaefer, L. & Fegley, B. Earth’s earliest atmospheres. Cold Spring Harb. Perspect. Biol. https://doi.org/10.1101/cshperspect.a004895 (2010).
Javaux, E. J. Challenges in evidencing the earliest traces of life. Nature 572, 451–460 (2019).
Ward, L. M., Rasmussen, B. & Fischer, W. W. Primary productivity was limited by electron donors prior to the advent of oxygenic photosynthesis. J. Geophys. Res. Biogeosci. 124, 211–226 (2019).
Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242 (2009).
Liu, Z. et al. Harnessing chemical energy for the activation and joining of prebiotic building blocks. Nat. Chem. 12, 1023–1028 (2020).
Maguire, O. R., Smokers, I. B. A. & Huck, W. T. S. A physicochemical orthophosphate cycle via a kinetically stable thermodynamically activated intermediate enables mild prebiotic phosphorylations. Nat. Commun. 12, 5517 (2021).
Ritson, D. J., Mojzsis, S. J. & Sutherland, J. D. Supply of phosphate to early Earth by photogeochemistry after meteoritic weathering. Nat. Geosci. 13, 344–348 (2020).
Turner, A. M. et al. An interstellar synthesis of phosphorus oxoacids. Nat. Commun. 9, 3851 (2018).
Cooper, G. W., Onwo, W. M. & Cronin, J. R. Alkyl phosphonic acids and sulfonic acids in the Murchison meteorite. Geochim. Cosmochim. Acta 56, 4109–4115 (1992).
Budde, G., Burkhardt, C. & Kleine, T. Molybdenum isotopic evidence for the late accretion of outer Solar System material to Earth. Nat. Astron. 3, 736–741 (2019).
Gibard, C. et al. Geochemical sources and availability of amidophosphates on the early Earth. Angew. Chem. Int. Ed. 58, 8151–8155 (2019).
Gibard, C., Bhowmik, S., Karki, M., Kim, E.-K. & Krishnamurthy, R. Phosphorylation, oligomerization and self-assembly in water under potential prebiotic conditions. Nat. Chem. 10, 212–217 (2018).
Pasek, M. A., Gull, M. & Herschy, B. Phosphorylation on the early Earth. Chem. Geol. 110, 10089–10094 (2017).
Britvin, S. N. et al. Cyclophosphates, a new class of native phosphorus compounds, and some insights into prebiotic phosphorylation on early Earth. Geology 49, 382–386 (2021).
Pasek, M. A. Schreibersite on the early Earth: scenarios for prebiotic phosphorylation. Geosci. Front. 8, 329–335 (2017).
Kim, H.-J. & Benner, S. A. Abiotic synthesis of nucleoside 5′-triphosphates with nickel borate and cyclic trimetaphosphate (CTMP). Astrobiology 21, 298–306 (2021).
Cheng, C. et al. Phosphorylation of adenosine with trimetaphosphate under simulated prebiotic conditions. Orig. Life Evol. Biosph. 32, 219–224 (2002).
Akoopie, A., Arriola, J. T., Magde, D. & Müller, U. F. A GTP-synthesizing ribozyme selected by metabolic coupling to an RNA polymerase ribozyme. Sci. Adv. 7, eabj7487 (2021).
Omran, A., Abbatiello, J., Feng, T. & Pasek, M. A. Oxidative phosphorus chemistry perturbed by minerals. Life 12, 198 (2022).
Feng, T., Gull, M., Omran, A., Abbott-Lyon, H. & Pasek, M. A. Evolution of ephemeral phosphate minerals on planetary environments. ACS Earth Space Chem. 5, 1647–1656 (2021).
Marchi, S. et al. Widespread mixing and burial of Earth’s Hadean crust by asteroid impacts. Nature 511, 578–582 (2014).
White, A. K. & Metcalf, W. W. Microbial metabolism of reduced phosphorus compounds. Annu. Rev. Microbiol. 61, 379–400 (2007).
Markou, G., Vandamme, D. & Muylaert, K. Microalgal and cyanobacterial cultivation: the supply of nutrients. Water Res. 65, 186–202 (2014).
Wu, J., Sunda, W., Boyle, E. A. & Karl, D. M. Phosphate depletion in the western North Atlantic Ocean. Science 289, 759–762 (2000).
Hou, E. et al. Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat. Commun. 11, 637 (2020).
Ruttenberg, K. in Treatise on Geochemistry 2nd edn, Vol. 10, 499–558 (Elsevier, 2014).
Yang, K. & Metcalf, W. W. A new activity for an old enzyme: Escherichia coli bacterial alkaline phosphatase is a phosphite-dependent hydrogenase. Proc. Natl Acad. Sci. USA 101, 7919–7924 (2004).
Sebastian, M. & Ammerman, J. W. The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J. 3, 563–572 (2009).
Lidbury, I. D. et al. A widely distributed phosphate-insensitive phosphatase presents a route for rapid organophosphorus remineralization in the biosphere. Proc. Natl Acad. Sci. USA 119, e2118122119 (2022).
Dyhrman, S. T. et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439, 68–71 (2006).
Figueroa, I. A. & Coates, J. D. in Advances in Applied Microbiology Vol. 98 (eds Sariaslani, S. & Gadd, G. M.) 93–117 (Academic Press, 2017).
Metcalf, W. W. & Wolfe, R. S. Molecular genetic analysis of phosphite and hypophosphite oxidation by Pseudomonas stutzeri WM88. J. Bacteriol. 180, 5547–5558 (1998).
Schink, B. & Friedrich, M. Phosphite oxidation by sulphate reduction. Nature 406, 37 (2000).
Figueroa, I. A. et al. Metagenomics-guided analysis of microbial chemolithoautotrophic phosphite oxidation yields evidence of a seventh natural CO2 fixation pathway. Proc. Natl Acad. Sci. USA 115, E92–E101 (2018).
Ewens, S. D. et al. The diversity and evolution of microbial dissimilatory phosphite oxidation. Proc. Natl Acad. Sci. USA 118, e2020024118 (2021).
Mao, Z. et al. Phosphitispora fastidiosa gen. nov. sp. nov., a new dissimilatory phosphite-oxidizing anaerobic bacterium isolated from anaerobic sewage sludge. Int. J. Syst. Evol. Microbiol. 71, 005142 (2021).
Schwartz, A. W. Phosphorus in prebiotic chemistry. Phil. Trans. R. Soc. B 361, 1743–1749 (2006).
Jusino-Maldonado, M. et al. A global network model of abiotic phosphorus cycling on Earth through time. Sci. Rep. 12, 9348 (2022).
Hartmann, J., Moosdorf, N., Lauerwald, R., Hinderer, M. & West, A. J. Global chemical weathering and associated P-release—the role of lithology, temperature and soil properties. Chem. Geol. 363, 145–163 (2014).
Tostevin, R. & Mills, B. J. Reconciling proxy records and models of Earth’s oxygenation during the Neoproterozoic and Palaeozoic. Interface Focus 10, 20190137 (2020).
Kipp, M. A. & Stüeken, E. E. Biomass recycling and Earth’s early phosphorus cycle. Sci. Adv. 3, eaao4795 (2017).
Föllmi, K. The phosphorus cycle, phosphogenesis and marine phosphate-rich deposits. Earth-Sci. Rev. 40, 55–124 (1996).
Korenaga, J., Planavsky, N. J. & Evans, D. A. D. Global water cycle and the coevolution of the Earth’s interior and surface environment. Phil. Trans. R. Soc. A 375, 20150393 (2017).
Flament, N., Coltice, N. & Rey, P. F. The evolution of the 87Sr/86Sr of marine carbonates does not constrain continental growth. Precambrian Res. 229, 177–188 (2013).
Catling, D. C. & Zahnle, K. J. The Archean atmosphere. Sci. Adv. 6, eaax1420 (2020).
Hao, J., Knoll, A. H., Huang, F., Hazen, R. M. & Daniel, I. Cycling phosphorus on the Archean Earth: Part I. Continental weathering and riverine transport of phosphorus. Geochim. Cosmochim. Acta 273, 70–84 (2020).
Rasmussen, B., Muhling, J. R., Suvorova, A. & Fischer, W. W. Apatite nanoparticles in 3.46–2.46 Ga iron formations: evidence for phosphorus-rich hydrothermal plumes on early Earth. Geology 49, 647–651 (2021).
Syverson, D. D. et al. Nutrient supply to planetary biospheres from anoxic weathering of mafic oceanic crust. Geophys. Res. Lett. 48, e2021GL094442 (2021).
Pasek, M. A. & Lauretta, D. S. Aqueous corrosion of phosphide minerals from iron meteorites: a highly reactive source of prebiotic phosphorus on the surface of the early Earth. Astrobiology 5, 515–535 (2005).
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).
Planavsky, N. J. et al. The evolution of the marine phosphate reservoir. Nature 467, 1088–1090 (2010).
Reinhard, C. T. et al. Evolution of the global phosphorus cycle. Nature 541, 386–389 (2017).
Konhauser, K. O., Lalonde, S. V., Amskold, L. & Holland, H. D. Was there really an Archean phosphate crisis? Science 315, 1234–1234 (2007).
Tosca, N. J., Jiang, C. Z., Rasmussen, B. & Muhling, J. Products of the iron cycle on the early Earth. Free Radic. Biol. Med. 140, 138–153 (2019).
Johnson, B. R. et al. Phosphorus burial in ferruginous SiO2-rich Mesoproterozoic sediments. Geology 48, 92–96 (2020).
Derry, L. A. Causes and consequences of mid-Proterozoic anoxia. Geophys. Res. Lett. 42, 8538–8546 (2015).
Brady, M. P., Tostevin, R. & Tosca, N. J. Marine phosphate availability and the chemical origins of life on Earth. Nat. Commun. 13, 5162 (2022).
Ingalls, M., Grotzinger, J. P., Present, T., Rasmussen, B. & Fischer, W. W. Carbonate-associated phosphate (CAP) indicates elevated phosphate availability in Neoarchean shallow marine environments. Geophys. Res. Lett. 49, e2022GL098100 (2022).
Zhao, M., Zhang, S., Tarhan, L. G., Reinhard, C. T. & Planavsky, N. The role of calcium in regulating marine phosphorus burial and atmospheric oxygenation. Nat. Commun. 11, 2232 (2020).
Crockford, P. & Halevy, I. Questioning the paradigm of a phosphate‐limited Archean biosphere. Geophys. Res. Lett. 49, e2022GL099818 (2022).
Toner, J. D. & Catling, D. C. A carbonate-rich lake solution to the phosphate problem of the origin of life. Proc. Natl Acad. Sci. USA 117, 883–888 (2020).
Burcar, B. et al. Darwin’s warm little pond: a one‐pot reaction for prebiotic phosphorylation and the mobilization of phosphate from minerals in a urea‐based solvent. Angew. Chem. Int. Ed. 55, 13249–13253 (2016).
Damer, B. & Deamer, D. The hot spring hypothesis for an origin of life. Astrobiology 20, 429–452 (2020).
Jordan, S. F. et al. Promotion of protocell self-assembly from mixed amphiphiles at the origin of life. Nat. Ecol. Evol. 3, 1705–1714 (2019).
Herschy, B. et al. An origin-of-life reactor to simulate alkaline hydrothermal vents. J. Mol. Evol. 79, 213–227 (2014).
Kim, H. J. et al. Evaporite borate‐containing mineral ensembles make phosphate available and regiospecifically phosphorylate ribonucleosides: borate as a multifaceted problem solver in prebiotic chemistry. Angew. Chem. Int. Ed. 128, 16048–16052 (2016).
Deal, A. M., Rapf, R. J. & Vaida, V. Water–air interfaces as environments to address the water paradox in prebiotic chemistry: a physical chemistry perspective. J. Phys. Chem. A 125, 4929–4942 (2021).
Cornell, C. E. et al. Prebiotic amino acids bind to and stabilize prebiotic fatty acid membranes. Proc. Natl Acad. Sci. USA 116, 17239–17244 (2019).
Krijt, S. et al. Chemical habitability: supply and retention of life’s essential elements during planet formation. Preprint at https://arxiv.org/abs/2203.10056 (2022).
Kipp, M. A. & Stueken, E. E. Biomass recycling and Earth’s early phosphorus cycle. Sci. Adv. 3, eaao4795 (2017).
Hudek, L., Premachandra, D., Webster, W. & Bräu, L. Role of phosphate transport system component PstB1 in phosphate internalization by Nostoc punctiforme. Appl. Environ. Microbiol. 82, 6344–6356 (2016).
Lis, H., Weiner, T., Pitt, F. D., Keren, N. & Angert, A. Phosphate uptake by cyanobacteria is associated with kinetic fractionation of phosphate oxygen isotopes. ACS Earth Space Chem. 3, 233–239 (2018).
Alori, E. T., Glick, B. R. & Babalola, O. O. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front. Microbiol. 8, 971 (2017).
Blake, R. E., Chang, S. J. & Lepland, A. Phosphate oxygen isotopic evidence for a temperate and biologically active Archaean ocean. Nature 464, 1029–1032 (2010).
Jusino-Maldonado, M. et al. A global network model of abiotic phosphorus cycling on Earth through time. Sci. Rep. 12, 9348 (2022).
Anderson, L. A. & Sarmiento, J. L. Global ocean phosphate and oxygen simulations. Glob. Biogeochem. Cycles 9, 621–636 (1995).
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).
Kadoya, S., Catling, D. C., Nicklas, R. W., Puchtel, I. S. & Anbar, A. D. Mantle data imply a decline of oxidizable volcanic gases could have triggered the Great Oxidation. Nat. Commun. 11, 2774 (2020).
Krissansen-Totton, J. & Catling, D. C. Constraining climate sensitivity and continental versus seafloor weathering using an inverse geological carbon cycle model. Nat. Commun. 8, 15423 (2017).
Acknowledgements
C.R.W. acknowledges the NERC and UKRI for support through a NERC DTP studentship, grant number NE/L002507/1. S.E. and J.D.C. acknowledge support from the US DOE, grant number DE-SC0020156. C.R.W. acknowledges funding from the Leverhulme Centre for Life in the Universe and Institute for Life and Planets in the Universe (grant title: ‘Did cosmic dust fertilize prebiotic chemistry?’). Funding for research on phosphorus redox cycling was generously provided to J.D.C. by the EBI–Shell Research Program. S.E. was supported by the EBI–Shell Directors’ fellowship. C.R. acknowledges support from the NASA Interdisciplinary Consortia for Astrobiology Research (ICAR) and the NASA Exobiology Program. J.H. acknowledges support from the Strategic Priority Research Program of Chinese Academy of Sciences (XDB 41000000), National Key R&D Program of China (2021YFA0718200), CAS Hundred-Talents Program and CIFAR Azrieli Global Scholarship. M.A.P. was supported by the NASA Exobiology Program (80NSSCC18K1288 and 80NSSC22K0509).
Author information
Authors and Affiliations
Contributions
C.R.W., J.H., S.E., J.D.C. and M.A.P. planned and wrote the paper. Data analysis was performed by all authors, who also edited the text.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Geoscience thanks Miquela Ingalls, Ziwei Liu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Rebecca Neely, in collaboration with the Nature Geoscience team.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Information
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Walton, C.R., Ewens, S., Coates, J.D. et al. Phosphorus availability on the early Earth and the impacts of life. Nat. Geosci. 16, 399–409 (2023). https://doi.org/10.1038/s41561-023-01167-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41561-023-01167-6
- Springer Nature Limited
This article is cited by
-
Co‐evolution of early Earth environments and microbial life
Nature Reviews Microbiology (2024)
-
Timing the evolution of phosphorus-cycling enzymes through geological time using phylogenomics
Nature Communications (2024)
-
The combined effect of root morphological and resistance traits alleviated the growth limitations of Pinus massoniana seedlings under low phosphorus conditions
Plant and Soil (2024)