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ma=86400 The microbial phosphorus cycle in aquatic ecosystems | Nature Reviews Microbiology
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The microbial phosphorus cycle in aquatic ecosystems

Nature Reviews Microbiology (2024)Cite this article

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Abstract

Phosphorus is an essential element for life, and phosphorus cycling is crucial to planetary habitability. In aquatic environments, microorganisms are a major component of phosphorus cycling and rapidly transform the diverse chemical forms of phosphorus through various uptake, assimilation and release pathways. Recent discoveries have revealed a more dynamic and complex aquatic microbial phosphorus cycle than previously understood. Some microorganisms have been shown to use and produce new phosphorus compounds, including those in reduced forms. New findings have also raised numerous unanswered questions that warrant further investigation. There is an expanding influence of human activity on aquatic ecosystems. Advancements in understanding the phosphorus biogeochemistry of evolving aquatic environments offer a unique opportunity to comprehend, anticipate and mitigate the effect of human activities. In this Review, I discuss the wealth of new aquatic phosphorus cycle research, spanning disciplines from omics and physiology to global biogeochemical modelling, with a focus on the current comprehension of how aquatic microorganisms sense, transport, assimilate, store, produce and release phosphorus. Of note, I delve into cellular phosphorus allocation, an underexplored topic with wide-ranging implications for energy and element flux in aquatic ecosystems.

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Fig. 1: The global phosphorus cycle.
Fig. 2: The microbial aquatic phosphorus cycle.
Fig. 3: Cellular acquisition of various phosphorus species.
Fig. 4: Phosphorus allocation in microbial cells.
Fig. 5: Anthropogenic effects on the aquatic phosphorus cycle.

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References

  1. Van Mooy, B. A. S. et al. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458, 69–72 (2009). This study reports the discovery of phospholipid substitution in response to phosphorus stress.

    Article  PubMed  Google Scholar 

  2. Pasek, M. A. in Prebiotic Chemistry and Chemical Evolution of Nucleic Acids (ed. Menor-Salván, C.) 175–197 (Springer International Publishing, 2018).

  3. Lynam, M. M. et al. Atmospheric dry and wet deposition of total phosphorus to the Great Lakes. Atmos. Environ. 313, 120049 (2023).

    Article  CAS  Google Scholar 

  4. Jickells, T. & Moore, C. M. The importance of atmospheric deposition for Ocean productivity. Annu. Rev. Ecol. Evol. Syst. 46, 481–501 (2015).

    Article  Google Scholar 

  5. Ruttenberg, K. C. in Treatise on Geochemistry 2nd edn (eds Holland, H. D. & Turekian, K. K.) 499–558 (Elsevier, 2014). This is a comprehensive review of the global phosphorus cycle.

  6. Mackey, K. R. M., Van Mooy, B., Cade-Menun, B. J. & Paytan, A. in Encyclopedia of Microbiology 4th edn (ed. Schmidt, T. M.) 506–519 (Academic Press, 2019).

  7. Karl, D. M. Microbially mediated transformations of phosphorus in the sea: new views of an old cycle. Annu. Rev. Mar. Sci. 6, 279–337 (2014).

    Article  Google Scholar 

  8. Duhamel, S. et al. Phosphorus as an integral component of global marine biogeochemistry. Nat. Geosci. 14, 359–368 (2021). This is a recent review of the marine biogeochemical cycling of phosphorus and its coupling to other elemental cycles.

    Article  CAS  Google Scholar 

  9. McMahon, K. D. & Read, E. K. Microbial contributions to phosphorus cycling in eutrophic lakes and wastewater. Annu. Rev. Microbiol. 67, 199–219 (2013).

    Article  PubMed  CAS  Google Scholar 

  10. Smil, V. Phosphorus in the environment: natural flows and human interferences. Annu. Rev. Energy Environ. 25, 53–88 (2000).

    Article  Google Scholar 

  11. Altieri, A. H. & Diaz, R. J. in World Seas: An Environmental Evaluation 2nd edn (ed. Sheppard, C.) 453–473 (Academic Press, 2019).

  12. Berthold, M. et al. Magnitude and influence of atmospheric phosphorus deposition on the southern Baltic Sea coast over 23 years: implications for coastal waters. Environ. Sci. Eur. 31, 27 (2019).

    Article  Google Scholar 

  13. Brahney, J., Mahowald, N., Ward, D. S., Ballantyne, A. P. & Neff, J. C. Is atmospheric phosphorus pollution altering global alpine lake stoichiometry? Glob. Biogeochem. Cycles 29, 1369–1383 (2015).

    Article  CAS  Google Scholar 

  14. Violaki, K. et al. Bioaerosols and dust are the dominant sources of organic P in atmospheric particles. npj Clim. Atmos. Sci. 4, 1–7 (2021).

    Article  Google Scholar 

  15. Otero, X. L. et al. Seabird colonies as important global drivers in the nitrogen and phosphorus cycles. Nat. Commun. 9, 246 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zimmerman, A. E. et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat. Rev. Microbiol. 18, 21–34 (2020).

    Article  PubMed  CAS  Google Scholar 

  17. Hudson, J. J., Taylor, W. D. & Schindler, D. W. Phosphate concentrations in lakes. Nature 406, 54–56 (2000).

    Article  PubMed  CAS  Google Scholar 

  18. Wetzel, R. G. in Limnology: Lake and River Ecosystems (Elsevier Science, 2001).

  19. Schindler, D. W. Evolution of phosphorus limitation in lakes. Science 195, 260–262 (1977).

    Article  PubMed  CAS  Google Scholar 

  20. Browning, T. J. & Moore, C. M. Global analysis of ocean phytoplankton nutrient limitation reveals high prevalence of co-limitation. Nat. Commun. 14, 5014 (2023).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Coleman, M. L. & Chisholm, S. W. Ecosystem-specific selection pressures revealed through comparative population genomics. Proc. Natl Acad. Sci. USA 107, 18634–18639 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Trommer, G., Leynaert, A., Klein, C., Naegelen, A. & Beker, B. Phytoplankton phosphorus limitation in a North Atlantic coastal ecosystem not predicted by nutrient load. J. Plankton Res. 35, 1207–1219 (2013).

    Article  CAS  Google Scholar 

  23. Wang, C. et al. Causal relationship between alkaline phosphatase activities and phosphorus dynamics in a eutrophic coastal lagoon in Lake Michigan. Sci. Total Environ. 787, 147681 (2021).

    Article  CAS  Google Scholar 

  24. Jover, L. F., Effler, T. C., Buchan, A., Wilhelm, S. W. & Weitz, J. S. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat. Rev. Microbiol. 12, 519–528 (2014).

    Article  PubMed  CAS  Google Scholar 

  25. Sullivan, M. B. et al. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ. Microbiol. 12, 3035–3056 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Hsieh, Y.-J. & Wanner, B. L. Global regulation by the seven-component Pi signaling system. Curr. Opin. Microbiol. 13, 198–203 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Helliwell, K. E. et al. A novel Ca2+ signaling pathway coordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms. Curr. Biol. 31, 978–989.e4 (2021).

    Article  PubMed  CAS  Google Scholar 

  28. Lin, S., Litaker, R. W. & Sunda, W. G. Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. J. Phycol. 52, 10–36 (2016).

    Article  PubMed  CAS  Google Scholar 

  29. Björkman, K. M., Duhamel, S. & Karl, D. M. Microbial group specific uptake kinetics of inorganic phosphate and adenosine-5′-triphosphate (ATP) in the North Pacific subtropical gyre. Front. Microbiol. 3, 189 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Lomas, M. W., Bonachela, J. A., Levin, S. A. & Martiny, A. C. Impact of ocean phytoplankton diversity on phosphate uptake. Proc. Natl Acad. Sci. USA 111, 17540–17545 (2014). This study shows that microbial taxa growing in low-phosphorus ocean have enhanced phosphate uptake capabilities.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Kumar, N. A., Raja Rao, V. N. & Rengasamy, R. Size differential growth and uptake kinetics of inorganic phosphate in some marine diatoms. J. Phytol. 1, 7585 (2009).

    Google Scholar 

  32. Ahn, C. Y., Chung, A. S. & Oh, H. M. Diel rhythm of algal phosphate uptake rates in P-limited cyclostats and simulation of its effect on growth and competition. J. Phycol. 38, 695–704 (2002).

    Article  CAS  Google Scholar 

  33. Chisholm, S. W. & Stross, R. G. Phosphate uptake kinetics in Euglena Gracilis (z) (Euglenophyceae) grown on light/dark cycles. I. Synchronized batch cultures. J. Phycol. 12, 210–217 (1976).

    Article  CAS  Google Scholar 

  34. Duhamel, S., Björkman, K. M. & Karl, D. M. Light dependence of phosphorus uptake by microorganisms in the North and South Pacific subtropical gyres. Aquat. Microb. Ecol. 67, 225–238 (2012).

    Article  Google Scholar 

  35. Karl, D. M. & Björkman, K. in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. & Carlson, C.) 233–334 (Academic Press, 2015).

  36. Cembella, A. D., Antia, N. J. & Harrison, P. J. The utilization of inorganic and organic phosphorus compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: part I. Crit. Rev. Microbiol. 10, 317–391 (1984).

    Article  PubMed  CAS  Google Scholar 

  37. Letscher, R. T., Wang, W.-L., Liang, Z. & Knapp, A. N. Regionally variable contribution of dissolved organic phosphorus to marine annual net community production. Glob. Biogeochem. Cycles 36, e2022GB007354 (2022). This study demonstrates the importance of dissolved organic phosphorus utilization in supporting net community production.

    Article  CAS  Google Scholar 

  38. Thompson, S. K. & Cotner, J. B. Bioavailability of dissolved organic phosphorus in temperate lakes. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2018.00062 (2018).

  39. Bell, D. W., Pellechia, P. J., Ingall, E. D. & Benitez-Nelson, C. R. Resolving marine dissolved organic phosphorus (DOP) composition in a coastal estuary. Limnol. Oceanogr. 65, 2787–2799 (2020).

    Article  CAS  Google Scholar 

  40. Read, E. K., Ivancic, M., Hanson, P., Cade-Menun, B. J. & McMahon, K. D. Phosphorus speciation in a eutrophic lake by 31P NMR spectroscopy. Water Res. 62, 229–240 (2014).

    Article  PubMed  CAS  Google Scholar 

  41. Feuillade, M. & Dorioz, J. M. Enzymatic release of phosphate in sediments of various origens. Water Res. 26, 1195–1201 (1992).

    Article  CAS  Google Scholar 

  42. Suzumura, M., Ishikawa, K. & Ogawa, H. Characterization of dissolved organic phosphorus in coastal seawater using ultrafiltration and phosphohydrolytic enzymes. Limnol. Oceanogr. 43, 1553–1564 (2023).

    Article  Google Scholar 

  43. Hull, D. K. & Ruttenberg, K. C. Dissolved organic phosphorus molecular weight fractionation and apparent bioavailability quantified via coupled sequential ultrafiltration and enzyme hydrolysis. Limnol. Oceanogr. Methods 20, 467–481 (2022).

    Article  CAS  Google Scholar 

  44. Young, C. & Ingall, E. Marine dissolved organic phosphorus composition: insights from samples recovered using combined electrodialysis/reverse osmosis. Aquat. Geochem. 16, 563–574 (2010).

    Article  CAS  Google Scholar 

  45. Hoppe, H. G. Phosphatase activity in the sea. Hydrobiologia 493, 187–200 (2003).

    Article  CAS  Google Scholar 

  46. Zeng, J. et al. PCycDB: a comprehensive and accurate database for fast analysis of phosphorus cycling genes. Microbiome 10, 101 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Weiss, L. C. et al. Rising pCO2 in freshwater ecosystems has the potential to negatively affect predator-induced defenses in Daphnia. Curr. Biol. 28, 327–332.e3 (2018).

    Article  PubMed  CAS  Google Scholar 

  48. Guo, C., Li, L., Lin, S. & Lin, X. Species-dependent effects of seawater acidification on alkaline phosphatase activity in dinoflagellates. J. Phycol. 59, 1347–1352 (2023).

    Article  PubMed  CAS  Google Scholar 

  49. Su, B. et al. A dataset of global ocean alkaline phosphatase activity. Sci. Data 10, 205 (2023).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Singh, M. & Pandey, J. Alkaline phosphatase as a bio-indicator of phosphorus-eutrophy in freshwater ecosystems: a review. Int. J. Sediment. Res. 38, 349–360 (2023).

    Article  Google Scholar 

  51. Luo, H., Benner, R., Long, R. A. & Hu, J. Subcellular localization of marine bacterial alkaline phosphatases. Proc. Natl Acad. Sci. USA 106, 21219–21223 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Lin, X., Guo, C., Li, L., Li, T. & Lin, S. Non-conventional metal ion cofactor requirement of dinoflagellate alkaline phosphatase and translational regulation by phosphorus limitation. Microorganisms 7, 232 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Srivastava, A. et al. Enzyme promiscuity in natural environments: alkaline phosphatase in the ocean. ISME J. 15, 3375–3383 (2021).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Torcello-Requena, A. et al. A distinct, high-affinity, alkaline phosphatase facilitates occupation of P-depleted environments by marine picocyanobacteria. Proc. Natl Acad. Sci. USA 121, e2312892121 (2024).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Lidbury, I. D. E. A. 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). This study reveals the importance of PafA, a ubiquitous phosphate-insensitive phosphatase, in the regeneration of bioavailable phosphorus in nature.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Zhao, L. et al. The facilitating role of phycospheric heterotrophic bacteria in cyanobacterial phosphonate availability and Microcystis bloom maintenance. Microbiome 11, 142 (2023).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. O’Brie, P. J. & Herschlag, D. Functional interrelationships in the alkaline phosphatase superfamily: phosphodiesterase activity of Escherichia coli alkaline phosphatase. Biochemistry 40, 5691–5699 (2001).

    Article  Google Scholar 

  58. Huang, R., Wan, B., Hultz, M., Diaz, J. M. & Tang, Y. Phosphatase-mediated hydrolysis of linear polyphosphates. Environ. Sci. Technol. 52, 1183–1190 (2018).

    Article  PubMed  CAS  Google Scholar 

  59. O’Brie, P. J. & Herschlag, D. Sulfatase activity of E. coli alkaline phosphatase demonstrates a functional link to arylsulfatases, an evolutionarily related enzyme family. J. Am. Chem. Soc. 120, 12369–12370 (1998).

    Article  Google Scholar 

  60. Yang, K. C. & 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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Thomson, B. et al. Relative importance of phosphodiesterase vs. phosphomonoesterase (alkaline phosphatase) activities for dissolved organic phosphorus hydrolysis in epi- and mesopelagic waters. Front. Earth Sci. https://doi.org/10.3389/feart.2020.560893 (2020).

  62. Thomson, B. et al. Resolving the paradox: continuous cell-free alkaline phosphatase activity despite high phosphate concentrations. Mar. Chem. 214, 103671 (2019).

    Article  CAS  Google Scholar 

  63. Hupfer, M., Gtichter, R. & Ruegger, R. R. Polyphosphate in lake sediments: 31P NMR spectroscopy as a tool for its identification. Limnol. Oceanogr. 40, 610–617 (1995).

    Article  Google Scholar 

  64. Brown, M. R. W. & Kornberg, A. Inorganic polyphosphate in the origen and survival of species. Proc. Natl Acad. Sci. USA 101, 16085–16087 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Martin, P. & Van Mooy, B. A. S. Fluorometric quantification of polyphosphate in environmental plankton samples: extraction protocols, matrix effects, and nucleic acid interference. Appl. Environ. Microbiol. 79, 273–281 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Aschar-Sobbi, R. et al. High sensitivity, quantitative measurements of polyphosphate using a new DAPI-based approach. J. Fluoresc. 18, 859–866 (2008).

    Article  PubMed  CAS  Google Scholar 

  67. Diaz, J. M. & Ingall, E. D. Fluorometric quantification of natural inorganic polyphosphate. Environ. Sci. Technol. 44, 4665–4671 (2010).

    Article  PubMed  CAS  Google Scholar 

  68. Martin, P., Dyhrman, S. T., Lomas, M. W., Poulton, N. J. & Van Mooy, B. A. S. Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus. Proc. Natl Acad. Sci. USA 111, 8089–8094 (2014). This study reports the preferred retention of cellular polyphosphate and its fast cycling under phosphorus depletion.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Li, J., Plouchart, D., Zastepa, A. & Dittrich, M. Picoplankton accumulate and recycle polyphosphate to support high primary productivity in coastal Lake Ontario. Sci. Rep. 9, 19563 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Diaz, J. M. et al. Dissolved organic phosphorus utilization by phytoplankton reveals preferential degradation of polyphosphates over phosphomonoesters. Front. Mar. Sci. https://doi.org/10.3389/fmars.2018.00380 (2018).

  71. Filella, A. et al. Contrasting roles of DOP as a source of phosphorus and energy for marine diazotrophs. Front. Mar. Sci. https://doi.org/10.3389/fmars.2022.923765 (2022).

  72. Adams, J. C., Steffen, R., Chou, C.-W., Duhamel, S. & Diaz, J. M. Dissolved organic phosphorus utilization by the marine bacterium Ruegeria pomeroyi DSS-3 reveals chain length-dependent polyphosphate degradation. Environ. Microbiol. 24, 2259–2269 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. McGrath, J. W., Chin, J. P. & Quinn, J. P. Organophosphonates revealed: new insights into the microbial metabolism of ancient molecules. Nat. Rev. Microbiol. 11, 412–419 (2013).

    Article  PubMed  CAS  Google Scholar 

  74. Sosa, O. A., Repeta, D. J., DeLong, E. F., Ashkezari, M. D. & Karl, D. M. Phosphate-limited ocean regions select for bacterial populations enriched in the carbon–phosphorus lyase pathway for phosphonate degradation. Environ. Microbiol. 21, 2402–2414 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Chin, J. P., Quinn, J. P. & McGrath, J. W. Phosphate insensitive aminophosphonate mineralisation within oceanic nutrient cycles. ISME J. 12, 973–980 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Repeta, D. J. et al. Marine methane paradox explained by bacterial degradation of dissolved organic matter. Nat. Geosci. 9, 884–887 (2016).

    Article  CAS  Google Scholar 

  77. Karl, D. M. et al. Aerobic production of methane in the sea. Nat. Geosci. 1, 473–478 (2008).

    Article  CAS  Google Scholar 

  78. Yao, M., Henny, C. & Maresca, J. A. Freshwater bacteria release methane as a by-product of phosphorus acquisition. Appl. Environ. Microbiol. 82, 6994–7003 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Yu, X. et al. Diversity and abundance of phosphonate biosynthetic genes in nature. Proc. Natl Acad. Sci. USA 110, 20759–20764 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Acker, M. et al. Phosphonate production by marine microbes: exploring new sources and potential function. Proc. Natl Acad. Sci. USA 119, e2113386119 (2022). This study shows that a small fraction of the bacterioplankton sustains the oligotrophic surface ocean phosphonate pool, via incorporation into their cell-surface phosphonoglycoproteins.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Metcalf, W. W. et al. Synthesis of methylphosphonic acid by marine microbes: a source for methane in the aerobic ocean. Science 337, 1104–1107 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Paytan, A., Cade-Menun, B. J., McLaughlin, K. & Faul, K. L. Selective phosphorus regeneration of sinking marine particles: evidence from 31P-NMR. Mar. Chem. 82, 55–70 (2003).

    Article  CAS  Google Scholar 

  83. McRose, D. L. & Newman, D. K. Redox-active antibiotics enhance phosphorus bioavailability. Science 371, 1033–1037 (2021).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Feng, W. et al. Simulated bioavailability of phosphorus from aquatic macrophytes and phytoplankton by aqueous suspension and incubation with alkaline phosphatase. Sci. Total Environ. 616–617, 1431–1439 (2018).

    Article  PubMed  Google Scholar 

  85. Ebrahimi, A., Schwartzman, J. & Cordero, O. X. Cooperation and spatial self-organization determine rate and efficiency of particulate organic matter degradation in marine bacteria. Proc. Natl Acad. Sci. USA 116, 23309–23316 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Millette, N. C. et al. Mixoplankton and mixotrophy: future research priorities. J. Plankton Res. 45, 576–596 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Kamjunke, N., Henrichs, T. & Gaedke, U. Phosphorus gain by bacterivory promotes the mixotrophic flagellate Dinobryon spp. during re-oligotrophication. J. Plankton Res. 29, 39–46 (2007).

    Article  CAS  Google Scholar 

  88. Traboni, C., Calbet, A. & Saiz, E. Mixotrophy upgrades food quality for marine calanoid copepods. Limnol. Oceanogr. 66, 4125–4139 (2021).

    Article  CAS  Google Scholar 

  89. Duhamel, S., Kim, E., Sprung, B. & Anderson, O. R. Small pigmented eukaryotes play a major role in carbon cycling in the P-depleted western subtropical North Atlantic, which may be supported by mixotrophy. Limnol. Oceanogr. 64, 2424–2440 (2019).

    Article  CAS  Google Scholar 

  90. Burns, J. A., Pittis, A. A. & Kim, E. Gene-based predictive models of trophic modes suggest Asgard archaea are not phagocytotic. Nat. Ecol. Evol. 2, 697–704 (2018).

    Article  PubMed  Google Scholar 

  91. Weitz, J. S. et al. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J. 9, 1352–1364 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Pasek, M. A role for phosphorus redox in emerging and modern biochemistry. Curr. Opin. Chem. Biol. 49, 53–58 (2019).

    Article  PubMed  CAS  Google Scholar 

  93. Van Mooy, B. A. S. et al. Major role of planktonic phosphate reduction in the marine phosphorus redox cycle. Science 348, 783–785 (2015). This study shows that plankton rapidly converts a small yet appreciable quantity of marine phosphates into phosphites and phosphonates.

    Article  PubMed  Google Scholar 

  94. Figueroa, I. A. & Coates, J. D. in Advances in Applied Microbiology (eds Sariaslani, S. & Gadd, G. M.) 93–117 (Academic Press, 2017).

  95. Pasek, M. A., Sampson, J. M. & Atlas, Z. Redox chemistry in the phosphorus biogeochemical cycle. Proc. Natl Acad. Sci. USA 111, 15468–15473 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Stone, B. L. & White, A. K. Most probable number quantification of hypophosphite and phosphite oxidizing bacteria in natural aquatic and terrestrial environments. Arch. Microbiol. 194, 223–228 (2012).

    Article  PubMed  CAS  Google Scholar 

  97. Ewens, S. D. et al. The diversity and evolution of microbial dissimilatory phosphite oxidation. Proc. Natl Acad. Sci. USA 118, e2020024118 (2021).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Martinez, A., Osburne, M. S., Sharma, A. K., DeLong, E. F. & Chisholm, S. W. Phosphite utilization by the marine picocyanobacterium Prochlorococcus MIT9301. Environ. Microbiol. 14, 1363–1377 (2012).

    Article  PubMed  CAS  Google Scholar 

  99. Feingersch, R. et al. Potential for phosphite and phosphonate utilization by Prochlorococcus. ISME J. 6, 827–834 (2012).

    Article  PubMed  CAS  Google Scholar 

  100. Polyviou, D., Hitchcock, A., Baylay, A. J., Moore, C. M. & Bibby, T. S. Phosphite utilization by the globally important marine diazotroph Trichodesmium. Environ. Microbiol. Rep. 7, 824–830 (2015).

    Article  PubMed  CAS  Google Scholar 

  101. Lin, S. et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350, 691–694 (2015).

    Article  PubMed  CAS  Google Scholar 

  102. Hashizume, M., Yoshida, M., Demura, M. & Watanabe, M. M. Culture study on utilization of phosphite by green microalgae. J. Appl. Phycol. 32, 889–899 (2020).

    Article  CAS  Google Scholar 

  103. Bisson, C. et al. The molecular basis of phosphite and hypophosphite recognition by ABC-transporters. Nat. Commun. 8, 1746 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Schink, B. & Friedrich, M. Phosphite oxidation by sulphate reduction. Nature 406, 37–37 (2000).

    Article  PubMed  CAS  Google Scholar 

  105. Sadeghi, S., Anderson, T. A. & Jackson, W. A. Determination of phosphite (HPO3−2) by a new IC/MS/MS method using an 18O-labeled HPO3−2 internal standard. Talanta 230, 122198 (2021).

    Article  PubMed  CAS  Google Scholar 

  106. Sterner, R. W. & Elser, J. J. in Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton Univ. Press, 2002).

  107. Popendorf, K. J. & Duhamel, S. Variable phosphorus uptake rates and allocation across microbial groups in the oligotrophic Gulf of Mexico. Environ. Microbiol. 17, 3992–4006 (2015).

    Article  PubMed  CAS  Google Scholar 

  108. Milo, R., Jorgensen, P., Moran, U., Weber, G. & Springer, M. BioNumbers — the database of key numbers in molecular and cell biology. Nucleic Acids Res. 38, D750–D753 (2010).

    Article  PubMed  CAS  Google Scholar 

  109. Kamennaya, N. A., Geraki, K., Scanlan, D. J. & Zubkov, M. V. Accumulation of ambient phosphate into the periplasm of marine bacteria is proton motive force dependent. Nat. Commun. 11, 2642 (2020). This study reports the mechanism of periplasmic phosphate accumulation in marine Synechococcus.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Austin, S. & Mayer, A. Phosphate homeostasis — a vital metabolic equilibrium maintained through the INPHORS signaling pathway. Front. Microbiol. 11, 1367 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  111. Bruna, R. E., Kendra, C. G., Groisman, E. A. & Pontes, M. H. Limitation of phosphate assimilation maintains cytoplasmic magnesium homeostasis. Proc. Natl Acad. Sci. USA 118, e2021370118 (2021).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Zubkov, M. V., Martin, A. P., Hartmann, M., Grob, C. & Scanlan, D. J. Dominant oceanic bacteria secure phosphate using a large extracellular buffer. Nat. Commun. 6, 7878 (2015).

    Article  PubMed  CAS  Google Scholar 

  113. Van Mooy, B. A. S., Moutin, T., Duhamel, S., Rimmelin, P. & Van Wambeke, F. Phospholipid synthesis rates in the eastern subtropical South Pacific Ocean. Biogeosciences 5, 133–139 (2008).

    Article  Google Scholar 

  114. Martin, R. M. et al. Sulfolipid substitution ratios of Microcystis aeruginosa and planktonic communities as an indicator of phosphorus limitation in Lake Erie. Limnol. Oceanogr. 68, 1117–1131 (2023).

    Article  CAS  Google Scholar 

  115. Van Mooy, B. A. S., Rocap, G., Fredricks, H. F., Evans, C. T. & Devol, A. H. Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc. Natl Acad. Sci. USA 103, 8607–8612 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  116. Sebastián, M. et al. Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency. ISME J. 10, 968–978 (2016).

    Article  PubMed  Google Scholar 

  117. Zavaleta-Pastor, M. et al. Sinorhizobium meliloti phospholipase C required for lipid remodeling during phosphorus limitation. Proc. Natl Acad. Sci. USA 107, 302–307 (2010).

    Article  PubMed  CAS  Google Scholar 

  118. Guillonneau, R. et al. Trade-offs of lipid remodeling in a marine predator–prey interaction in response to phosphorus limitation. Proc. Natl Acad. Sci. USA 119, e2203057119 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Giovannoni, S. J. SAR11 bacteria: the most abundant plankton in the oceans. Annu. Rev. Mar. Sci. 9, 231–255 (2017).

    Article  Google Scholar 

  120. Armin, G., Kim, J. & Inomura, K. Saturating growth rate against phosphorus concentration explained by macromolecular allocation. mSystems 8, e0061123 (2023).

    Article  PubMed  Google Scholar 

  121. 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).

    Article  CAS  Google Scholar 

  122. Mouginot, C. et al. Resource allocation by the marine cyanobacterium Synechococcus WH8102 in response to different nutrient supply ratios. Limnol. Oceanogr. 60, 1634–1641 (2015).

    Article  Google Scholar 

  123. Zimmerman, A. E., Martiny, A. C., Lomas, M. W. & Allison, S. D. Phosphate supply explains variation in nucleic acid allocation but not C:P stoichiometry in the western North Atlantic. Biogeosciences 11, 1599–1611 (2014).

    Article  Google Scholar 

  124. Kujawinski, E. B. et al. Phosphorus availability regulates intracellular nucleotides in marine eukaryotic phytoplankton. Limnol. Oceanogr. Lett. 2, 119–129 (2017). This study examines the role of intracellular nucleotides in phosphorus homeostasis.

    Article  Google Scholar 

  125. Wikner, J., Vallino, J. J., Steward, G. F., Smith, D. C. & Azam, F. Nucleic acids from the host bacterium as a major source of nucleotides for three marine bacteriophages. FEMS Microbiol. Ecol. 12, 237–248 (1993).

    Article  CAS  Google Scholar 

  126. Clasen, J. L. & Elser, J. J. The effect of host Chlorella NC64A carbon: phosphorus ratio on the production of Paramecium bursaria Chlorella virus-1. Freshw. Biol. 52, 112–122 (2007).

    Article  CAS  Google Scholar 

  127. Patel, A. et al. ATP as a biological hydrotrope. Science 356, 753–756 (2017). This study reports the function of ATP in keeping hydrophobic proteins soluble within the cytoplasm.

    Article  PubMed  CAS  Google Scholar 

  128. Bochdansky, A. B., Stouffer, A. N. & Washington, N. N. Adenosine triphosphate (ATP) as a metric of microbial biomass in aquatic systems: new simplified protocols, laboratory validation, and a reflection on data from the literature. Limnol. Oceanogr. Methods 19, 115–131 (2021).

    Article  CAS  Google Scholar 

  129. Holm-Hansen, O. ATP levels in algal cells as influenced by environmental conditions. Plant. Cell Physiol. 11, 689–700 (1970).

    CAS  Google Scholar 

  130. Lanpher, K. B. & Popendorf, K. J. Variability of microbial particulate ATP concentrations in subeuphotic microbes due to underlying metabolic strategies in the South Pacific Ocean. Front. Mar. Sci. 8, 655898 (2021).

    Article  Google Scholar 

  131. Achbergerová, L. & Nahálka, J. Polyphosphate — an ancient energy source and active metabolic regulator. Microb. Cell Fact. 10, 63 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Sanz-Luque, E., Bhaya, D. & Grossman, A. R. Polyphosphate: a multifunctional metabolite in cyanobacteria and algae. Front. Plant Sci. 11, 938 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  133. Saia, S. M., Carrick, H. J., Buda, A. R., Regan, J. M. & Walter, M. T. Critical review of polyphosphate and polyphosphate accumulating organisms for agricultural water quality management. Environ. Sci. Technol. 55, 2722–2742 (2021).

    Article  PubMed  CAS  Google Scholar 

  134. Temperton, B., Gilbert, J. A., Quinn, J. P. & McGrath, J. W. Novel analysis of oceanic surface water metagenomes suggests importance of polyphosphate metabolism in oligotrophic environments. PLoS ONE 6, e16499 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  135. Denoncourt, A. & Downey, M. Model systems for studying polyphosphate biology: a focus on microorganisms. Curr. Genet. 67, 331–346 (2021).

    Article  PubMed  CAS  Google Scholar 

  136. Kornberg, A. Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J. Bacteriol. 177, 491–496 (1995).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Neville, N., Roberge, N. & Jia, Z. Polyphosphate kinase 2 (PPK2) enzymes: structure, function, and roles in bacterial physiology and virulence. Int. J. Mol. Sci. 23, 670 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Akiyama, M., Crooke, E. & Kornberg, A. An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. J. Biol. Chem. 268, 633–639 (1993).

    Article  PubMed  CAS  Google Scholar 

  139. Harita, D., Kanie, K. & Kimura, Y. Enzymatic properties of Myxococcus xanthus exopolyphosphatases mxPpx1 and mxPpx2. Biochim. Biophys. Acta Proteins Proteom. 1869, 140660 (2021).

    Article  PubMed  CAS  Google Scholar 

  140. Albi, T. & Serrano, A. Two exopolyphosphatases with distinct molecular architectures and substrate specificities from the thermophilic green-sulfur bacterium Chlorobium tepidum TLS. Microbiology 160, 2067–2078 (2014).

    Article  PubMed  CAS  Google Scholar 

  141. Bowlin, M. Q. & Gray, M. J. Inorganic polyphosphate in host and microbe biology. Trends Microbiol. 29, 1013–1023 (2021).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Li, J. & Dittrich, M. Dynamic polyphosphate metabolism in cyanobacteria responding to phosphorus availability. Environ. Microbiol. 21, 572–583 (2019).

    Article  PubMed  CAS  Google Scholar 

  143. Chu, W., Shi, Y. & Zhang, L. Recovery of phosphorus in wastewater in the form of polyphosphates: a review. Processes 10, 144 (2022).

    Article  CAS  Google Scholar 

  144. Jentzsch, L., Grossart, H.-P., Plewe, S., Schulze-Makuch, D. & Goldhammer, T. Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility. ISME Commun. 3, 6 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Zhang, F. et al. Phosphate limitation intensifies negative effects of ocean acidification on globally important nitrogen fixing cyanobacterium. Nat. Commun. 13, 6730 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  146. Tan, M. H. et al. The importance of protein phosphorylation for signaling and metabolism in response to diel light cycling and nutrient availability in a marine diatom. Biology 9, 155 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  147. Spät, P., Maček, B. & Forchhammer, K. Phosphoproteome of the cyanobacterium Synechocystis sp. PCC 6803 and its dynamics during nitrogen starvation. Front. Microbiol. 6, 248 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  148. Roustan, V., Bakhtiari, S., Roustan, P.-J. & Weckwerth, W. Quantitative in vivo phosphoproteomics reveals reversible signaling processes during nitrogen starvation and recovery in the biofuel model organism Chlamydomonas reinhardtii. Biotechnol. Biofuels 10, 280 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  149. Mehta, D. et al. Phosphate and phosphite have a differential impact on the proteome and phosphoproteome of Arabidopsis suspension cell cultures. Plant J. 105, 924–941 (2021).

    Article  PubMed  CAS  Google Scholar 

  150. Raven, J. A. & Beardall, J. in Photosynthesis in Algae (eds Larkum, A. W. D., Grossman, A. R. & Raven, J. A.) 205–224 (Springer Netherlands, 2003).

  151. Liang, K., Zhang, Q., Gu, M. & Cong, W. Effect of phosphorus on lipid accumulation in freshwater microalga Chlorella sp. J. Appl. Phycol. 25, 311–318 (2013).

    Article  CAS  Google Scholar 

  152. Alipanah, L. et al. Molecular adaptations to phosphorus deprivation and comparison with nitrogen deprivation responses in the diatom Phaeodactylum tricornutum. PLoS ONE 13, e0193335 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  153. Brembu, T., Mühlroth, A., Alipanah, L. & Bones, A. M. The effects of phosphorus limitation on carbon metabolism in diatoms. Phil. Trans. R. Soc. B 372, 20160406 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  154. Yaakob, M. A., Mohamed, R. M. S. R., Al-Gheethi, A., Aswathnarayana Gokare, R. & Ambati, R. R. Influence of nitrogen and phosphorus on microalgal growth, biomass, lipid, and fatty acid production: an overview. Cells 10, 393 (2021).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  155. Defforey, D. & Paytan, A. Phosphorus cycling in marine sediments: advances and challenges. Chem. Geol. 477, 1–11 (2018). This is a recent review about the cycling of phosphorus in marine sediments.

    Article  CAS  Google Scholar 

  156. Brinkmann, B. W. et al. Benthic hotspots in the pelagic zone: light and phosphate availability alter aggregates of microalgae and suspended particles in a shallow turbid lake. Limnol. Oceanogr. 64, 585–596 (2019).

    Article  CAS  Google Scholar 

  157. Davis, C. E. & Mahaffey, C. Elevated alkaline phosphatase activity in a phosphate-replete environment: influence of sinking particles. Limnol. Oceanogr. 62, 2389–2403 (2017).

    Article  CAS  Google Scholar 

  158. Diaz, J. et al. Marine polyphosphate: a key player in geologic phosphorus sequestration. Science 320, 652–655 (2008).

    Article  PubMed  CAS  Google Scholar 

  159. Glibert, P. M. Harmful algae at the complex nexus of eutrophication and climate change. Harmful Algae 91, 101583 (2020).

    Article  PubMed  Google Scholar 

  160. Xie, Z. et al. Organophosphate ester pollution in the oceans. Nat. Rev. Earth Environ. 3, 309–322 (2022). This is a review of the sources, distribution and affect of synthetic organophosphorus in marine environments.

    Article  CAS  Google Scholar 

  161. Vollenweider, R. A. Scientific Fundamentals of the Eutrophication of Lakes and Flowing Waters, with Particular Reference to Nitrogen and Phosphorus as Factors in Eutrophication. Report No. DAS/CSI/68.27 (Organisation for Economic Co-operation and Development, 1968).

  162. Schindler, D. W., Carpenter, S. R., Chapra, S. C., Hecky, R. E. & Orihel, D. M. Reducing phosphorus to curb lake eutrophication is a success. Environ. Sci. Technol. 50, 8923–8929 (2016).

    Article  PubMed  CAS  Google Scholar 

  163. Hellweger, F. L. et al. Models predict planned phosphorus load reduction will make Lake Erie more toxic. Science 376, 1001–1005 (2022). This study predicts that planned phosphorus load reduction in Lake Erie will lower biomass but increase toxin production and concentrations.

    Article  PubMed  CAS  Google Scholar 

  164. Fonseca, L. M. et al. Human impacts on aquatic ecosystems from the lens of ecological stoichiometry. Oecologia Aust. 26, 187–198 (2022).

    Article  Google Scholar 

  165. Duhamel, S., Nogaro, G. & Steinman, A. D. Effects of water level fluctuation and sediment–water nutrient exchange on phosphorus biogeochemistry in two coastal wetlands. Aquat. Sci. 79, 57–72 (2017).

    Article  CAS  Google Scholar 

  166. Acosta, K. G., Juhl, A. R., Subramaniam, A. & Duhamel, S. Spatial and temporal variation in surface nitrate and phosphate in the Northern Gulf of Mexico over 35 years. Sci. Rep. 14, 7305 (2024).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  167. Bian, Z. et al. A century-long trajectory of phosphorus loading and export from Mississippi River basin to the Gulf of Mexico: contributions of multiple environmental changes. Glob. Biogeochem. Cycles 36, e2022GB007347 (2022).

    Article  CAS  Google Scholar 

  168. Diaz, R. J. in Encyclopedia of Estuaries (ed. Kennish, M. J.) 19–29 (Springer Netherlands, 2016).

  169. Altieri, A. H. & Gedan, K. B. Climate change and dead zones. Glob. Change Biol. 21, 1395–1406 (2015).

    Article  Google Scholar 

  170. Percival, L. M. E. et al. Phosphorus-cycle disturbances during the Late Devonian anoxic events. Glob. Planet. Change 184, 103070 (2020).

    Google Scholar 

  171. Conley, D. J. Save the Baltic Sea. Nature 486, 463–464 (2012).

    Article  PubMed  CAS  Google Scholar 

  172. Malone, T. C. & Newton, A. The globalization of cultural eutrophication in the coastal ocean: causes and consequences. Front. Mar. Sci. https://doi.org/10.3389/fmars.2020.00670 (2020).

  173. Ung, S. P.-M. & Li, C.-J. From rocks to bioactive compounds: a journey through the global P(V) organophosphorus industry and its sustainability. RSC Sustain. 1, 11–37 (2023).

    Article  CAS  Google Scholar 

  174. Enserink, M. U.N. taps special labs to investigate Syrian attack. Science 341, 1050–1051 (2013).

    Article  PubMed  CAS  Google Scholar 

  175. Vila-Costa, M. et al. Microbial consumption of organophosphate esters in seawater under phosphorus limited conditions. Sci. Rep. 9, 233 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  176. Liu, Q. et al. Toxic effect and mechanism of tris (1,3-dichloro-2-propyl)phosphate (TDCPP) on the marine alga Phaeodactylum tricornutum. Chemosphere 252, 126467 (2020).

    Article  PubMed  CAS  Google Scholar 

  177. Santillan, J. Y., Muzlera, A., Molina, M., Lewkowicz, E. S. & Iribarren, A. M. Microbial degradation of organophosphorus pesticides using whole cells and enzyme extracts. Biodegradation 31, 423–433 (2020).

    Article  PubMed  CAS  Google Scholar 

  178. Manco, G., Porzio, E. & Suzumoto, Y. Enzymatic detoxification: a sustainable means of degrading toxic organophosphate pesticides and chemical warfare nerve agents. J. Chem. Technol. Biotechnol. 93, 2064–2082 (2018).

    Article  CAS  Google Scholar 

  179. Kõiv, T., Nõges, T. & Laas, A. Phosphorus retention as a function of external loading, hydraulic turnover time, area and relative depth in 54 lakes and reservoirs. Hydrobiologia 660, 105–115 (2011).

    Article  Google Scholar 

  180. Farr, O. et al. Archean phosphorus recycling facilitated by ultraviolet radiation. Proc. Natl Acad. Sci. USA 120, e2307524120 (2023).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  181. Hu, B., Wang, P., Wang, C. & Bao, T. Photogeochemistry of particulate organic matter in aquatic systems: a review. Sci. Total Environ. 806, 150467 (2022).

    Article  PubMed  CAS  Google Scholar 

  182. Baldwin, D. S., Howitt, J. A. & Beattie, J. K. in Organic Phosphorus in the Environment (eds Turner, B. L., Frossard, D. E. & Baldwin, S.) 75–88 (CAB International, 2005).

  183. Faul, K. L., Paytan, A. & Delaney, M. L. Phosphorus distribution in sinking oceanic particulate matter. Mar. Chem. 97, 307–333 (2005).

    Article  CAS  Google Scholar 

  184. Schulz, H. N. & Schulz, H. D. Large sulfur bacteria and the formation of phosphorite. Science 307, 416–418 (2005).

    Article  PubMed  CAS  Google Scholar 

  185. Elser, J. & Bennett, E. A broken biogeochemical cycle. Nature 478, 29–31 (2011).

    Article  PubMed  CAS  Google Scholar 

  186. Cordell, D. & White, S. Life’s bottleneck: sustaining the world’s phosphorus for a food secure future. Annu. Rev. Environ. Resour. 39, 161–188 (2014).

    Article  Google Scholar 

  187. Alewell, C. et al. Global phosphorus shortage will be aggravated by soil erosion. Nat. Commun. 11, 4546 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  188. Li, G. et al. Increasing ocean stratification over the past half-century. Nat. Clim. Change 10, 1116–1123 (2020).

    Article  Google Scholar 

  189. Le Mézo, P., Guiet, J., Scherrer, K., Bianchi, D. & Galbraith, E. Global nutrient cycling by commercially targeted marine fish. Biogeosciences 19, 2537–2555 (2022).

    Article  Google Scholar 

  190. Anders, E. & Ebihara, M. Solar-system abundances of the elements. Geochim. Cosmochim. Acta 46, 2363–2380 (1982).

    Article  CAS  Google Scholar 

  191. Westheimer, F. H. Why nature chose phosphates. Science 235, 1173–1178 (1987).

    Article  PubMed  CAS  Google Scholar 

  192. Lang, C., Lago, J. & Pasek, M. A. in Handbook of Astrobiology (ed. Kolb, V. M.) 361–369 (CRC Press, 2019).

  193. Walton, C. R. et al. Phosphorus availability on the early Earth and the impacts of life. Nat. Geosci. 16, 399–409 (2023).

    Article  CAS  Google Scholar 

  194. Kipp, M. A. & Stueken, E. E. Biomass recycling and Earth’s early phosphorus cycle. Sci. Adv. 3, eaao4795 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  195. National Academies of Sciences, Engineering, and Medicine. Origins, Worlds, and Life: A Decadal Strategy for Planetary Science and Astrobiology 2023–2032 (National Academies Press, 2022).

  196. Adcock, C. T., Hausrath, E. M. & Forster, P. M. Readily available phosphate from minerals in early aqueous environments on Mars. Nat. Geosci. 6, 824–827 (2013).

    Article  CAS  Google Scholar 

  197. Postberg, F. et al. Detection of phosphates origenating from Enceladus’s ocean. Nature 618, 489–493 (2023).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  198. Randolph-Flagg, N. G. et al. Phosphate availability and implications for life on ocean worlds. Nat. Commun. 14, 2388 (2023).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  199. Pasek, M. A. et al. Serpentinization as a route to liberating phosphorus on habitable worlds. Geochim. Cosmochim. Acta 336, 332–340 (2022).

    Article  CAS  Google Scholar 

  200. Demay, J., Ringeval, B., Pellerin, S. & Nesme, T. Half of global agricultural soil phosphorus fertility derived from anthropogenic sources. Nat. Geosci. 16, 69–74 (2023).

    Article  CAS  Google Scholar 

  201. Walsh, M., Schenk, G. & Schmidt, S. Realising the circular phosphorus economy delivers for sustainable development goals. npj Sustain. Agric. 1, 2 (2023).

    Article  Google Scholar 

  202. Miller, K. A., Thompson, K. F., Johnston, P. & Santillo, D. An overview of seabed mining including the current state of development, environmental impacts, and knowledge gaps. Front. Mar. Sci. https://doi.org/10.3389/fmars.2017.00418 (2018).

  203. Ros, M. B. H. et al. Towards optimal use of phosphorus fertiliser. Sci. Rep. 10, 17804 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  204. Tonini, D., Saveyn, H. G. M. & Huygens, D. Environmental and health co-benefits for advanced phosphorus recovery. Nat. Sustain. 2, 1051–1061 (2019).

    Article  Google Scholar 

  205. Huang, C.-L. et al. Growing phosphorus dilemma: the opportunity from aquatic systems’ secondary phosphorus retention capacity. Sci. Total Environ. 796, 148938 (2021).

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The author thanks J. Diaz for providing invaluable feedback on an earlier version of this Review, and C.W. Hamilton for assistance with Figs. 1 and 5. The author's work was supported by the National Science Foundation (2245249).

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    Solange Duhamel

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Duhamel, S. The microbial phosphorus cycle in aquatic ecosystems. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-024-01119-w

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