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Processes and patterns of oceanic nutrient limitation

Abstract

Microbial activity is a fundamental component of oceanic nutrient cycles. Photosynthetic microbes, collectively termed phytoplankton, are responsible for the vast majority of primary production in marine waters. The availability of nutrients in the upper ocean frequently limits the activity and abundance of these organisms. Experimental data have revealed two broad regimes of phytoplankton nutrient limitation in the modern upper ocean. Nitrogen availability tends to limit productivity throughout much of the surface low-latitude ocean, where the supply of nutrients from the subsurface is relatively slow. In contrast, iron often limits productivity where subsurface nutrient supply is enhanced, including within the main oceanic upwelling regions of the Southern Ocean and the eastern equatorial Pacific. Phosphorus, vitamins and micronutrients other than iron may also (co-)limit marine phytoplankton. The spatial patterns and importance of co-limitation, however, remain unclear. Variability in the stoichiometries of nutrient supply and biological demand are key determinants of oceanic nutrient limitation. Deciphering the mechanisms that underpin this variability, and the consequences for marine microbes, will be a challenge. But such knowledge will be crucial for accurately predicting the consequences of ongoing anthropogenic perturbations to oceanic nutrient biogeochemistry.

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Figure 1: Comparisons between intracellular and dissolved seawater elemental stoichiometry.
Figure 2: Example timescales and space scales of nutrient-related phenomena.
Figure 3: Patterns of nutrient limitation.

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References

  1. Frausto da Silva, J. J. R. & Williams, R. J. P. The Biological Chemistry of the Elements: The Inorganic Chemistry of Life, 2nd edn (Oxford Univ. Press, 2001).

    Google Scholar 

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

    Google Scholar 

  3. Redfield, A. C. in James Johnstone Memorial Volume, 176–192 (Liverpool Univ. Press, 1934).

    Google Scholar 

  4. Redfield, A. C., The biological control of chemical factors in the environment. Am. Sci. 46, 205–221 (1958).

    Google Scholar 

  5. de Baar, H. J. W., von Liebig's law of the minimum and plankton ecology (1899–1991). Prog. Oceanogr. 33, 347–386 (1994).

    Article  Google Scholar 

  6. Morel, F. M. M., Milligan, A. J. & Saito, M. A. Marine Bioinorganic Chemistry: The Role of Trace Metals in the Ocean Cycles of Major Nutrients. Treatise on Geochemistry Vol. 6, 113–143 (2003).

    Google Scholar 

  7. Arrigo, K. R. Marine microorganisms and global nutrient cycles. Nature 437, 349–355 (2005).

    Article  Google Scholar 

  8. Saito, M. A., Goepfert, T. J. & Ritt, J. T. Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability. Limnol. Oceanogr. 53, 276–290 (2008).

    Article  Google Scholar 

  9. Geider, R. J. & La Roche, J. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur. J. Phycol. 37, 1–17 (2002).

    Article  Google Scholar 

  10. Quigg, A. et al. The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425, 291–294 (2003).

    Article  Google Scholar 

  11. Klausmeier, C. A., Litchman, E., Daufresne, T. & Levin, S. A. Phytoplankton stoichiometry. Ecol. Res. 23, 479–485 (2008).

    Article  Google Scholar 

  12. Duce, R. A. et al. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893–897 (2008).

    Article  Google Scholar 

  13. Krishnamurthy, A. et al. Impacts of increasing anthropogenic soluble iron and nitrogen deposition on ocean biogeochemistry. Glob. Biogeochem. Cycles 23, GB3016 (2009).

    Article  Google Scholar 

  14. Falkowski, P. et al. The global carbon cycle: A test of our knowledge of Earth as a system. Science 290, 291–296 (2000).

    Article  Google Scholar 

  15. Raven, J. A. Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquat. Microb. Ecol. 56, 177–192 (2009).

    Article  Google Scholar 

  16. Eppley, R. W. & Peterson, B. J. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 677–680 (1979).

    Article  Google Scholar 

  17. Blackman, F. F. Optima and limiting factors. Ann. Bot. 19, 281–298 (1905).

    Article  Google Scholar 

  18. Cullen, J. J. Hypotheses to explain high-nutrient conditions in the open sea. Limnol. Oceanogr. 36, 1578–1599 (1991).

    Article  Google Scholar 

  19. von Liebig, J., Chemistry and its Application to Agriculture And Physiology. (Taylor and Walton, London, 1840).

    Google Scholar 

  20. Thingstad, T. F. et al. Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309, 1068–1071 (2005).

    Article  Google Scholar 

  21. Boyd, P. W., Strzepek, R., Fu, F. X. & Hutchins, D. A. Environmental control of open-ocean phytoplankton groups: Now and in the future. Limnol. Oceanogr. 55, 1353–1376 (2010).

    Article  Google Scholar 

  22. Cavender-Bares, K. K., Mann, E. L., Chisholm, S. W., Ondrusek, M. E. & Bidigare, R. R. Differential response of equatorial Pacific phytoplankton to iron fertilisation. Limnol. Oceanogr. 44, (1999).

  23. Chisholm, S. W. in Primary Productivity and Biogeochemical Cycles in the Sea (eds Falkowski, P. G. & Woodhead, A. D.) 213–237 (Plenum, 1992).

    Book  Google Scholar 

  24. Raven, J. A. The twelfth Tansley lecture. Small is beautiful: The picophytoplankton. Funct. Ecol. 12, 503–513 (1998).

    Article  Google Scholar 

  25. 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).

    Article  Google Scholar 

  26. Irigoien, X., Huisman, J. & Harris, R. P. Global biodiversity patterns of marine phytoplankton and zooplankton. Nature 429, 863–867 (2004).

    Article  Google Scholar 

  27. Tyrrell, T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999).

    Article  Google Scholar 

  28. Falkowski, P. G. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275 (1997).

    Article  Google Scholar 

  29. Mills, M. M., Ridame, C., Davey, M., La Roche, J. & Geider, R. J. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292–294 (2004).

    Article  Google Scholar 

  30. Moore, J. K. & Doney, S. C. Iron availability limits the ocean nitrogen inventory stabilizing feedbacks between marine denitrification and nitrogen fixation. Glob. Biogeochem. Cycles 21, GB2001 (2007).

    Article  Google Scholar 

  31. Moore, C. M. et al. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nature Geosci. 2, 867–871 (2009).

    Article  Google Scholar 

  32. Dupont, C. L., Butcher, A., Valas, R. E., Bourne, P. E. & Caetano-Anolles, G. History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc. Natl Acad. Sci. USA 107, 10567–10572 (2010).

    Article  Google Scholar 

  33. Anderson, L. A. & Sarmiento, J. L. Redfield ratios of remineralization determined by nutrient data-analysis. Glob. Biogeochem. Cycles 8, 65–80 (1994).

    Article  Google Scholar 

  34. Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N. & Dunne, J. P. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007).

    Article  Google Scholar 

  35. Ho, T. Y. et al. The elemental composition of some marine phytoplankton. J. Phycol. 39, 1145–1159 (2003).

    Article  Google Scholar 

  36. Sunda, W. G. & Huntsman, S. A. Cobalt and zinc interreplacement in marine phytoplankton: Biological and geochemical implications. Limnol. Oceanogr. 40, 1404–1417 (1995).

    Article  Google Scholar 

  37. Sunda, W. G. & Huntsman, S. A. Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390, 389–392 (1997).

    Article  Google Scholar 

  38. Sunda, W. G. & Huntsman, S. A. Control of Cd concentrations in a coastal diatom by interactions among free ionic Cd, Zn, and Mn in seawater. Environ. Sci. Technol. 32, 2961–2968 (1998).

    Article  Google Scholar 

  39. Saito, M. A., Sigman, D. M. & Morel, F. M. M. The bioinorganic chemistry of the ancient ocean: The co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean–Proterozoic boundary? Inorg. Chim. Acta 356, 308–318 (2003).

    Article  Google Scholar 

  40. Grzymski, J. J. & Dussaq, A. M. The significance of nitrogen cost minimization in proteomes of marine microorganisms. ISME J. 6, 71–80 (2012).

    Article  Google Scholar 

  41. Wu, J., Sunda, W., Boyle, E. A. & Karl, D. M. Phosphate depletion in the Western North Atlantic Ocean. Science 289, 759–762 (2000).

    Article  Google Scholar 

  42. Lenton, T. M. & Klausmeier, C. A. Biotic stoichiometric controls on the deep ocean N:P ratio. Biogeosciences 4, 353–367 (2007).

    Article  Google Scholar 

  43. Sarmiento, J. L., Gruber, N., Brezinski, M. A. & Dunne, J. P. High-latitude controls of thermocline nutrients and low latitude biological productivity. Nature 427, 56–60 (2004).

    Article  Google Scholar 

  44. Deutsch, C. & Weber, T. Nutrient ratios as a tracer and driver of ocean biogeochemistry. Annu. Rev. Mar. Sci. 4, 113–141 (2012).

    Article  Google Scholar 

  45. Moore, J. K., Doney, S. C., Glover, D. M. & Fung, I. Y. Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep-Sea Res. II Top. Studies Oceanogr. 49, 463–507 (2002).

    Article  Google Scholar 

  46. Krishnamurthy, A., Moore, J. K., Mahowald, N., Luo, C. & Zender, C. S. Impacts of atmospheric nutrient inputs on marine biogeochemistry. J. Geophys. Res. 115, G01006 (2010).

    Article  Google Scholar 

  47. Moore, C. M. et al. Relative influence of nitrogen and phosphorus availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical North Atlantic Ocean. Limnol. Oceanogr. 53, 291–305 (2008).

    Article  Google Scholar 

  48. Tanaka, T. et al. Lack of P-limitation of phytoplankton and heterotrophic prokaryotes in surface waters of three anticyclonic eddies in the stratified Mediterranean Sea. Biogeosciences 8, 525–538 (2011).

    Article  Google Scholar 

  49. Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008).

    Article  Google Scholar 

  50. Flynn, K. J. Ecological modelling in a sea of variable stoichiometry: Dysfunctionality and the legacy of Redfield and Monod. Prog. Oceanogr. 84, 52–65 (2010).

    Article  Google Scholar 

  51. Steinacher, M. et al. Projected 21st century decrease in marine productivity: A multi-model analysis. Biogeosciences 7, 979–1005 (2010).

    Article  Google Scholar 

  52. Moutin, T. et al. Phosphate availability and the ultimate control of new nitrogen input by nitrogen fixation in the tropical Pacific Ocean. Biogeosciences 5, 95–109 (2008).

    Article  Google Scholar 

  53. Martin, J. H. & Fitzwater, S. E. Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331, 341–343 (1988).

    Article  Google Scholar 

  54. Boyd, P. W. et al. Mesoscale iron enrichment experiments 1993–2005: Synthesis and future directions. Science 315, 612–617 (2007).

    Article  Google Scholar 

  55. Menzel, D. W. & Ryther, J. H. Nutrients limiting the production of phytoplankton in the Sargasso Sea, with special reference to iron. Deep-Sea Res. 7, 276–281 (1961).

    Google Scholar 

  56. Graziano, L. M., Geider, R. J., Li, W. K. W. & Olaizola, M. Nitrogen limitation of North Atlantic phytoplankton: Analysis of physiological condition in nutrient enrichment experiments. Aquat. Microb. Ecol. 11, 53–64 (1996).

    Article  Google Scholar 

  57. Dyhrman, S. T., Webb, E. A., Anderson, D. M., Moffett, J. W. & Waterbury, J. B. Cell-specific detection of phosphorus stress in Trichodesmium from the western north Atlantic. Limnol. Oceanogr. 47, 1832–1836 (2002).

    Article  Google Scholar 

  58. Lomas, M. W., Swain, A., Shelton, R. & Ammerman, J. W. Taxonomic variability of phosphorus stress in Sargasso Sea phytoplankton. Limnol. Oceanogr. 49, 2303–2310 (2004).

    Article  Google Scholar 

  59. Zohary, T. et al. P-limited bacteria but N and P co-limited phytoplankton in the Eastern Mediterranean: A microcosm experiment. Deep-Sea Res. II 52, 3011–3023 (2005).

    Article  Google Scholar 

  60. La Roche, J., Geider, R. J., Graziano, L. M., Murray, H. & Lewis, K. Induction of specific proteins in eukaryotic algae grown under iron-, phosphorus-, or nitrogen-deficient conditions. J. Phycol. 29, 767–777 (1993).

    Article  Google Scholar 

  61. Chappell, P. D., Moffett, J. W., Hynes, A. M. & Webb, E. A. Molecular evidence of iron limitation and availability in the global diazotroph Trichodesmium. ISME J. 6, 1728–1739 (2012).

    Article  Google Scholar 

  62. Marchetti, A. et al. Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc. Natl Acad. Sci. USA 109, E317–E325 (2012).

    Article  Google Scholar 

  63. Sigman, D. M., Hain, M. P. & Haug, G. H. The polar ocean and glacial cycles in atmospheric CO2 concentration. Nature 466, 47–55 (2010).

    Article  Google Scholar 

  64. Martinez-Garcia, A. et al. Southern Ocean dust–climate coupling over the past four million years. Nature 476, 312–315 (2011).

    Article  Google Scholar 

  65. Ren, H. et al. Foraminiferal isotope evidence of reduced nitrogen fixation in the ice age Atlantic Ocean. Science 323, 244–248 (2009).

    Article  Google Scholar 

  66. Noble, A. E. et al. Basin-scale inputs of cobalt, iron, and manganese from the Benguela–Angola front to the South Atlantic Ocean. Limnol. Oceanogr. 57, 989–1010 (2012).

    Article  Google Scholar 

  67. Shi, D. L., Xu, Y., Hopkinson, B. M. & Morel, F. M. M. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327, 676–679 (2010).

    Article  Google Scholar 

  68. Beman, J. M. et al. Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc. Natl Acad. Sci. USA 108, 208–213 (2011).

    Article  Google Scholar 

  69. Sunda, W. G. Iron and the carbon pump. Science 327, 654–655 (2010).

    Article  Google Scholar 

  70. Sarmiento, J. L., Hughes, T. M. C., Stouffer, R. J. & Manabe, S. Simulated response of the ocean carbon cycle to anthropogenic climate warming. Nature 393, 245–249 (1998).

    Article  Google Scholar 

  71. Sarmiento, J. L. et al. Response of ocean ecosystems to climate warming. Glob. Biogeochem. Cycles 18, GB3003 (2004).

    Article  Google Scholar 

  72. Polovina, J. J., Howell, E. A. & Abecassis, M. Ocean's least productive waters are expanding. Geophys. Res. Lett. 35, L03618 (2008).

    Article  Google Scholar 

  73. Saba, V. S. et al. Challenges of modeling depth-integrated marine primary productivity over multiple decades: A case study at BATS and HOT. Glob. Biogeochem. Cycles 24, GB3020 (2010).

    Article  Google Scholar 

  74. Henson, S. A. et al. Detection of anthropogenic climate change in satellite records of ocean chlorophyll and productivity. Biogeosciences 7, 621–640 (2010).

    Article  Google Scholar 

  75. Stramma, L., Johnson, G. C., Sprintall, J. & Mohrholz, V. Expanding oxygen-minimum zones in the tropical oceans. Science 320, 655–658 (2008).

    Article  Google Scholar 

  76. Godfray, H. C. J. et al. Food security: The challenge of feeding 9 billion people. Science 327, 812–818 (2010).

    Article  Google Scholar 

  77. Mahowald, N. et al. Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob. Biogeochem. Cycles 22, GB4026 (2008).

    Article  Google Scholar 

  78. Mahowald, N. M. et al. Observed 20th century desert dust variability: Impact on climate and biogeochemistry. Atmos. Chem. Phys. 10, 10875–10893 (2010).

    Article  Google Scholar 

  79. Seitzinger, S. P. et al. Global river nutrient export: A scenario analysis of past and future trends. Glob. Biogeochem. Cycles 24, GB0A08 (2010).

    Google Scholar 

  80. Cordell, D., Drangert, J. O. & White, S. The story of phosphorus: Global food security and food for thought. Glob. Environ. Change Hum. Policy Dimens. 19, 292–305 (2009).

    Article  Google Scholar 

  81. Raiswell, R. & Canfield, D. E. The iron biogeochemical cycle past and present geochemical perspectives. Geochem. Persp. 1, 1–220 (2012).

    Article  Google Scholar 

  82. Jickells, T. D. et al. Global iron connections between desert dust, ocean biogeochemistry, and climate. Science 308, 67–71 (2005).

    Article  Google Scholar 

  83. Monteiro, F. M., Dutkiewicz, S. & Follows, M. J. Biogeographical controls on the marine nitrogen fixers. Glob. Biogeochem. Cycles 25, GB2003 (2011).

    Article  Google Scholar 

  84. Diaz, R. J. & Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929 (2008).

    Article  Google Scholar 

  85. Levitan, O. et al. Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Change Biol. 13, 531–538 (2007).

    Article  Google Scholar 

  86. Eppley, R. W. Temperature and phytoplankton growth in the sea. Fishery Bull. 70, 1063–1085 (1972).

    Google Scholar 

  87. Shi, D., Kranz, S. A., Kim, J-M. & Morel, F. M. M. Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc. Natl Acad. Sci. USA 109, E3094–3100 (2012).

    Article  Google Scholar 

  88. Taucher, J. & Oschlies, A. Can we predict the direction of marine primary production change under global warming? Geophys. Res. Lett. 38, 6 (2011).

    Article  Google Scholar 

  89. Breitbarth, E., Oschlies, A. & LaRoche, J. Physiological constraints on the global distribution of Trichodesmium—effect of temperature on diazotrophy. Biogeosciences 4, 53–61 (2007).

    Article  Google Scholar 

  90. Marinov, I. et al. Impact of oceanic circulation on biological carbon storage in the ocean and atmospheric pCO2 . Glob. Biogeochem. Cycles 22, GB3007 (2008).

    Article  Google Scholar 

  91. Marinov, I., Gnanadesikan, A., Toggweiler, J. R. & Sarmiento, J. L. The Southern Ocean biogeochemical divide. Nature 441, 964–967 (2006).

    Article  Google Scholar 

  92. Ito, T. & Follows, M. J. Preformed phosphate, soft tissue pump and atmospheric CO2 . J. Mar. Res. 63, 813–839 (2005).

    Article  Google Scholar 

  93. Sarmiento, J. L. & Toggweiler, J. R. A new model for the role of the oceans in determining atmospheric pCO2 . Nature 308, 621–624 (1984).

    Article  Google Scholar 

  94. Mills, M. M. & Arrigo, K. R. Magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton. Nature Geosci. 3, 412–416 (2010).

    Article  Google Scholar 

  95. Henderson, G. M. et al. GEOTRACES—An international study of the global marine biogeochemical cycles of trace elements and their isotopes. Chem. Erde Geochem. 67, 85–131 (2007).

    Article  Google Scholar 

  96. Raiswell, R. et al. Contributions from glacially derived sediment to the global iron (oxyhydr)oxide cycle: Implications for iron delivery to the oceans. Geochim. Cosmochim. Acta 70, 2765–2780 (2006).

    Article  Google Scholar 

  97. Wynn, P. M., Hodson, A. J., Heaton, T. H. E. & Chenery, S. R. Nitrate production beneath a high arctic glacier, Svalbard. Chem. Geol. 244, 88–102 (2007).

    Article  Google Scholar 

  98. Wallmann, K. Phosphorus imbalance in the global ocean? Glob. Biogeochem. Cycles 24, GB4030 (2010).

    Article  Google Scholar 

  99. Cullen, J. J., Yang, X. & MacIntyre, H. L. in Primary Productivity and Biogeochemical Cycles in the Sea (eds Falkowski, P. G. & Woodhead, A.) 69–88 (Plenum, 1992).

    Book  Google Scholar 

  100. Thingstad, T. F., Ovreas, L., Egge, J. K., Lovdal, T. & Heldal, M. Use of non-limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecol. Lett. 8, 675–682 (2005).

    Article  Google Scholar 

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Acknowledgements

This review results from the activities of the International Geosphere–Biosphere Programme (IGBP) Fast Track Initiative on Upper Ocean Nutrient Limitation and in particular a workshop hosted at the National Oceanography Centre, Southampton, UK. Financial support for the workshop was provided by IGBP, US Ocean Carbon and Biogeochemistry, the Scientific Committee on Oceanic Research (SCOR) and EU-COST-735.

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Regulation of marine phytoplankton by two nutrient limitation regimes (PDF 5654 kb)

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Moore, C., Mills, M., Arrigo, K. et al. Processes and patterns of oceanic nutrient limitation. Nature Geosci 6, 701–710 (2013). https://doi.org/10.1038/ngeo1765

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