Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean

Nature volume 387, pages 272–275 (1997)Cite this article

Abstract

Over geological time, photosynthetic carbon fixation in the oceans has exceeded respiratory oxidation of organic carbon. The imbalance between the two processes has resulted in the simultaneous accumulation of oxygen in, and drawdown of carbon dioxide from, the Earth's atmosphere, and the burial of organic carbon in marine sediments1–3. It is generally assumed that these processes are limited by the availability of phosphorus4,5, which is supplied by continental weathering and fluvial discharge5–7. Over the past two million years, decreases in atmospheric carbon dioxide concentrations during glacial periods correlate with increases in the export of organic carbon from surface waters to the marine sediments8–11, but variations in phosphorus fluxes appear to have been too small to account for these changes12,13. Consequently, it has been assumed that total oceanic primary productivity remained relatively constant during glacial-to-interglacial transitions, although the fraction of this productivity exported to the sediments somehow increased during glacial periods12,14. Here I present an analysis of the evolution of biogeochemical cycles which suggests that fixed nitrogen, not phosphorus, limits primary productivity on geological timescales. Small variations in the ratio of nitrogen fixation to denitrification can significantly change atmospheric carbon dioxide concentrations on glacial-to-interglacial timescales. The ratio of these two processes appears to be determined by the oxidation state of the ocean and the supply of trace elements, especially iron.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Berner, R. A. A model for atmosphereic CO2 over the Phanerozoic. Am. J. Sci. 291, 339–376 (1991).

    Article  ADS  CAS  Google Scholar 

  2. Holland, H. D. The Chemical Evolution of the Atmosphere and Oceans (Princeton Univ. Press, Princeton, 1984).

    Google Scholar 

  3. Walker, J. C. G. Was the Archaean Biosphere upside down? Nature 329, 710–712 (1987).

    Article  ADS  CAS  Google Scholar 

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

    CAS  Google Scholar 

  5. Broecker, W. S. Glacial to interglacial changes in ocean chemistry. Prog. Oceanogr. 11, 151–197 (1982).

    Article  ADS  Google Scholar 

  6. Meybeck, M. Carbon, nitrogen, and phsophorus transport by world rivers. Am. J. Sci. 282, 401–450 (1982).

    Article  ADS  CAS  Google Scholar 

  7. Froelich, P. N. Kinetic control of dissolved phosphate in natural rivers and estuaries: a primer on the phosphate buffer mechanism. Limnol. Oceanogr. 33, 649–668 (1988).

    ADS  CAS  Google Scholar 

  8. Mix, A. C. Influence of productivity variations on long-term atmospheric CO2 . Nature 337, 541–544 (1989).

    Article  ADS  CAS  Google Scholar 

  9. Sarnthein, M., Winn, K., Duplessy, J.-C. & Fontugne, M. R. Global variations of surface ocean primary productivity in low and mid latitudes: influence on CO2 reservoirs of the deep ocean and atmosphere during the last 21,000 years. Paleoceanography 3, 361–399 (1988).

    Article  ADS  Google Scholar 

  10. Lyle, M. W., Prahl, F. G. & Sparrow, M. A. Upwelling and productivity changes inferred from a temperature record in the central equatorial Pacific. Nature 355, 812–815 (1992).

    Article  ADS  Google Scholar 

  11. Bender, M. & Sowers, T. The Dole effect and its variations during the last 130,000 years as measured in the Vostok ice core. Global Biogeochem. Cycles 8, 363–376 (1994).

    Article  ADS  CAS  Google Scholar 

  12. Boyle, E. A. The role of vertical chemical fractionation in controlling late quaternary atmospheric carbon dioxide. J. Geochem. Res. 93, 15701–15714 (1988).

    ADS  Google Scholar 

  13. Imbrie, J. et al. On the structure and origin of major glaciation cycles. I. Linear responses to Milankovitch forcing. Paleoceanography 7, 701–738 (1992).

    Article  ADS  Google Scholar 

  14. Archer, D. & Maier-Reimer, E. Effect of deep-sea sedimentary calcite preservation on atmospheric CO2 concentration. Nature 367, 260–263 (1994).

    Article  ADS  CAS  Google Scholar 

  15. Broecker, W. S., Peng, T.-H. & Engh, R. Modeling the carbon system. Radiocarbon 22, 565–598 (1980).

    Article  CAS  Google Scholar 

  16. Barber, R. T. in Primary Productivity and Biogeochemical Cycles in the Sea (eds Falkowski, P. G. & Woodhead, A.) 89–106 (Plenum, New York, 1992).

    Book  Google Scholar 

  17. Kasting, J. F. Bolide impacts and the oxidation state of carbon in the Earth's early atmosphere. Origins Life Evol. Biosphere 20, 199–231 (1990).

    Article  ADS  CAS  Google Scholar 

  18. Warneck, P. Chemistry of the Natural Atmosphere (Academic, New York, 1988).

    Google Scholar 

  19. Postgate, J. R. Nitrogen Fixation (Edward Arnold, London, 1987).

    Google Scholar 

  20. Zehr, J. P. et al. Diversity of heterotrophic nitrogen-fixation genes in a marine cyanobacterial mat. Appl. Environ. Microbiol. 61, 2527–2532 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Van Cappellen, P. & Ingall, E. D. Redox stabilization of the atmosphere and oceans by phosphorus-limited marine productivity. Sceince 271, 493–496 (1996).

    Article  ADS  CAS  Google Scholar 

  22. Berner, R. A. Early Diagenesis, a Theoretical Approach (Princeton Univ. Press, Princeton, 1980).

    Google Scholar 

  23. Stumm, W. & Morgan, J. J. Aquatic Chemistry (Wiley, New York, 1981).

    Google Scholar 

  24. Copin-Montegut, C. & Copin-Montegut, G. Stoichiometry of carbon, nitrogen and phosphorus in marine particulate matter. Deep-Sea Res. 30, 31–46 (1983).

    Article  ADS  CAS  Google Scholar 

  25. Letelier, R. M. & Karl, D. M. The role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean. Mar. Ecol. Prog. Ser. 133, 263–273 (1996).

    Article  ADS  Google Scholar 

  26. Kaplan, W. A. in Nitrogen in the Marine Environment (eds Carpenter, E. J. & Capone, D. G.) 139–190 (Academic, New York, 1983).

    Book  Google Scholar 

  27. Christensen, J. P., Murray, J. W., Devol, A. H. & Codispoti, L. A. Denitrification in continental shelf sediments has major impact on the oceanic nitrogen budget. Global Biogeochem. Cycles 1, 97–116 (1987).

    Article  ADS  CAS  Google Scholar 

  28. Codispoti, L. A. & Christensen, J. P. Nitrification, denitrification and nitrous oxide cycling in the eastern tropical south Pacific Ocean. Mar. Chem. 16, 277–300 (1985).

    Article  CAS  Google Scholar 

  29. Devol, A. H. Direct measurement of nitrogen gas fluxes from continental shelf sediments. Nature 349, 319–321 (1991).

    Article  ADS  CAS  Google Scholar 

  30. Seitzinger, S. Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical importance. Limnol. Oceanogr. 33, 702–724 (1988).

    ADS  CAS  Google Scholar 

  31. Zumpft, W. G. in The Prokaryotes: A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Applications (eds Ballow, A, Truper, H. G., Dworkin, M., Harder, W. & Schleifer, K.-H.) 554–582 (Springer, New York, 1992).

    Google Scholar 

  32. Krom, M. D., Kress, N., Brenner, S. & Gordon, L. I. Phosphorus limitation of primary productivity in the eastern Mediterranean Sea. Limnol. Oceanogr. 36, 424–432 (1991).

    Article  ADS  CAS  Google Scholar 

  33. Martin, J. H. in Primary Productivity and Biogeochemical Cycles in the Sea (eds Falkowski, P. & Woodhead, A.) 123–137 (Plenum, New York, 1992).

    Book  Google Scholar 

  34. Rhther, J. H. & Dunstan, W. M. Nitrogen, phsophorus, and eutrophication in the coastal marine environment. Science 171, 1008–10013 (1971).

    Article  ADS  Google Scholar 

  35. Dugdale, R. C. Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12, 685–695 (1967).

    Article  ADS  Google Scholar 

  36. McElroy, M. B. Marine biological controls on atmospheric CO2 & climate. Nature 302, 328–329 (1983).

    Article  ADS  CAS  Google Scholar 

  37. Fanning, K. A. Nutrient provinces in the sea: concentration ratios, reaction rate ratios, and ideal covariation. J. Geophys. Res. 97C, 5693–5712 (1992).

    Article  ADS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  39. Codispoti, L. A. Is the ocean losing nitrate? Nature 376, 724 (1995).

    Article  ADS  CAS  Google Scholar 

  40. Carpenter, E. J. & Romans, K. Major role of the cyanobacterium Trichodesrnium in nutrient cycling in the North Atlantic Ocean. Science 254, 1356–1358 (1991).

    Article  ADS  CAS  Google Scholar 

  41. Carpenter, E. J. & McCarthy, J. J. Nitrogen fixation and uptake of combined nitrogenous nutrients by Oscillatoria (Trichodesmium) thiebautii in the western Sargasso Sea. Limnol. Oceanogr. 20, 389–401 (1975).

    Article  ADS  CAS  Google Scholar 

  42. Raven, J. A. The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol. 109, 279–287 (1988).

    Article  CAS  Google Scholar 

  43. Williams, R. J. P. Natural selection of the elements. Proc. R. Soc. Lond. B213, 361–397 (1981).

    ADS  Google Scholar 

  44. Falkowski, P. G. & Raven, J. A. Aquatic Photosynthesis (Blackwell, Oxford, 1997).

    Google Scholar 

  45. Duce, R. A. & Tindale, N. W. Atmospheric transport of iron and its deposition in the ocean. Limnol. Oceanogr. 36, 1715–1726 (1991).

    Article  ADS  CAS  Google Scholar 

  46. Carpenter, E. J. in Nitrogen in the Marine Environment (eds Carpenter, E. J. & Capone, D. G.) (Academic, New York, 1983).

    Google Scholar 

  47. Reuter, J. G. J. Theoretical Fe limitations of microbial N2 fixation in the oceans. Eos 63, 445 (1982).

    Google Scholar 

  48. Howarth, R. W., Marino, R. & Cole, J. J. Nitrogen fixation in freshwater, estuarine, & marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33, 688–701 (1988).

    ADS  CAS  Google Scholar 

  49. Martin, J. H. et al. Testing the iron hypothesis in the Equatorial Pacific. Nature 371, 123–129 (1994).

    Article  ADS  CAS  Google Scholar 

  50. Kolber, Z. S. et al. Iron limitation of phytoplankton photosynthesis in the Equatorial Pacific Ocean. Nature 371, 145–149 (1994).

    Article  ADS  CAS  Google Scholar 

  51. Behrenfeld, M., Bale, A., Kolber, Z., Aiken, J. & Falkowski, P. G. Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383, 508–511 (1996).

    Article  ADS  CAS  Google Scholar 

  52. Herguerra, J. C. & Berger, W. H. Glacial to postglacial drop in productivity in the western equatorial Pacific: mixing rate vs. nutrient concentration. Geology 22, 629–632 (1994).

    Article  ADS  Google Scholar 

  53. Ganeshram, R. S., Pedersen, T. F., Calvert, S. E. & Murray, J. W. Large changes in oceanic nutrient inventories from glacial to interglacial periods. Nature 376, 755–758 (1995).

    Article  ADS  CAS  Google Scholar 

  54. Altabet, M. A., Francois, R., Murray, D. W. & Prell, W. L. Climate-related variations in denitrification in the Arabian Sea from sediment 15N/14N ratios. Nature 373, 506–509 (1995).

    Article  ADS  CAS  Google Scholar 

  55. Sarmiento, J. & Orr, J. Three-dimensional simulations of the impact of Southern Ocean nutrient depletion on atmospheric CO2 and ocean chemistry. Limnol. Oceanogr. 36, 1928–1950 (1991).

    Article  ADS  CAS  Google Scholar 

  56. Peng, T.-H. & Broecker, W. S. Factors limiting the reduction of atmospheric CO2 by iron fertilization. Limnol. Oceanogr. 36, 1919–1927 (1991).

    Article  ADS  CAS  Google Scholar 

  57. Raynaud, D. et al. The ice record of greenhouse gases. Science 259, 926–934 (1993).

    Article  ADS  CAS  Google Scholar 

  58. Dickson, A. G. & Millero, F. W. A comparison of the equilibrium constant for the dissociation of carbonic acid in seawater media. Deep-Sea Res. 34, 1733–1743 (1987).

    Article  ADS  CAS  Google Scholar 

  59. Carpenter, E. J. & Capone, D. G. in Marine Pelagic Cyanobacteria: Trichodesrnium and Other Diazotrophs (eds Carpenter, E. J., Capone, D. G. & Rueter, J. G.) 211–217 (Academic, Dordrecht, 1992).

    Google Scholar 

  60. Gruber, N. & Sarmiento, S. L. Global patterns of marine fixation and denitrification revealed by the conservative tracer N*. Global Biogeochem. Cycles (in the press).

  61. Farrell, J. W., Pedersen, T. F., Calvert, S. E. & Nielsen, B. Glacial-interglacial changes in nutrient utilization in the equatorial Pacific Ocean. Nature 377, 514–517 (1995).

    Article  ADS  CAS  Google Scholar 

  62. Berger, A. Milankovitch theory and climate. Rev. Geophys. 26, 624–657 (1988).

    Article  ADS  Google Scholar 

  63. Shaffer, G. A non-linear climate oscillator controlled by biogeochemical cycling in the ocean: an alternative model of Quaternary ice ages cycles. Clim. Dyn. 4, 127–143 (1990).

    Article  Google Scholar 

  64. Hutchinson, G. E. A Treatise on Limnology (Wiley, New York, 1957).

    Google Scholar 

  65. Broecker, W. S. & Peng, T.-H. Tracers in the Sea (Eldigo Press, Lamont-Doherty Geological Observatory, New York, 1982).

    Google Scholar 

  66. Codispoti, L. A. in Productivity of the Ocean: Present and Past (eds Berger, W. H., Smetacek, V. S. & Wefer, G.) 377–394 (Wiley, New York, 1989).

    Google Scholar 

  67. Paytan, A., Kastner, M. & Chavez, F. P. Glacial to interglacial fluctuations in productivity in the equatorial Pacific as indicated by marine barite. Science 274, 1355–1357 (1996).

    Article  ADS  CAS  Google Scholar 

  68. Sarmiento, J. L. & Le Quéré, C. Oceanic carbon dioxide uptake in a model of century-scale global warming. Science 274, 1346–1350 (1996).

    Article  ADS  CAS  Google Scholar 

  69. Michaels, A. F. et al. Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean. Biogeochemistry 35, 181–226 (1996).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Oceanographic and Atmospheric Sciences Division, Brookhaven National Laboratory, Upton, New York, 11973, USA

    Paul G. Falkowski

Authors
  1. Paul G. Falkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Falkowski, P. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275 (1997). https://doi.org/10.1038/387272a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/387272a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing