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The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean

Nature volume 388, pages 533–538 (1997)Cite this article

Abstract

Seven years of time-series observations of biogeochemical processes in the subtropical North Pacific Ocean gyre have revealed dramatic changes in the microbial community structure and in the mechanisms of nutrient cycling in response to large-scale ocean–atmosphere interactions. Several independent lines of evidence show that the fixation of atmospheric nitrogen by cyanobacteria can fuel up to half of the new production. These and other observations demand a reassessment of present views of nutrient and carbon cycling in one of the Earth′s largest biomes.

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Figure 1: Time series of N and P analyses of dissolved and particulate matter, expressed as N:P (mol:mol) ratios, for dissolved matter (upper panel), suspended particulate matter (centre panel) and exported particulate matter (lower panel).
Figure 2: Role of N2 fixation as a source of new nitrogen as determined by the N–P mass-balance model (see text).
Figure 3: Dissolved nitrogen pool dynamics for the upper portion of the water column (0–100 m) at station ALOHA during the 1991–92 ENSO event.
Figure 4: Dissolved phosphorus pool dynamics at station ALOHA for the period 1989–94, including the period corresponding to the extended 1991 –92 ENSO event.

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References

  1. Capone, D. G., Zehr, J. P., Paerl, H. W., Bergman, B. & Carpenter, E. J. Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221–1229 (1997).

    Article  CAS  Google Scholar 

  2. Dugdale, R. C., Menzel, D. W. & Ryther, J. H. Nitrogen fixation in the Sargasso Sea. Deep-Sea Res. 7, 297–300 (1961).

    CAS  ADS  Google Scholar 

  3. Goering, J. J., Dugdale, R. C. & Menzel, D. W. Estimates of rates of nitrogen uptake by Trichodesmium sp. in the tropical Atlantic Ocean. Limnol. Oceanogr. 11, 614–620 (1966).

    Article  CAS  ADS  Google Scholar 

  4. Carpenter, E. J. Nitrogen fixation by Oscillatoria (Trichodesmium) thiebautii in the southwestern Sargasso Sea. Deep-Sea Res. 20, 285–288 (1973).

    Google Scholar 

  5. Mague, T. H., Weare, N. M. & Holm-Hansen, O. Nitrogen fixation in the North Pacific Ocean. Mar. Biol. 24, 109–119 ( 1974).

    Article  CAS  Google Scholar 

  6. Carpenter E. J. & Price, C. C. Nitrogen fixation, distribution, and production of Oscillatoria (Trichodesmium) spp. in the western Sargasso and Caribbean Seas. Limnol. Oceanogr. 22, 60–72 ( 1977).

    Article  CAS  ADS  Google Scholar 

  7. Howarth, R. W., Marino, R., Lane, J. & Cole, J. J. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnol. Oceanogr. 33, 669– 687 (1988).

    CAS  ADS  Google Scholar 

  8. Capone, D. G. & Carpenter, E. J. Nitrogen fixation in the marine environment. Science 217, 1140– 1142 (1982).

    Article  CAS  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  10. Karl, D. M., Letelier, R., Hebel, D. V., Bird, D. F. & Winn, C. D. in Marine Pelagic Cyanobacteia: Trichodesmium and Other Diazotrophs(eds Carpenter, E. J., Capone, D. G. & Rueter, J. G.) 219–237 (Kluwer Academic, Dordrecht, (1992)).

    Book  Google Scholar 

  11. Altabet, M. A., Robinson, A. R. & Walstad, L. J. Amodel for the vertical flux of nitrogen in the upper ocean: simulating the alteration of isotopic ratios. J. Mar. Res. 44, 203–225 ( 1986).

    Article  CAS  Google Scholar 

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

    Article  ADS  Google Scholar 

  13. Lewis, M. R., Harrison, W. G., Oakey, N. S., Hebert, D. & Platt, T. Vertical nitrate fluxes in the oligotrophic ocean. Science 234, 870– 873 (1986).

    Article  CAS  ADS  Google Scholar 

  14. Martin, J. H., Knauer, G. A., Karl, D. M. & Broenkow, W. W. VERTEX: carbon cycling in the northeast Pacific. Deep-Sea Res. 34, 267–286 ( 1987).

    Article  CAS  ADS  Google Scholar 

  15. Karl, D. M. & Lukas, R. The Hawaii Ocean Time-series (HOT) Program: Background, rationale and field implementation. Deep-Sea Res. 43, 129–156 ( 1996).

    CAS  ADS  Google Scholar 

  16. Karl, D. M. HOT and the North Pacific gyre. Nature 378, 21–22 (1995).

    Article  ADS  Google Scholar 

  17. Trenberth, K. E. & Hurrell, J. W. Decadal atmosphere-ocean variations in the Pacific. Clim. Dyn. 9, 303–319 (1994).

    Article  Google Scholar 

  18. Karl, D. M.et al. Ecosystem changes in the North Pacific subtropical gyre attributed to the 1991–92 El Niño. Nature 373, 230–234 (1995).

    Article  CAS  ADS  Google Scholar 

  19. Carpenter, E. J., Capone, D. G. & Rueter, J. G. (eds) Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs(Kluwer Academic, Dordrecht, ( 1992)).

    Book  Google Scholar 

  20. Letelier, R. M. & Karl, D. M. 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 

  21. Carpenter, E. J. Physiology and ecology of marine planktonic Oscillatoria (Trichodesmium ). Mar. Biol. Lett. 4, 69– 85 (1983).

    CAS  Google Scholar 

  22. Mitsui, A.et al. Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. Nature 323, 720 –722 (1986).

    Article  CAS  ADS  Google Scholar 

  23. Redfield, A. C., Ketchum, B. H. & Richards, F. A. in The Sea: Ideas and Observations on Progress in the Study of the Seas Vol. 2(ed. Hill, M. N.) 26– 77 (Wiley Interscience, New York, (1963)).

    Google Scholar 

  24. Goldman, J. C., McCarthy, J. J. & Peavey, D. G. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279, 210–215 (1979).

    Article  CAS  ADS  Google Scholar 

  25. Sakshaug, E. & Holm-Hansen, O. Chemical composition of Skeletonema costatum (Grev.) Cleve and Pavlova (Monochrysis) lutheri (Droop) Green as a function of nitrate-, phoshate-, and iron-limited growth. J. Exp. Mar. Biol. Ecol. 29, 1– 34 (1977).

    Article  CAS  Google Scholar 

  26. Carpenter, E. J. & Price, C. C. Marine Oscillatoria (Trichodesmium): Explanation for aerobic nitrogen fixation without heterocysts. Science 191, 1278– 1280 (1976).

    Article  CAS  ADS  Google Scholar 

  27. Glibert, P. M. & Bronk, D. A. Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 60, 3996– 4000 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Capone, D. C., Ferrier, M. D. & Carpenter, E. J. Amino acid cycling in colonies of the planktonic marine cyanobacterium Trichodemium thiebautii. Appl. Environ. Microbiol. 60, 3989–3995 ( 1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Karl, D. M., Tien, G., Dore, J. & Winn, C. D. Total dissolved nitrogen and phosphorus concentrations at U.S.-JGOFS Station ALOHA: Redfield reconciliation. Mar. Chem. 41, 203–208 (1993).

    Article  CAS  Google Scholar 

  30. Winn, C. D., Mackenzie, F. T., Carrillo, C. J., Sabine, C. L. & Karl, D. M. Air-sea carbon dioxide exchange in the North Pacific subtropical gyre: Implications for the global carbon budget. Glob. Biogeochem. Cycles 8, 157– 163 (1994).

    Article  CAS  ADS  Google Scholar 

  31. Owens, N. J. P. Natural variations in 15N in the marine environment. Adv. Mar. Biol. 24, 389–451 ( 1987).

    Article  Google Scholar 

  32. Wada, E. & Hattori, A. Nitrogen in the Sea: Forms, Abundances, and Rate Processes(CRC, Boca Raton, Florida, (1991)).

    Google Scholar 

  33. Wada, E. in Isotope Marine Chemistry(eds Goldberg, E. D., Horibe, Y. & Saruhashi, K.) 375–398 (Uchida Rokakuho, Tokyo, ( 1980)).

    Google Scholar 

  34. Björkman, K. & Karl, D. M. Bioavailability of inorganic and organic phosphorus compounds to natural assemblages of microorganisms in Hawaiian coastal waters. Mar. Ecol. Prog. Ser. 111 , 265–273 (1994).

    Article  ADS  Google Scholar 

  35. Karl, D. M.et al. Seasonal and interannual variability in primary production and particle flux at Station ALOHA. Deep-Sea Res. II 43 , 539–568 (1996).

    Article  CAS  ADS  Google Scholar 

  36. Dugdale, R. C. & Goering, J. J. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol. Oceanogr. 12, 196–206 ( 1967).

    Article  CAS  ADS  Google Scholar 

  37. Rueter, J. G., Hutchins, D. A., Smith, R. W. & Unsworth, N. L. in Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs(eds Carpenter, E. J., Capone, D. G. & Rueter, J. G.) 289– 306 (Kluwer Academic, Dordrecht, (1992)).

    Book  Google Scholar 

  38. Tersol, V., Vink, S., Yuan, J. & Measures, C. I. Variations in iron, aluminum and berylium concentrations in surface waters at Station ALOHA. Eos 76, OS65 ( 1996).

    Google Scholar 

  39. Armstrong, F. A., Williams, P. M. & Strickland, J. D. H. Photo-oxidation of organic matter in seawater by ultraviolet radiation, analytical and other applications. Nature 211, 481–483 ( 1966).

    Article  CAS  ADS  Google Scholar 

  40. Karl, D. M., Dore, J. E., Hebel, D. V. & Winn, C. in Marine Particles: Analysis and Characterization(eds Hurd, D. C. & Spencer, D. W.) 71–77 (Am. Geophys. Un., Washington DC, (1991)).

    Google Scholar 

  41. Garside, C. Achemiluminescent technique for the determination of nanomolar concentrations of nitrate and nitrite in seawater. Mar. Chem. 11, 159–167 (1982).

    Article  CAS  Google Scholar 

  42. Karl, D. M. & Tien, G. MAGIC: A sensitive and precise method for measuring dissolved phosphorus in aquatic environments. Limnol. Oceanogr. 37, 105–116 ( 1992).

    Article  CAS  ADS  Google Scholar 

  43. Stewart, W. D. P., Fitzgerald, G. P. & Burris, R. H. In situ studies on N2 fixation using the acetylene reduction technique. Proc. Natl Acad. Sci. USA 58, 2071–2078 (1967).

    Article  CAS  ADS  Google Scholar 

  44. Honjo, S. & Doherty, K. W. Large aperture time-series sediment traps; design objectives, construction and application. Deep-Sea Res. 35, 133–149 ( 1988).

    Article  CAS  ADS  Google Scholar 

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Acknowledgements

We thank the HOT Program scientists and staff, and the officers and crew members of the research vessels used in our field work for making this study possible, and E. Laws for comments on the manuscript. This work was supported in part by the National Science Foundation.

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Authors and Affiliations

  1. Department of Oceanography, School of Ocean and Earth Science and Technology, University of Hawaii, Honolulu, 96822, Hawaii, USA

    D. Karl, L. Tupas, J. Dore & D. Hebel

  2. College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, 97331-5503, Oregon , USA

    R. Letelier

  3. Aquasearch Inc., 73-4460 Queen Kaahumanu Highway, Suite 110, Kailua-Kona, 96740, Hawaii, USA

    J. Dore

  4. Department of Oceanography, Dalhousie University, Halifax, B3H 4J1, Nova Scotia, Canada

    J. Christian

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Correspondence to D. Karl.

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Karl, D., Letelier, R., Tupas, L. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997). https://doi.org/10.1038/41474

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