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N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica

Abstract

In oxygen-depleted zones of the open ocean, and in anoxic basins and fjords, denitrification (the bacterial reduction of nitrate to give N2) is recognized as the only significant process converting fixed nitrogen to gaseous N2. Primary production in the oceans is often limited by the availability of fixed nitrogen such as ammonium or nitrate1, and nitrogen-removal processes consequently affect both ecosystem function and global biogeochemical cycles. It was recently discovered that the anaerobic oxidation of ammonium with nitrite—the ‘anammox’ reaction, performed by bacteria—was responsible for a significant fraction of N2 production in some marine sediments2. Here we show that this reaction is also important in the anoxic waters of Golfo Dulce, a 200-m-deep coastal bay in Costa Rica, where it accounts for 19–35% of the total N2 formation in the water column. The water-column chemistry in Golfo Dulce is very similar to that in oxygen-depleted zones of the oceans—in which one-half to one-third of the global nitrogen removal is believed to occur3,4. We therefore expect the anammox reaction to be a globally significant sink for oceanic nitrogen.

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Figure 1: Water column data.
Figure 2: Isotopic enrichment experiments.

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References

  1. Falkowski, P. G., Barber, R. T. & Smetacek, V. Biogeochemical controls and feedbacks on ocean primary production. Science 281, 200–206 (1998)

    Article  CAS  PubMed  Google Scholar 

  2. Thamdrup, B. & Dalsgaard, T. Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl. Environ. Microbiol. 68, 1312–1318 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11, 235–266 (1997)

    Article  ADS  CAS  Google Scholar 

  4. Codispoti, L. A. et al. The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the anthropocene? Sci. Mar. 65 (suppl. 2), 85–105 (2001)

    Article  CAS  Google Scholar 

  5. Thamdrup, B., Canfield, D. E., Ferdelman, T. G., Glud, R. N. & Gundersen, J. K. A biogeochemical survey of the anoxic basin Golfo Dulce, Costa Rica. Rev. Biol. Trop. 44, 19–33 (1996)

    Google Scholar 

  6. Vargas, J. A. Pacific coastal ecosystems of Costa Rica with emphasis on the Golfo Dulce and adjacent areas: A synoptic view based on the R.V. Victor Hensen expedition 1993/94 and previous studies. Preface. Rev. Biol. Trop. 44, U1–U4 (1996)

    Google Scholar 

  7. Lipschultz, F. et al. Bacterial transformations of inorganic nitrogen in the oxygen-deficient waters of the Eastern Tropical South-Pacific ocean. Deep-Sea Res. 37, 1513–1541 (1990)

    Article  ADS  CAS  Google Scholar 

  8. Bange, H. W. et al. A revised nitrogen budget for the Arabian Sea. Glob. Biogeochem. Cycles 14, 1283–1297 (2000)

    Article  ADS  CAS  Google Scholar 

  9. Deutsch, C., Gruber, N., Key, R. M., Sarmiento, J. L. & Ganachaud, A. Denitrification and N2 fixation in the Pacific Ocean. Glob. Biogeochem. Cycles 15, 483–506 (2001)

    Article  ADS  CAS  Google Scholar 

  10. Richards, F. A. in Advances in Water Pollution Research (ed. Pearson, E. A.) 215–232 (Pergamon, London, 1965)

    Google Scholar 

  11. Richards, F. A. in Chemical Oceanography (eds Riley, J. P. & Skirrow, G.) 611–645 (Academic, London, 1965)

    Google Scholar 

  12. van de Graaf, A. et al. Anaerobic oxidation of ammonium is a biologically mediated process. Appl. Environ. Microbiol. 61, 1246–1251 (1995)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Dalsgaard, T. & Thamdrup, B. Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl. Environ. Microbiol. 68, 3802–3808 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Knowles, R. Denitrification. Microbiol. Rev. 46, 43–70 (1982)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Luther, G. W. I., Sundby, B., Lewis, P. J. & Silverburg, N. Interactions of manganese with the nitrogen cycle: alternative pathways to dinitrogen. Geochim. Cosmochim. Acta. 61, 4043–4052 (1997)

    Article  ADS  CAS  Google Scholar 

  16. Hulth, S., Aller, R. C. & Gilbert, F. Coupled anoxic nitrification/manganese reduction in marine sediments. Geochim. Cosmochim. Acta. 63, 49–66 (1999)

    Article  ADS  CAS  Google Scholar 

  17. Murray, J. W., Lee, B., Bullister, J. & Luther, G. W. in Environmental Degradation of the Black Sea: Challenges and Remedies (eds Besiktepe, S. T., Ünlüata, Ü. & Bologa, A. S.) 75–91 (Kluwer Academic, Dordrecht, 1999)

    Book  Google Scholar 

  18. Nielsen, L. P. Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiol. Ecol. 86, 357–362 (1992)

    Article  CAS  Google Scholar 

  19. Van Mooy, B. A. S., Keil, R. G. & Devol, A. H. Impact of suboxia on sinking particulate organic carbon: Enhanced carbon flux and preferential degradation of amino acids via denitrification. Geochim. Cosmochim. Acta. 66, 457–465 (2002)

    Article  ADS  CAS  Google Scholar 

  20. 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 

  21. Cline, J. D. & Richards, F. A. Oxygen deficient conditions and nitrate reduction in the Eastern tropical northern Pacific Ocean. Limnol. Oceanogr. 17, 885–900 (1972)

    Article  ADS  CAS  Google Scholar 

  22. Naqvi, S. W. A. Some aspects of the oxygen-deficient conditions and denitrification in the Arabian Sea. J. Mar. Res. 45, 1049–1072 (1987)

    Article  CAS  Google Scholar 

  23. Otte, S. et al. Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl. Environ. Microbiol. 65, 3148–3157 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Braman, R. S. & Hendrix, S. A. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal. Chem. 61, 2715–2718 (1989)

    Article  CAS  PubMed  Google Scholar 

  25. Grasshoff, K., Ehrhardt, M. & Kremling, K. Methods of Seawater Analysis (Verlag Chemie, Weinheim, 1983)

    Google Scholar 

  26. Hall, P. O. J. & Aller, R. C. Rapid, small-volume, flow injection analysis for CO2 and NH4+ in marine and freshwaters. Limnol. Oceanogr. 37, 1113–1119 (1992)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank J. A. Vargas for assistance in arranging field work, and E. Ruiz and D. Morera for assistance during sampling. We also thank L. Salling, P. Søholt, K. G. Lauridsen, E. Frandsen, T. Quottrup, M. V. Skjærbæk and A. Haxen for analytical work. D.E.C., J.P. and B.T. were supported by the Danish National Research Foundation and the Danish National Science Research Council.

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Correspondence to Tage Dalsgaard.

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Dalsgaard, T., Canfield, D., Petersen, J. et al. N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422, 606–608 (2003). https://doi.org/10.1038/nature01526

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