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.

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.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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

References

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

    CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  Google Scholar 

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

    ADS  CAS  Article  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)

    ADS  CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  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)

    ADS  CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  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)

    CAS  Article  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)

    CAS  Article  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)

    ADS  CAS  Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tage Dalsgaard.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01526

Further reading

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

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