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Isotopic ratios of nitrite as tracers of the sources and age of oceanic nitrite

Abstract

Nitrite is a central intermediate in the marine nitrogen cycle, and is generally found at low concentrations in the ocean. However, nitrite accumulates at the base of the sunlit surface ocean. The origin of this ubiquitous feature, known as the primary nitrite maximum, is debated and has been difficult to resolve through short-term isotope tracer incubations. Here, we use measurements of the dual isotopic composition of nitrite to evaluate the sources, sinks and average rates of nitrite turnover in the primary nitrite maximum in the Arabian Sea. We determined the rate of abiotic oxygen isotope exchange between nitrite and water, as well as equilibrium isotope effects, under a variety of conditions in a series of laboratory experiments. We used these data to model nitrite isotope data from several sites in the Arabian Sea. The results suggest that ammonia oxidation is the primary source of nitrite at most sites. Steady-state nitrite turnover times of 33–178 days correspond to ammonia oxidation rates of 9–30 nM per day at these sites. We suggest that a similar approach could be used to determine the rates of nitrite turnover in other environments, including the secondary nitrite maximum in low-oxygen regions.

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Figure 1: A box model diagram illustrating the processes that control δ15N and δ18O of nitrite in the PNM.
Figure 2: Time courses of δ 18 O NO 2 values during three different experiments in which pH, temperature and salinity were varied.
Figure 3: Interpretation of δ 15 N NO 2 and δ 18 O NO 2 values from the Arabian Sea PNM.

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References

  1. Dore, J. E. & Karl, D. M. Nitrification in the euphotic zone as a source for nitrite, nitrate, and nitrous oxide at Station ALOHA. Limnol. Oceanogr. 41, 1619–1628 (1996).

    Article  Google Scholar 

  2. Kiefer, D. A., Olson, R. J. & Holmhansen, O. Another look at nitrite and chlorophyll maxima in central North Pacific. Deep-Sea Res. 23, 1199–1208 (1976).

    Google Scholar 

  3. Lipschultz, F., Zafiriou, O. C. & Ball, L. A. Seasonal fluctuations of nitrite concentrations in the deep oligotrophic ocean. Deep-Sea Res. II 43, 403–419 (1996).

    Article  Google Scholar 

  4. Zafiriou, O. C., Ball, L. A. & Hanley, Q. Trace nitrite in oxic waters. Deep-Sea Res. A 39, 1329–1347 (1992).

    Article  Google Scholar 

  5. Brandhorst, W. Nitrification and denitrification in the Eastern Tropical North Pacific. Journal du Conseil Permanent International pour l’Exploration de la Mer 25, 2–20 (1959).

    Google Scholar 

  6. 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  Google Scholar 

  7. Codispoti, L. A. Interesting times for marine N2O. Science 327, 1339–1340 (2010).

    Article  Google Scholar 

  8. Freing, A., Wallace, D. W. R. & Bange, H. W. Global oceanic production of nitrous oxide. Phil. Trans. R. Soc. B 367, 1245–1255 (2012).

    Article  Google Scholar 

  9. Lomas, M. W. & Lipschultz, F. Forming the primary nitrite maximum: Nitrifiers or phytoplankton? Nature Med. 51, 2453–2467 (2006).

    Google Scholar 

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

    Article  Google Scholar 

  11. Harrison, W. G. & Harris, L. R. Isotope-dilution and its effects on measurements of nitrogen and phosphorus uptake by oceanic microplankton. Mar. Ecol. 27, 253–261 (1986).

    Article  Google Scholar 

  12. Clark, D. R., Rees, A. P. & Joint, I. Ammonium regeneration and nitrification rates in the oligotrophic Atlantic Ocean: Implications for new production estimates. Limnol. Oceanogr. 53, 52–62 (2008).

    Article  Google Scholar 

  13. Jenkins, W. J. Oxygen utilization rates in North-Atlantic sub-tropical gyre and primary production in oligotrophic systems. Nature 300, 246–248 (1982).

    Article  Google Scholar 

  14. Platt, T. et al. Biological production of the oceans—the case for a consensus. Mar. Ecol. 52, 77–88 (1989).

    Article  Google Scholar 

  15. Karl, D. M., Laws, E. A., Morris, P., Williams, P. J. L. & Emerson, S. Global carbon cycle—metabolic balance of the open sea. Nature 426, 32–32 (2003).

    Article  Google Scholar 

  16. Luz, B. & Barkan, E. Assessment of oceanic productivity with the triple-isotope composition of dissolved oxygen. Science 288, 2028–2031 (2000).

    Article  Google Scholar 

  17. Knapp, A. N., Sigman, D. M., Lipschultz, F., Kustka, A. B. & Capone, D. G. Interbasin isotopic correspondence between upper-ocean bulk DON and subsurface nitrate and its implications for marine nitrogen cycling. Glob. Biogeochem. Cycles 25, GB4004 (2011).

    Article  Google Scholar 

  18. Casciotti, K. L., McIlvin, M. & Buchwald, C. Oxygen isotopic exchange and fractionation during bacterial ammonia oxidation. Limnol. Oceanogr. 55, 753–762 (2010).

    Article  Google Scholar 

  19. Buchwald, C., Santoro, A. E., McIlvin, M. R. & Casciotti, K. L. Oxygen isotopic composition of nitrate and nitrite produced by nitrifying cocultures in and natural marine assemblages. Limnol. Oceanogr. 57, 1361–1375 (2012).

    Article  Google Scholar 

  20. Granger, J., Sigman, D. M., Needoba, J. A. & Harrison, P. J. Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton. Limnol. Oceanogr. 49, 1763–1773 (2004).

    Article  Google Scholar 

  21. Granger, J., Sigman, D. M., Rohde, M. M., Maldonado, M. T. & Tortell, P. D. N and O isotope effects during nitrate assimilation by unicellular prokaryotic and eukaryotic plankton cultures. Geochim. Cosmochim. Acta 74, 1030–1040 (2010).

    Article  Google Scholar 

  22. Casciotti, K. L., Böhlke, J. K., McIlvin, M. R., Mroczkowski, S. J. & Hannon, J. E. Oxygen isotopes in nitrite: Analysis, calibration, and equilibration. Anal. Chem. 79, 2427–2436 (2007).

    Article  Google Scholar 

  23. Fawcett, S. E., Lomas, M., Casey, J. R., Ward, B. B. & Sigman, D. M. Assimilation of upwelled nitrate by small eukaryotes in the Sargasso Sea. Nature Geosci. 4, 717–722 (2011).

    Article  Google Scholar 

  24. Montoya, J. P. & Voss, M. Nitrogen cycling in suboxic waters: Isotopic signatures of nitrogen transformation in the Arabian Sea oxygen minimum zone. Past Present Water Column Anoxia 64, 259–281 (2006).

    Google Scholar 

  25. Checkley, D. M. & Miller, C. A. Nitrogen isotope fractionation by oceanic zooplankton. Deep-Sea Res. A 36, 1449–1456 (1989).

    Article  Google Scholar 

  26. Macko, S. A., Estep, M. L. F., Engel, M. H. & Hare, P. E. Kinetic fractionation of stable nitrogen isotopes during amino-acid transamination. Geochim. Cosmochim. Acta 50, 2143–2146 (1986).

    Article  Google Scholar 

  27. Waser, N. A. D., Harrison, P. J., Nielsen, B., Calvert, S. E. & Turpin, D. H. Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom. Limnol. Oceanogr. 43, 215–224 (1998).

    Article  Google Scholar 

  28. Santoro, A. E. & Casciotti, K. L. Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J. 5, 1796–1808 (2011).

    Article  Google Scholar 

  29. Casciotti, K. L. Inverse kinetic isotope fractionation during bacterial nitrite oxidation. Geochim. Cosmochim. Acta 73, 2061–2076 (2009).

    Article  Google Scholar 

  30. Buchwald, C. & Casciotti, K. L. Oxygen isotopic fractionation and exchange during bacterial nitrite oxidation. Limnol. Oceanogr. 55, 1064–1074 (2010).

    Article  Google Scholar 

  31. Yool, A., Martin, A. P., Fernandez, C. & Clark, D. R. The significance of nitrification for oceanic new production. Nature 447, 999–1002 (2007).

    Article  Google Scholar 

  32. Newell, S. E., Babbin, A. R., Jayakumar, A. & Ward, B. B. Ammonia oxidation rates and nitrification in the Arabian Sea. Glob. Biogeochem. Cycles 25, GB4016 (2011).

    Article  Google Scholar 

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

    Article  Google Scholar 

  34. Ward, B. B., Olson, R. J. & Perry, M. J. Microbial nitrification rates in the primary nitrite maximum off Southern-California. Deep-Sea Res. A 29, 247–255 (1982).

    Article  Google Scholar 

  35. Dore, J. E., Popp, B. N., Karl, D. M. & Sansone, F. J. A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters. Nature 396, 63–66 (1998).

    Article  Google Scholar 

  36. Santoro, A. E., Buchwald, C., McIlvin, M. R. & Casciotti, K. L. Isotopic signature of N2O produced by marine ammonia-oxidizing archaea. Science 333, 1282–1285 (2011).

    Article  Google Scholar 

  37. Bunton, C. A., Halevi, E. A. & Llewellyn, D. R. Oxygen exchange between nitric acid and water. J. Chem. Soc. 4913–4916 (1952).

  38. Betts, R. H. & Voss, R. H. Kinetics of oxygen exchange between sulfite ion and water. Canad. J. Chem. 48, 2035–2041 (1970).

    Article  Google Scholar 

  39. Gomori, G. Preparation of buffers for use in enzyme studies. Methods Enzymol. 1, 138–146 (1955).

    Article  Google Scholar 

  40. Robert-Baldo, G. L., Morris, M. J. & Byrne, R. H. Spectrophotometric determination of seawater pH using phenol red. Anal. Chem. 57, 2564–2567 (1985).

    Article  Google Scholar 

  41. Durst, R. A. & Staples, B. R. Tris/tris HCl-standard buffer for use in physiologic pH range. Clin. Chem. 18, 206–208 (1972).

    Google Scholar 

  42. McIlvin, M. R. & Altabet, M. A. Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal. Chem. 77, 5589–5595 (2005).

    Article  Google Scholar 

  43. Strickland, J. D. H. & Parsons, T. R. A practical handbook of seawater analysis. Bull. Fish. Res. Board Canada 167, 1–310 (1972).

    Google Scholar 

  44. Clayton, T. D. & Byrne, R. H. Spectrophotometric seawater pH measurements—total hydrogen-ion concentration scale calibration of M-Cresol purple and at-sea results. Deep-Sea Res. I 40, 2115–2129 (1993).

    Article  Google Scholar 

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Acknowledgements

We would like to thank M. McIlvin and B. Peters for help collecting data. We would like to thank the chief scientist B. Ward and the captain and crew of the R/V Revelle for assistance in the collection of nitrite isotope samples in the Arabian Sea. Financial support was provided from NSF/OCE 07-48674 and 11-40404 to K.L.C.

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C.B. and K.L.C. designed the experiments and the model formulations. C.B. performed the experiments and model calculations. C.B. and K.L.C. authored the paper.

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Correspondence to Carolyn Buchwald or Karen L. Casciotti.

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Buchwald, C., Casciotti, K. Isotopic ratios of nitrite as tracers of the sources and age of oceanic nitrite. Nature Geosci 6, 308–313 (2013). https://doi.org/10.1038/ngeo1745

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