Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 7 8 2010 10.5194/bg-7-2327-2010 http://www.biogeosciences.net/7/2327/2010/ http://www.biogeosciences.net/7/2327/2010/bg-7-2327-2010.html http://www.biogeosciences.net/7/2327/2010/bg-7-2327-2010.pdf 2327 2337 2010-08-06 Heterotrophic denitrification vs. autotrophic anammox – quantifying collateral effects on the oceanic carbon cycle W. Koeve wkoeve@ifm-geomar.de P. Kähler IFM-GEOMAR, Leibniz-Institut für Meereskunde, Düsternbrooker Weg 20, 24105 Kiel, Germany The conversion of fixed nitrogen to N₂ in suboxic waters is estimated to contribute roughly a third to total oceanic losses of fixed nitrogen and is hence understood to be of major importance to global oceanic production and, therefore, to the role of the ocean as a sink of atmospheric CO₂. At present heterotrophic denitrification and autotrophic anammox are considered the dominant sinks of fixed nitrogen. Recently, it has been suggested that the trophic nature of pelagic N₂-production may have additional, "collateral" effects on the carbon cycle, where heterotrophic denitrification provides a shallow source of CO₂ and autotrophic anammox a shallow sink. Here, we analyse the stoichiometries of nitrogen and associated carbon conversions in marine oxygen minimum zones (OMZ) focusing on heterotrophic denitrification, autotrophic anammox, and dissimilatory nitrate reduction to nitrite and ammonium in order to test this hypothesis quantitatively. For open ocean OMZs the combined effects of these processes turn out to be clearly heterotrophic, even with high shares of the autotrophic anammox reaction in total N₂-production and including various combinations of dissimilatory processes which provide the substrates to anammox. In such systems, the degree of heterotrophy (ΔCO₂:ΔN₂), varying between 1.7 and 6.5, is a function of the efficiency of nitrogen conversion. On the contrary, in systems like the Black Sea, where suboxic N-conversions are supported by diffusive fluxes of NH₄⁺ originating from neighbouring waters with sulphate reduction, much lower values of ΔCO₂:ΔN₂ can be found. However, accounting for concomitant diffusive fluxes of CO₂, the ratio approaches higher values similar to those computed for open ocean OMZs. Based on this analysis, we question the significance of collateral effects concerning the trophic nature of suboxic N-conversions on the marine carbon cycle. Altabet, M. A., Francois, R., Murray, D. W., and Prell, W. L.: Climate-related variations in denitrification in the Arabian Sea from sediment $^15$N/$^14$N ratios, Nature, 373, 506–509, 1995. Anderson, L. A.: On the hydrogen and oxygen content of marine phytoplankton, Deep-Sea Res. I, 42, 1675–1680, 1995. Brettar, I. and Rheinheimer, G.: Denitrification in the Central Baltic: evidence for H₂S-oxidation as motor of denitrification at the oxic-anoxic interface, Mar. Ecol. Prog. Ser., 77, 157–169, 1991. Brewer, P. G. and Peltzer, E. T.: Limits to marine life, Science, 324, 347–348, 2009. Broda, E.: Two kinds of lithotrophs missing in nature, Z. Allg. Mikrobiol., 17, 491–493, 1977. Brzezinski, M. A.: Vertical distribution of ammonium in stratified oligotrophic waters, Limnol. Oceanogr., 33, 1176–1182, 1988. Canfield, D. E.: Models of oxic respiration, denitrification and sulfate reduction in zones of coastal upwelling, Geochim. Cosmochim. Acta, 70, 5753–5765, 2006. Cline, J. D. and Richards, F. A.: Oxygen deficient conditions and nitrate reduction in the eastern tropical North Pacific Ocean, Limnol. Oceanogr., 17, 885–900, 1972. Codispoti, L. A.: Is the ocean losing nitrate?, Nature, 376, 724, 1995. Codispoti, L. A. and Christensen, J. P.: Nitrification, denitrification and nitrous oxide cycling in the eastern tropical South Pacific ocean, Mar. Chem., 16, 277–300, 1985. Codispoti, L. A., Friederich, G. E., Murray, J. W., and Sakamoto, C. M.: Chemical variability in the Black Sea: implications of continuous vertical profiles that penetrated the oxic/anoxic interface, Deep-Sea Res., 38(S2), S691–S710, 1991. Devol, A. H.: Denitrification including anammox, in: Nitrogen in the Marine Environment, 2nd Edition, edited by: Capone, D., Bronk, D., Mulholland, M., and Carpenter, E., Elsevier, Amsterdam, 263–301, 2008. Devol, A. H., Uhlenhopp, A. G., Naqvi, S. W. A., et al.: Denitrification rates and excess nitrogen gas concentrations in the Arabian Sea oxygen deficient zone, Deep-Sea Res., 53, 1533–1547, 2006. Fuchsman, C. A., Murray, J. W., and Konovalov, S. K.: Concentration and natural stable isotope profiles of nitrogen species in the Black Sea, Mar. Chem., 111, 90–105, 2008. Ganeshram, R. S., Pedersen, T. F., Calvert, S. E., and Murray, J. W.: Large changes in oceanic nutrient inventories from glacial to interglacial periods, Nature, 376, 755–757, 1995. Gibb, S. W., Mantoura, R. F. C., Liss, P. S., and Barlow, R. G.: Distributions and biogeochemistries of methylamines and ammonium in the Arabian Sea, Deep-Sea Res. II, 46, 593–615, 1999. Hamersley, M. R., Lavik, G., Woebken, D., et al.: Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone, Limnol. Oceanogr., 52, 923–933, 2007. Hanning, M., Lavik, G., Kuypers, M. M. M., et al.: Shift from denitrification to anammox after inflow events in the central Baltic Sea, Limnol. Oceanogr., 52, 1336–1345, 2007. Hofmann, M. and Schellnhuber, H.-J.: Oceanic acidification affects marine carbon pump and triggers extended marine oxygen holes, P. Natl. Acad. Sci., 106, 3017–3022, doi:10.1073/pnas.0813384106, 2009. Hulth, S., Aller, R. C., Canfield, D. E., et al.: Nitrogen removal in marine environments: recent findings and future research challenges, Mar. Chem., 94, 125–145, 2005. Jin, X. and Gruber, N.: Offsetting the radiative benefit of ocean iron fertilization by enhancing \chemN_2O emissions, Geophys. Res. Lett., 30, 2249, doi:10.1029/2003GL018458, 2003. Kartal, B., Kuypers, M. M. M., Lavik, G., et al.: Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium, Environ. Microbiol., 9, 635–642, 2007. Key, R. M., Kozyr, A., Sabine, C. L., Lee, K., Wanninkhof, R., Bullister, J. L., Feely, R. A., Millero, F. J., Mordy, C., and Peng, T.-H.: A global ocean carbon climatology: results from Global Data Analysis Project (GLODAP), Global Biogeochem. Cycles, 18, GB4031, doi:10:1029/2004GB002247, 2004. Konovalov, S. K., Fuchsman, C. A., Belokopitov, V., and Murray, J. W.: Modelling the distribution of nitrogen species and isotopes in the water column of the Black Sea, Mar. Chem., 111, 106–124, 2008. Kuenen, J. G.: Anammox bacteria: from discovery to application, Nature Reviews Microbiol., 6, 320–326, 2008. Kuypers, M. M. M., Sllekers, A. O., Lavik, G., et al.: Anaerobic ammonium oxidation by anammox bacteria in the Black Sea, Nature, 422, 608–611, 2003. Kuypers, M. M. M., Lavik, G., Woebken, D., et al.: Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation, P. Natl. Acad. Sci. USA, 102, 6478–6483, 2005. Lam, P., Lavik, G., Jensen, M. M., et al.: Revising the nitrogen cycle of the Peruvian oxygen minimum zone, P. Natl. Acad. Sci. USA, 106, 4752–4757, 2009. Laws, E. A.: Photosynthetic quotients in the open ocean, Deep-Sea Res., 38, 143–167, 1991. Matear, R. J. and Hirst, A. C.: Long term changes in the dissolved oxygen concentrations in the ocean caused by protracted global warming, Global Biogeochem. Cycles, 17, 1125, doi:10.1029/2002GB001997, 2003. Martens-Habbena, W., Berube, P. M., Urakawa, H., et al.: Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria, Nature, 461, 976–979, doi:10.1038/nature08465, 2009. Molina, V. and Farías, L.: Aerobic ammonium oxidation in the oxycline and oxygen minimum zone of the eastern tropical South Pacific off northern Chile ($\sim $20° S), Deep-Sea Res. II, 56, 1032–1041, 2009. Molina, V., Farías, L., Eissler, Y., et al.: Ammonium cycling under a strong oxygen gradient associated with the oxygen minimum zone off northern Chile ($\sim $23° S), Mar. Ecol. Prog. Ser., 288, 35–43, 2005. Mulder, A., van de Graaf, A. A., Robertson, L. A., and Kuenen, J. G.: Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor, FEMS Microbiol. Ecol., 16, 177–183, 1995. Murray, J. W., Fuchsman, C., Kirkpatrick, J., Paul, B., and Konovalov, S. K.: Species and $\delta ^15$N signatures of nitrogen transformations in the suboxic zone of the Black Sea, Oceanography, 18, 36–47, 2005. Oschlies, A., Schulz, K. G., Riebesell, U., and Schmittner, A.: Simulated 21st century's increase in oceanic suboxia by CO₂-enhanced biotic carbon export, Global Biogeochem. Cycles, 22, GB4008, doi:10.1029/2007GB003147, 2008. Paulmier, A., Kriest, I., and Oschlies, A.: Stoichiometries of remineralisation and denitrification in global biogeochemical ocean models, Biogeosciences, 6, 923–935, doi:10.5194/bg-6-923-2009, 2009. Redfield, A. C., Ketchum, B. H., and Richards, F. A.: The influence of organisms on the composition of seawater, in: The sea, Vol 2, edited by: Hill, M. N., John Wiley and Sons, New York, 26–77, 1963. Richards, F. A.: Anoxic basins and fjords, in: Chemical Oceanography, edited by: Riley, J. P. and Skirrow, G., Academic Press, London, 611–643, 1965. Schmidt, I., Sliekers, O., Schmid, M., et al.: Aerobic and anaerobic ammonia oxidizing bacteria – competitors or natural partners?, FEMS Microbiol. Ecol., 39, 175–181, 2002. Sen Gupta, R. and Koroleff, F.: A quantitative study of nutrient fractions and a stoichiometric model of the Baltic, Estuar. Coast. Mar. Sci., 1, 335–360, 1973. Sen Gupta, R. and Naqvi, S. W. A.: Chemical oceanography of the Indian Ocean, north of the aquator, Deep-Sea Res., 31, 671–706, 1984. Stramma, L., Johnson, G. C., Sprintall, J., and Mohrholz, V.: Expanding oxygen-minimum zones in the tropical oceans, Science, 320, 655–658, 2008. Strous, M., Heijnen, J. J., Kuenen, J. G., and Jetten, M. S. M.: The sequencing batch reactor as a powerful tool to study very slowly growing micro-organisms, Appl. Microbiol. Biotechnol., 50, 589–596, 1998. Stumm, W. and Morgan, J. J.: Aquatic chemistry – chemical equilibria and rates in natural waters, John Wiley & Sons, Inc., New York, 1022~pp., 1996. Thamdrup, B. and Dalsgaard, T.: Production of \chemN_2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments, Appl. Environ. Microbiol., 68, 1312–1318, 2002. Thamdrup, B., Dalsgaard, T., Jensen, M. M., et al.: Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile, Limnol. Oceanogr., 51, 2145–2156, 2006. Thomas, W. H.: On denitrification in the northeastern tropical Pacific Ocean, Deep-Sea Res., 13, 1109–1114, 1966. Tijhuis, L., Van Loosdrecht, M. C. M., and Heijnen, J. J.: A thermodynamically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth, Biotechnol. Bioeng., 42, 509–519, 1993. van de Graaf, A. A., de Bruijn, P., Robertson, L., Jetten, M. S. M., and Kuenen, J. G.: Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor, Microbiol., 142, 2187–2196, 1996. Van Mooy, B. A. S., Keil, R. G., and 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. Volkov, I. I. and Rozanov, A. G.: Fundamentals of biohydrochemistry of anoxic basins, Oceanology, 46, 803–816, 2006. Voss, M. and Montoya, J. P.: Oceans apart, Nature, 461, 49–50, 2009. Ward, B. B.: Nitrification in marine systems, in: Nitrogen in the Marine Environment, 2nd Edition, edited by: Capone, D., Bronk, D., Mulholland, M., and Carpenter, E., Elsevier, Amsterdam, 2008. Ward, B. B., Capone, D. G., and Zehr, J. P.: What's new in the nitrogen cycle?, Oceanography, 20, 101–109, 2007. Ward, B. B., Devol, A. H., Rich, J. J., Chang, B. X., Bulow, S. E., Naik, H., Pratihary, A., and Jayakumar, A.: Denitrification as the dominant nitrogen loss process in the Arabian Sea, Nature, 461, 78–81, 2009. Yoshinari, T. and Knowles, R.: Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria, Biochem. Biophys. Res. Comm., 69, 705–710, 1976. Zafiriou, O. C., Ball, L. A., and Hanley, Q.: Trace nitrite in oxic waters, Deep-Sea Res., 39, 1329–1347, 1992. Zumft, W. G.: Cell biology and molecular basis of denitrification, Microbiol. Mol. Biol. Rev., 61, 533–616, 1997.