Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 6 12 2009 10.5194/bg-6-3053-2009 http://www.biogeosciences.net/6/3053/2009/ http://www.biogeosciences.net/6/3053/2009/bg-6-3053-2009.html http://www.biogeosciences.net/6/3053/2009/bg-6-3053-2009.pdf 3053 3069 2009-12-17 Chemolithoautotrophic production mediating the cycling of the greenhouse gases N₂O and CH₄ in an upwelling ecosystem L. Farías lfarias@profc.udec.cl C. Fernández J. Faúndez M. Cornejo M. E. Alcaman Laboratorio de Procesos Oceanográficos y Clima (PROFC), Departamento de Oceanografía and Centro de Investigación Oceanográfica en el Pacífico Suroriental (COPAS, Universidad de Concepción, Casilla 160-C, Concepción, Chile Laboratoire d'Océanographie biologique de Banyuls, Université Paris VI, CNRS-UMR 7621, BP44, 66651 Banyuls-sur-Mer Cedex, France The high availability of electron donors occurring in coastal upwelling ecosystems with marked oxyclines favours chemoautotrophy, in turn leading to high N₂O and CH₄ cycling associated with aerobic NH₄⁺ (AAO) and CH₄ oxidation (AMO). This is the case of the highly productive coastal upwelling area off central Chile (36° S), where we evaluated the importance of total chemolithoautotrophic vs. photoautotrophic production, the specific contributions of AAO and AMO to chemosynthesis and their role in gas cycling. Chemolithoautotrophy was studied at a time-series station during monthly (2007–2009) and seasonal cruises (January 2008, September 2008, January 2009) and was assessed in terms of the natural C isotopic ratio of particulate organic carbon (δ¹³POC), total and specific (associated with AAO and AMO) dark carbon assimilation (CA), and N₂O and CH₄ cycling experiments. At the oxycline, δ¹³POC averaged −22.2‰; this was significantly lighter compared to the surface (−19.7‰) and bottom layers (−20.7‰). Total integrated dark CA in the whole water column fluctuated between 19.4 and 2.924 mg C m^−2 d^−1, was higher during active upwelling, and contributed 0.7 to 49.7% of the total integrated autotrophic CA (photo plus chemoautotrophy), which ranged from 135 to 7.626 mg C m^−2 d^−1, and averaged 20.3% for the whole sampling period. Dark CA was reduced by 27 to 48% after adding a specific AAO inhibitor (ATU) and by 24 to 76% with GC7, a specific archaea inhibitor. This indicates that AAO and AMO microbes (most of them archaea) were performing dark CA through the oxidation of NH₄⁺ and CH₄. Net N₂O cycling rates varied between 8.88 and 43 nM d^−1, whereas net CH₄ cycling rates ranged from −0.41 to −26.8 nM d^−1. The addition of both ATU and GC7 reduced N₂O accumulation and increased CH₄ consumption, suggesting that AAO and AMO were responsible, in part, for the cycling of these gases. These findings show that chemically driven chemolithoautotrophy (with NH₄⁺ and CH₄ acting as electron donors) could be more important than previously thought in upwelling ecosystems, raising new questions concerning its relevance in the future ocean. % vor jede Referenz Bakum, A.: Global climate changes and the intensification of coastal upwelling. Science, 241, 148–201,1990. Bange, H., Rapsomanikis, S., and Andreae, M. O.: Nitrous oxide in coastal waters, Global Biogeochem. Cy., 10, 197–207, 1996. Coban-Yildiz, Y., Altabet, M. A., Yilmaz, A., and Suleyman, S.: Carbon and nitrogen isotopic ratios of suspended particulate organic matter (SPOM) in the Black Sea water columns, Deep Sea Res. II., 53, 1875–1892, 2006. Cornejo, M., Farías, L., and Gallegos, M.: Seasonal variability in N₂O levels and air-sea N₂O fluxes over the continental shelf waters off central Chile ($\sim $36° S), Prog. Oceanogr., 75, 383–395, 2007. Crutzen, P. J.: Methane's sink and source, Nature, 350, 380–391, 1991. Daneri, G., Dellarossa, V., Quiñones, R. A., Jacob, B., Montero, P., and Ulloa, O.: Primary production and community respiration in the Humboldt Current System off Chile and associated oceanic areas, Mar. Ecol. Prog. Ser., 197, 41–49, 2000. Deutsch, C., Emerson, S. R., and Thompson, L.: Fingerprints of climate change in North Pacific oxygen, Geophys. Res. Lett., 32, L16604, doi:10.1029/2005GL023190, 2005. Elkins, J. W., Wofsy, S. C., Mcelroy, M. B., Kolb, C., and Kaplan, W. A.: Aquatic sources and sinks for nitrous oxide, Nature, 275, 602–606, 1978. Eppley, R. W.: New production: history, methods, problems, in: Productivity of the ocean: present and past, edited by: Berger W. H., Smetacek, V. S., and Wefer, G., John Wiley & Sons Limited, Chichester, New York, 85–97, 1989. Escribano, R., Daneri, G., Farías, L., Gallardo, V. A., González, H. E., Gutierrez, D., Lange, C. B., Morales, C. E., Pizarro, O., Ulloa, O., and Braun, M.: Biological and chemical consequences of the 1997-1998 El Niño in the Chilean coastal upwelling system: a synthesis, Deep Sea Res., 51, 2389–2411, 2004. Farías, L., Graco, M., and Ulloa, O.: Nitrogen cycling in continental shelf sediments of the upwelling ecosystem off central Chile, Deep Sea Res. II., 51, 2491–2505, 2004. Farías, L. and Cornejo, M.: Effect of seasonal change in bottom water oxygenation on sediment N-oxide and N₂O cycling in the coastal upwelling regime off central Chile (36.5° S), Prog. Oceanogr., 75, 561–575, 2007. Farías, L., Castro-González, M., Cornejo, M., Charpentier, J., Fa\'undez, J., Boontanon, N., and Yoshida, N.: Denitrification and nitrous oxide cycling within the upper oxycline of the oxygen minimum zone off the eastern tropical South Pacific, Limnol. Oceanogr., 54, 132–144, 2009. Fry, B., Jannasch, H. W., Molyneaux, S. J., Wirsen, C. O., Muramoto, J. A., and King, S.: Stable isotope studies of the carbon, nitrogen ans sulfur cycles in the Black Sea and Cariaco trench, Deep-Sea Res., 38, S1003–S1019,1991. Ginestet, P., Audic, J., Urbain, V., and Block, J.: Estimation of nitrifying bacterial activities by measuring oxygen uptake in the presence of the metabolic inhibitors Allylthiourea and Azide, Appl. Environ. Microb., 64, 2266–2268, 1998. Grantham, B. A., Chan, F., Nielsen, K., David, S., Fox, D. S., Barth, J. A., Huyer, A., Lubchenco, J., and Menge, B. A.: Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northerm Pacific, Nature, 429, 749–754, 2004. Grasshoff, K., Ehrhardt, M., and Kremling, K.: Methods of seawater analysis: Second Edition. Springer-Verlag, Basel, Switzerland, 419~pp., 1983. Hanson R. and Hanson, T. E.: Methanotrophic Bacteria, Microb Rev., 60, 439–471, 2000. Hayes, J. M.: Fractionation of carbon and hydrogen isotopes in biosynthetic processes, in: Stable isotope geochemistry, edited by: Valley J. W. and Cole, D. R., Rev. Mineral Geochem., 43, 225–278, 2001. Helly, J. and Levin, L.: Global distribution of naturally occurring marine hypoxia on continental margins, Deep-Sea Res., 51, 1159–1168, 2004. Ho, T.-Y., Taylor, G., Astor, Y., Varela, R., Taylor, G. T., and Scranton, M. I.: Vertical and temporal variability of redox zonation in the water column of the Cariaco: implications for organic carbon oxidation pathways, Mar. Chem., 86, 89–104, 2004. Holmes, R. M., Aminot, A., Kérouel, R., Hooker, B. A., and Peterson, B. J.: A simple and precise method for measuring ammonium in marine and freshwater ecosystems, Can. J. Fish. Aquat. Sci., 56, 1801–1808, 1999. IPCC.: Climate Change: The Scientific Basis, edited by: Houghton, J. T., Ding, Y., Griggs, D. J., Noguer, M., van der Linden, P. J., Dai, X., Maskell, K., and Johnson, C. A., Cambridge University Press, 2001. Janson, P. B. M., Malandrin, L., and Johansson, H.: Cell cycle arrest in Archea by the Hypusination inhibitor N$^1$-Guanyl-1, 7-Diaminoheptane, J. Bacteriol., 182, 1158–1161, 2000. Jørgensen, B. B. and Gallardo, V. A.: \textitThioploca spp.: Filamentous sulfur bacteria with nitrate vacuoles, FEMS Microb. Ecol., 28, 301–313, 1999. Jost, G., Zubkov, M. V., Yakushev, E., Labrenz, M., and Jurgens, K.: High abundance and dark CO₂ fixation of chemolithotrophic prokaryoyes in anoxic water of the Baltic Sea, Limnol. Oceanogr., 53, 14–22, 2008. Joyce, S. B. and Hollibaugh, J. T.: Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments, Science, 270, 623–625, 1995. Labrenz, M., Jost, G., Pohl, C., Beckmann, S., Martens-Habbena, W., and Jürgens, K.: Impact of different in vitro Electron donor/acceptor conditions on potential chemolithoautotrophic communities from marine pelagic redoxclines, Appl. Environ. Microb., 71, 6664–6672, 2005. Lavik, G., Stührmann, T., Brüchert, V., Van der Plas, A., Mohrholz, V., Lam, P., Mußmann, M., Fuchs, B. M., Amann, R., Lass, U., and Kuypers, M. M. M.: Detoxification of sulphidic African shelf waters by blooming chemolithotrophs, Nature, 457, 581–584, 2009. Law, C. S. and Owens, N. J. P.: Significance flux of atmospheric nitrous oxide from the northwest Indian Ocean, Nature, 346, 826–828, 1990. Lein, A. Y., Pimenov, N. V., and Galchenko, V. F.: Bacterial chemosynthesis and methanotrophy in the Manus and Lau basis ecosystems, Mar. Geol., 142, 47–56, 1997. Levipan, H. A., Quiñones, R. A., and Urrutia, H.: A time series of prokaryote secondary production in the oxygen minimum zone of the Humboldt Current System, Prog. Oceanogr.,75, 531–549, 2007a. Levipan, H. A., Quiñones, R. A., Johansson, H. E., and Urrutia, H.: Methylotrophic Methanogens in the Water Column of an Upwelling Zone with a Strong Oxygen Gradient Off Central Chile, Microb. Environ., 22, 268–278, 2007b. Madigan, M., Martinko, J., and Parker, J.: Brock Biology of Microorganism. Nutrition and Metabolism, Prentice Hall, New Jersey, 1011~pp., 2003. Naqvi, S. W. A., Jayakumar, D. A., Narvekar, P. V., Naik, H., Sarma, V. V., D'Souza, W., Joseph, S., and George, M. D.: Increased marine production of N₂O due to intensifying anoxia on the Indian continental shelf, Nature, 408, 346–349, 2000. Nevison, C. D., Weiss, R. F., and Erickson, D. J.: Global oceanic emissions of nitrous oxide, J. Geophys. Res, 100, 15809–15820, 1995. Nevison, C. D., Lueker, T. J., and Weiss, R. F.: Quantifying the nitrous oxide source from coastal upwelling, Global Biogeochem. Cy., 18, GB1018, doi:10.1029/2003GB002110, 2004. Owens, N. J. P., Law, C. S., Mantoura, R. F., Burkill, P. H., and Llewellyn, C. A.: Methane flux to the atmosphere from the Arabian Sea, Nature, 354, 293–296, 1991. Pauly, D. and Christensen, V.: Primary production required to sustain global fisheries, Nature, 374, 255–257, 1995. Pimenov, N. V. and Neretin, L.: Composition and activities of microbial communities involved in carbon, sulfur, nitrogen and manganese cycling in the oxic/anoxic interface of the Black Sea, edited by: Neretin, L. N., Past and present Water Column Anoxia. NATO Science Series: IV: Earth and Environmental Sciences, 501–502, 2006. Quiñones, R. A., Levipan, H. A., and Urrutia, H.: Spatial and temporal variability of planktonic archaeal abundance in the Humboldt Current System off Chile, Deep Sea Res II., 56(16), 1073–1072, 2009. Rykaczewski, R. R. and Checkley Jr., D. M.: Influence of ocean winds on the pelagic ecosystem in upwelling regions, Poner el nombre complete, P. Natl. Acad. Sci., 105, 1965–1970, doi:10.1073pnas.0711777105, 2008. Schubert, C. J., Coolen, M. J. L., Neretin, N. L., and Schippers, A.: Aerobic and anaerobic methanotrophs in the Black Sea water column, Environ. Microbiol., 8, 1844–1856, 2006. Sobarzo, M. and Djurfeldt, L.: Coastal upwelling process on a continental shelf limited by submarine canyons, Concepción, central Chile, J.Geophys. Res., 109, C12012, doi:10.1029/2004JC002350, 2004. Slawyk, G. and Collos, Y.: $^13$C and $^15$N uptake by marine phytoplankton III. Interactions in euphotic zone profiles of stratified oceanic areas, Mar. Ecol. Prog. Ser., 19, 223–231, 1984. Stramma, L., Johnson, G. C., Sprintall J., and Mohrholz, V.: Expanding Oxygen-Minimum Zones in the Tropical Oceans, Science, 320, 655–658, 2008. Strub, P. T., Mesías, J., Montecinos, V., Rutllant J., and Salinas, S.: Coastal ocean circulation off western south America, in: The Sea, edited by: Robinson A. R. and Brink, K. H, John Wiley & Sons, 273–313, 1998. Taylor, G. T., Iabichella, M., Tung-yuan, H., Scranton, M., Thunell, R., Muller-Karger, F., and Varela, R.: Chemoautotrophy in the redox transition zone of the Cariaco Basin: A significant midwater source of organic carbon production, Limnol. Oceanogr., 46, 148–163, 2001. Thamdrup, B. and Canfield, D. E.: Pathway of carbon oxidation in the continental margin off central Chile, Limnol.Oceanogr., 41, 1629–1650, 1996. Trotsenko, Y. A. and Murrell, J. C.: Metabolic aspects of aerobic obligate methanotrophy, Adv. Appl. Microbiol., 63, 183–229, 2008. Upstill-Goddard, R. C., Barnes, J., and Owens, N. J.: Nitrous oxide and methane during the SW mosoon in the Arabian Sea/northwestern Indian Ocean, J. Geophys. Res., 104, 30067–30084, 1999. Wanninkhof, R.: Relationship between wind speed and gas exchange over the ocean, J. Geophys. Res., 97, 7373–7382, 1992. Ward, B. B., Glover, H. E., and Lipschultz, F.: Chemoautotrophic activity and nitrification in the oxygen minimum zone off Peru, Deep Sea Res., 36, 1031–1051, 1989. Weisenburg, D. A. and Guinasso, N. L.: Equilibrium solubilities of methane, carbon monoxide and hydrogen in water and seawater, J. Chem. Eng. Data, 24, 354–360, 1979. Weiss, R. F. and Price, B. A.: Nitrous oxide solubility in water and seawater, Mar. Chem., 8, 347–359, 1980. Zopfi, J., Ferdelman, T. G., Jorgensen, B. B., Teske, A., and Thamdrup, B.: Influence of water columns dynamics on sulfide oxidation and other major biogeochemcial processes in the chemocline of Mariager Fkord (Denmark), Mar. Chem., 74, 29–51, 2001.