References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-7-1099-2010

Methane production in aerobic oligotrophic surface water in the central Arctic Ocean

Damm

¹ Helmke

¹ Thoms

¹ Schauer

¹ Nöthig

¹ Bakker

² Kiene

R. P.

³ ⁴

Alfred Wegener Institute for Polar and Marine Research, P.O. Box 12061, 27515 Bremerhaven, Germany

Royal Netherlands Institute for Sea Research, Texel, The Netherlands

Department of Marine Sciences, University of South Alabama, Mobile, Alabama, USA

Dauphin Island Sea Lab, Dauphin Island, Alabama, USA

19 03 2010

7 3 1099 1108

2010

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

This article is available from https://bg.copernicus.org/articles/7/1099/2010/bg-7-1099-2010.html

The full text article is available as a PDF file from https://bg.copernicus.org/articles/7/1099/2010/bg-7-1099-2010.pdf

A methane surplus relative to the atmospheric equilibrium is a frequently observed feature of ocean surface water. Despite the common fact that biological processes are responsible for its origin, the formation of methane in aerobic surface water is still poorly understood. We report on methane production in the central Arctic Ocean, which was exclusively detected in Pacific derived water but not nearby in Atlantic derived water. The two water masses are distinguished by their different nitrate to phosphate ratios. We show that methane production occurs if nitrate is depleted but phosphate is available as a P source. Apparently the low N:P ratio enhances the ability of bacteria to compete for phosphate while the phytoplankton metabolite dimethylsulfoniopropionate (DMSP) is utilized as a C source. This was verified by experimentally induced methane production in DMSP spiked Arctic sea water. Accordingly we propose that methylated compounds may serve as precursors for methane and thermodynamic calculations show that methylotrophic methanogenesis can provide energy in aerobic environments.

References 1

Atkins, P. W.: Physical Chemistry, 4. Edn., Oxford University Press, Oxford, 1990.

Boulygina, E. S., Kuznetsov, B. B., Marusina, A. I., Tourova, T. P., Kravchenko, I. K., Bykova, S. A., Kolganova, T. V. and Galchenko, V. F.: A study of nucleotide sequences of nifH genes of some methanotrophic bacteria. Microbiology (English translation of Mikrobiologiya) 71, 425–432, 2002.

Carmack, E. C., Aargard, K., Swift, J. H., McDonald, R. W., McLaughlin, F. A., Jones, P. E., Perkin, R. G., Smith, J. N., Ellis, K. M. and Killius, L. R.: Changes in temperature and tracer distributions within the Arctic Ocean: Results from the 1994 Arctic Ocean section, Deep-Sea Res Pt. II, 44(8), 1487–1502, https://doi.org/10.1016/S0967-0645(97)00056-8, 1997.

Charlson, R. J., Lovelock, J. E., Andreae, M. O. and Warren, S. G.: Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate, Nature, 326, 655–661, 1987.

Craig, H.: Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide, Geochim. Cosmochim. Ac., 12, 133–149, 1957.

Curran, M. A. J., Jones, G. B. and Burton, H.: Spatial distribution of dimethylsulfide and dimethylsulfoniopropionate in the Australian sector of the southern Ocean, J. Geophys. Res., 103, 16667–16689, 1998.

Damm, E., Mackensen, A., Budeus, G., Faber, E. and Hanfland, C.: Pathways of methane in seawater: Plume spreading in an Arctic shelf environment (SW-Spitsbergen), Cont. Shelf Res., 25, 1433–1452, 2005.

Damm, E., Schauer, U., Rudels, B., and Hass, C.: Excess of bottom-released methane in an Arctic shelf sea polynya in winter, Cont. Shelf Res., 27, 1692–1701, https://doi.org/10.1016/j.-csr.2007.02.003, 2007. \blackbox

Damm, E., Kiene, R.P., Schwarz, J. Falck, E. and Dieckmann, G.: Methane cycling in Arctic shelf water and its relationship with phytoplankton biomass and DMSP, Mar. Chem., 109, 45–59, 2008.

Dedysh, S. N., Ricke, P. and Liesack, W.: NifH ans NifD phylogenies: an evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria, Microbiology, 150, 1301–1313, 2004.

Edler, L.: Recommendations on methods for marine biological studies in the Baltic Sea, Phytoplankton and chlorophyll, BMB Publ., 5, 1–38, 1979.

Evans, C. A. and O'Reily, J. E.: A handbook for the measurement of chlorophyll a in netplankton and nanoplankton, BIOMASS Handbook, 9, 1–14, 1987.

Forster, G., Upstill-Godard, R. C., Gist, N., Robinson, C., Uher, G., and Woodward, E. M. S.: Nitrous oxide and methane in the Atlantic Ocean between 50° N and 52° S: Latitudinal distribution and sea-to-air flux, Deep-Sea. Res. Pt. II, 56, 964–976, https://doi.org/10.1016/jdsr2.2008.12.002, 2008. \blackbox

Gallon, J. R.: Tansley Review No. 44, Reconciling the incompatible: N2 fixation and O2, New Phytol., 122, 571–609, 1992.

Gerdes, B., Brinkmeyer, R., Dieckmann, G., and Helmke, E.: Influence of crude oil on changes of bacterial communities in Arctic sea-ice, FEMS Microbiology Ecology, 53, 129–139, 2005.

Grasshoff, K., Ehrhardt, M., and Kremling, K.: Methods of seawater Analysis. Verlag Chemie, Weinheim, 419 pp, 1983.

Gruber, N. and Sarmiento, J. L.: Global patterns of nitrogen fixation and denitrification, Global Biogeochem. Cy., 11, 235–266, 1997.

Hobbie, J. E., Daley, R. J. and Jasper, S.: Use of Nuclepore filters for counting bacteria by fluorescence microscopy, Appl. Environ. Microbiol., 33, 1225–1228, 1977.

Jeong, K. S., Cho, J. H., Kim, S. R., Hyun, S., and Tsunogai, U.: Geophysical and geochemical observations on actively seeping hydrocarbon gases on the south-eastern Yellow Sea continental shelf, Geo-Mar. Lett., 24, 53–62, 2004.

Jones, P. E., Anderson, L. G. and Swift, J. H.: Distribution of Atlantic and Pacific waters in the upper Arctic Ocean: Implications for circulation; Geophys. Res. Lett., 25(6), 765–768, 1998.

Jones, P. E., Anderson, L. G., Jutterström, S., Mintrop, L., and Swift, J. H.: Pacific freshwater, river water and sea ice meltwater across Arctic Ocean basins: Results from the 2005 Beringia Expedition, J. Geophys. Res, 113, C08012, https://doi.org/10.1029/2007JC004124, 2008.

Karl, D. M., Beversdorf, L., Björkman, K., Church, M. J., Martinez, A., and DeLong, E. F.: Aerobic production of methane in the sea, Nat. Geosci., 1, 473–478, https://doi.org/10.1038/ngeo234, 2008.

Kiene, R. P.: Methane, Nitrogen Oxides and Halomethanes, in: Microbial Production and Consumption of Greenhouse Gases, edited by: Rogers, J. E. and Whitman, W. B., 111–146, ASM Washington DC, 1991.

Kiene, R. P., Linn, L. J and Bruton, J. A.: New and important roles for DMSP in marine microbial communities, J. Sea Res., 43, 209–224, 2000.

Kvenfolden, K., Lilley, M., Lorenson, T. D., Barnes, P. W. and McLaughlin, E.: The Beaufort Sea continental shelf as a seasonal source of atmospheric methane, Geophys. Res. Lett., 20, 2459–2462, 1993.

Lammers, S., Suess, E., and Hovland, M.: A large methane plume east of Bear Island (Barents Sea): implications for the marine methane cycle, Geol. Rundsch., 84, 59–66, 1994.

Lamontagne, R. A., Swinnerton, J. W., Linnebom, V. J. and Smith, W. D.: Methane concentrations in various marine environments, J. Geophys. Res., 78, 5317–5324, 1973.

Lide, D. R.: CRC Handbook of Chemistry and Physics, 80. Edn., CRC Press, Inc., Boca Raton, FL, 1999.

Moran, J. J., Beal, E. J., Vrentas, J. M., Orphan, V. J., Freeman, K. H., and House, C. H.: Methyl sulphides as intermediates in the anaerobic oxidation of methane, Environ. Microbiol., 10, 162–173, 2008.

Moran, M. A., Gonzalez, J. M., and Kiene, R. P.: Linking a bacterial taxon to sulfur cycling in the sea: studies of the marine Roseobacter group, Geomicrobiol. J., 20, 375–388, 2003.

Moran, M. A., Belas, R., Schell, M. A., Gonzalez, J. M., Sun, F., Sun, S., Binder, B. J., Edmonds, B., Ye, J. W., Orcutt, B., Howard, E. C., Meile, C., Palefsky, W., Goesmann, A., Ren, Q., Paulsen, I., Ulrich, L. E., Thompson, L. S., Saunders, E. and Buchan, A.: Ecological genomics of marine Roseobacters, Appl. Environ. Microbiol., 73, 4559–4569, 2007.

Murphy, J. and Riley, J. P.: A modified single solution method for the determination of phosphate in natural waters, Anal. Chim. Acta, 27, 31–36, 1962.

Myzer, G., de Waal, E., and Uitterlinden, A.: Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA, Appl. Environ. Microbiol., 59, 695–700, 1993.

Pabi, S., v. Dijken, G. L., and Arrigo, K. R.: Primary production in the Arctic Ocean, 1998–2006, J. Geophys. Res., 113, CO8005, https://doi.org/10.1029/2007JC004578, 2008.

Pernthaler, A., Pernthaler, J., and Amann, R.: Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria, Appl. Environ. Microbiol., 68, 3094–3101, 2002.

Pinhassi, J., Simo, R., Gonzalez, J. M., Vila, M., Alonso-Saez, L., Kiene, R. P., Moran, M. A., and Pedros-Alio, C.: Dimethylsulfoniopropionate turnover is linked to the composition and dynamics of the bacterioplankton assemblage during a microcosm phytoplankton bloom, Appl. Environ. Microbiol., 71, 7650–7660, 2005.

Rabe, B., Schauer, U., Mackensen, A., Karcher, M., Hansen, E., and Beszczynska-Möller, A.: Freshwater components and transports in the Fram Strait �- recent observations and changes since the late 1990s, Ocean Sci., 5, 219–233, 2009.

Sakshaug, E.: Primary and secondary production in the Arctic Seas, in The Organic Carbon Cycle in the Arctic Ocean, edited by: R. Stein and R.W. McDonald, 57–81, Springer, Berlin, 2003.

Sander, R.: Compilation of Henry's Law Constants for Inorganic and Organic Species of Potential Importance in Environmental Chemistry (Version 3), <a href="http://www.henrys-law.org">http://www.henrys-law.org</a>, 1999.

Schauer, U.: The expedition ARKTIS-XXII/2 of the research vessel "Polarstern" in 2007. Reports on Polar and Marine Research, AWI, Bremerhaven, 579, 2008.

Schink, B.: Energetics of syntrophic cooperation in methanogenic degradation, Microbiol. Mol. Biol. Rev., 61, 262–280, 1997.

Scranton, M. I. and Brewer, P. G.: Occurrence of methane in the near surface waters of the western subtropical North-Atlantic, Deep-Sea Res., 24, 127–138, 1977.

Shakhova, N. and Semiletov, I.: Methane release and coastal environment in the East Siberian Arctic shelf, J. Marine Syst., 66, 227–243, 2007.

Simo, R., Archer, S. D., Pedros-Alio, C., Gilpin, L., and Stelfox-Widdicombe, C. E.: Coupled dynamics of dimethylsulfoniopropionate and dimethylsulfide cycling and the microbial food web in surface waters of the North Atlantic, Limnol. Oceanogr., 47, 53–61, 2002.

Stefels, J.: Physiological aspects of the production and conversion of DMSP in marine algae and higher plants, J. Sea Res. 43, 183–197, 2000.

Tallant, T. C. and Krycki, J. A.: Methylthiol: coenzyme M methyltransferase from methanosarcina barkeri, an enzyme of methangenesis from dimethylsulfide and methylmercatopropionate, J. Bacteriol., 179, 6902–6911, 1997.

Thingstad, T. F., Bellerby, R. G. J., Bratbak, G., Borsheim, K. Y., Egge, J. K., Heldal, M., Larsen, A., Neill, C., Nejstgaard, J., Norland, S., Sandaa, R. A., Skjoldal, E. F., Tanaka, T., Thyraug, R., and Töpper, B.: Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem, Nature, 455, 387–390, https://doi.org/10.1038/nature07235, 2008.

Wallner, G., Amann, R., and Beisker, W.: Optimizing fluorescence in situ hybridization with ribosomal-RNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms, Cytometry, 14, 136–143, 1993.

Woodgate, R. A., Aagaard, K., and Weingartner T. J.: A year in the physical oceanography of the Chukchi Sea: Moored measurements from autumn 1990–1991, Deep-Sea Res. Pt. II, 52, 3116–3149, https://doi.org/10.1016/j.dsr2.2005.10.016, 2005. \blackbox

Yamamoto-Kawai, M., Carmack, E. C., and McLaughlin, F. A.: Nitrogen balance and Arctic throughflow, Nature, 443, 43, 2006.

Zehr, J. P. and McReynolds, L. A.: Use of degenerate oligonucleotides for amplification of nifH gene from the marine cyanobacterium Trichodesmium thiebautii, Appl. Environ. Microbiol., 55, 2522–2526, 1989.