Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen‐sulfate reducer consortium

Field and laboratory studies of anoxic sediments from Cape Lookout Bight, North Carolina, suggest that anaerobic methane oxidation is mediated by a consortium of methanogenic and sulfate-reducing bacteria. A seasonal survey of methane oxidation and CO2 reduction rates indicates that methane production was confined to sulfate-depleted sediments at all times of year, while methane oxidation occurred in two modes. In the summer, methane oxidation was confined to sulfate-depleted sediments and occurred at rates lower than those of CO2 reduction. In the winter, net methane oxidation occurred in an interval at the base of the sulfate-containing zone. Sediment incubation experiments suggest both methanogens and sulfate reducers were responsible for the observed methane oxidation. In one incubation experiment both modes of oxidation were partially inhibited by 2-bromoethanesulfonic acid (a specific inhibitor of methanogens). This evidence, along with the apparent confinement of methane oxidation to sulfate-depleted sediments in the summer, indicates that methanogenic bacteria are involved in methane oxidation. In a second incubation experiment, net methane oxidation was induced by adding sulfate to homogenized methanogenic sediments, suggesting that sulfate reducers also play a role in the process. We hypothesize that methanogens oxidize methane and produce hydrogen via a reversal of CO2 reduction. The hydrogen is efficiently removed and maintained at low concentrations by sulfate reducers. Pore water H2 concentrations in the sediment incubation experiments (while net methane oxidation was occurring) were low enough that methanogenic bacteria could derive sufficient energy for growth from the oxidation of methane. The methanogen-sulfate reducer consortium is consistent not only with the results of this study, but may also be a feasible mechanism for previously documented anaerobic methane oxidation in both freshwater and marine environments.

[1]  R. Garrels,et al.  A chemical model for sea water at 25 degrees C and one atmosphere total pressure , 1962 .

[2]  W. Reeburgh,et al.  Inhibition Experiments on Anaerobic Methane Oxidation , 1985, Applied and environmental microbiology.

[3]  Derek R. Lovley,et al.  Kinetic Analysis of Competition Between Sulfate Reducers and Methanogens for Hydrogen in Sediments , 1982, Applied and environmental microbiology.

[4]  P. Mitchell.  Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic type of Mechanism , 1961, Nature.

[5]  Bess B. Ward,et al.  Black Sea methane geochemistry , 1991 .

[6]  C. Martens,et al.  Factors that control the stable carbon isotopic composition of methane produced in an anoxic marine sediment , 1992 .

[7]  E. Faber,et al.  Methane oxidation in sediment and water column environments—Isotope evidence , 1986 .

[8]  C. Martens,et al.  The seasonality of nutrient regeneration in an organic-rich coastal sediment: Kinetic modeling of changing pore-water nutrient and sulfate distributions , 1989 .

[9]  D. Lovley,et al.  Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments , 1988 .

[10]  H. Sano,et al.  Catalytic combustion of hydrogen I—Its role in hydrogen utilization system and screening of catalyst materials , 1981 .

[11]  W. Reeburgh,et al.  Microbial methane consumption reactions and their effect on methane distributions in freshwater and marine environments1 , 1977 .

[12]  Stephen H. Zinder,et al.  Isolation and Characterization of a Thermophilic Bacterium Which Oxidizes Acetate in Syntrophic Association with a Methanogen and Which Grows Acetogenically on H2-CO2 , 1988, Applied and environmental microbiology.

[13]  M. Scranton.  Temporal variations in the methane content of the Cariaco Trench , 1988 .

[14]  C. Martens,et al.  Methane production from acetate and associated methane fluxes from anoxic coastal sediments. , 1981, Science.

[15]  Thomas D. Brock,et al.  Anaerobic Methane Oxidation: Occurrence and Ecology , 1980, Applied and environmental microbiology.

[16]  R. Barnes,et al.  Methane production and consumption in anoxic marine sediments , 1976 .

[17]  S. Zinder,et al.  Selective Inhibition by 2-Bromoethanesulfonate of Methanogenesis from Acetate in a Thermophilic Anaerobic Digestor , 1984, Applied and environmental microbiology.

[18]  A. Devol.  Methane oxidation rates in the anaerobic sediments of Saanich Inlet1 , 1983 .

[19]  W. Konings.  Do the stoichiometries of ion-linked transport system vary? , 1981 .

[20]  A comparison of methods for the quantification of bacterial sulfate reduction in coastal marine sediments , 1978 .

[21]  A. Zehnder,et al.  Methane formation and methane oxidation by methanogenic bacteria , 1979, Journal of bacteriology.

[22]  C. Martens,et al.  Biogeochemical cycling in an organic-rich coastal marine basin—I. Methane sediment-water exchange processes , 1980 .

[23]  S. Ferguson,et al.  Proton electrochemical gradients and energy-transduction processes. , 1982, Annual review of biochemistry.

[24]  P. Crill,et al.  Methane production from bicarbonate and acetate in an anoxic marine sediment , 1986 .

[25]  D. D. Marais,et al.  Distribution, abundance and carbon isotopic composition of gaseous hydrocarbons in Big-Soda Lake, Nevada-an Alkaline, Meromictic Lake , 1983 .

[26]  M. Lidstrom,et al.  Methane oxidation in Saanich Inlet during summer stratification , 1989 .

[27]  R. Gunsalus,et al.  Preparation of coenzyme M analogues and their activity in the methyl coenzyme M reductase system of Methanobacterium thermoautotrophicum. , 1978, Biochemistry.

[28]  Sachio Yamamoto,et al.  Solubility of hydrogen in water, sea water, and sodium chloride solutions , 1974 .

[29]  W. Reeburgh,et al.  METHANE CONSUMPTION IN CARIACO TRENCH WATERS AND SEDIMENTS , 1976 .

[30]  Allan H. Devol,et al.  Are high rates of sulphate reduction associated with anaerobic oxidation of methane? , 1981, Nature.

[31]  J. Cloern,et al.  Microbial and biogeochemical processes in Big Soda Lake, Nevada , 1988, Geological Society, London, Special Publications.

[32]  P. Novelli,et al.  Methane oxidation and methane fluxes in the ocean surface layer and deep anoxic waters , 1987, Nature.

[33]  P. Westermann.  The effect of incubation temperature on steady-state concentrations of hydrogen and volatile fatty acids during anaerobic degradation in slurries from wetland sediments , 1994 .

[34]  W. Reeburgh.  A major sink and flux control for methane in marine sediments; Anaerobic consumption , 1982 .

[35]  R. Oremland,et al.  Big Soda Lake (Nevada). 3. Pelagic methanogenesis and anaerobic methane oxidation1 , 1987 .

[36]  E. Canuel,et al.  Seasonal variations in 7Be activity in the sediments of Cape Lookout Bight, North Carolina , 1990 .

[37]  H. Schütz,et al.  Temperature limitation of hydrogen turnover and methanogenesis in anoxic paddy soil , 1987 .

[38]  T. Blackburn,et al.  Seasonal Rates of Methane Oxidation in Anoxic Marine Sediments , 1981, Applied and environmental microbiology.

[39]  W. Reeburgh.  Anaerobic methane oxidation: Rate depth distributions in Skan Bay sediments , 1980 .

[40]  P. Crill,et al.  Biogeochemical cycling in an organic-rich coastal marine basin. 6. Temporal and spatial variations in sulfate reduction rates , 1987 .

[41]  C. Martens,et al.  Biogeochemical cycling in an organic-rich coastal marine basin 4. An organic carbon budget for sediments dominated by sulfate reduction and methanogenesis , 1984 .

[42]  W. Reeburgh,et al.  Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation , 1988 .

[43]  R. Oremland,et al.  Use of “Specific” Inhibitors in Biogeochemistry and Microbial Ecology , 1988 .

[44]  R. Cicerone,et al.  Biogeochemical aspects of atmospheric methane , 1988 .

[45]  W. Balch,et al.  Specificity and biological distribution of coenzyme M (2-mercaptoethanesulfonic acid) , 1979, Journal of bacteriology.

[46]  R. Alberty.  Standard Gibbs free energy, enthalpy, and entropy changes as a function of pH and pMg for several reactions involving adenosine phosphates. , 1969, The Journal of biological chemistry.

[47]  G. King.  Metabolism of Trimethylamine, Choline, and Glycine Betaine by Sulfate-Reducing and Methanogenic Bacteria in Marine Sediments , 1984, Applied and environmental microbiology.

[48]  E. Canuel,et al.  Organic matter accumulation, diagenesis and burial in a rapidly depositing coastal sediment , 1992 .

[49]  J. Davis,et al.  Anaerobic oxidation of hydrocarbons by Desulfovibrio desulfuricans , 1966 .

[50]  J. Chanton,et al.  Lead-210 sediment geochronology in a changing coastal environment , 1983 .

[51]  R. Berner,et al.  Interstitial water chemistry of anoxic Long Island Sound sediments. 1. Dissolved gases1 , 1977 .

[52]  Bo Barker Jørgensen,et al.  Anaerobic methane oxidation rates at the sulfate‐methane transition in marine sediments from Kattegat and Skagerrak (Denmark) , 1985 .

[53]  C. Martens,et al.  Sulfate reduction rates and low molecular weight fatty acid concentrations in the water column and surficial sediments of the Black Sea , 1995 .