Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 5 6 2008 10.5194/bg-5-1587-2008 http://www.biogeosciences.net/5/1587/2008/ http://www.biogeosciences.net/5/1587/2008/bg-5-1587-2008.html http://www.biogeosciences.net/5/1587/2008/bg-5-1587-2008.pdf 1587 1599 2008-11-24 Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions B. Orcutt C. Meile cmeile@uga.edu Department of Marine Sciences, University of Georgia, Athens, GA 30 602, USA Marine Environmental Biology Section, University of Southern California, Los Angeles, CA 90 089, USA Anaerobic oxidation of methane (AOM) is the main process responsible for the removal of methane generated in Earth's marine subsurface environments. However, the biochemical mechanism of AOM remains elusive. By explicitly resolving the observed spatial arrangement of methanotrophic archaea and sulfate reducing bacteria found in consortia mediating AOM, potential intermediates involved in the electron transfer between the methane oxidizing and sulfate reducing partners were investigated via a consortium-scale reaction transport model that integrates the effect of diffusional transport with thermodynamic and kinetic controls on microbial activity. Model simulations were used to assess the impact of poorly constrained microbial characteristics such as minimum energy requirements to sustain metabolism and cell specific rates. The role of environmental conditions such as the influence of methane levels on the feasibility of H₂, formate and acetate as intermediate species, and the impact of the abundance of intermediate species on pathway reversal were examined. The results show that higher production rates of intermediates via AOM lead to increased diffusive fluxes from the methane oxidizing archaea to sulfate reducing bacteria, but the build-up of the exchangeable species can cause the energy yield of AOM to drop below that required for ATP production. Comparison to data from laboratory experiments shows that under the experimental conditions of Nauhaus et al. (2007), none of the potential intermediates considered here is able to support metabolic activity matching the measured rates. Barnes, R. O. and Goldberg, E. D.: Methane production and consumption in anaerobic marine sediments, Geology, 4, 297–300, 1976. Boetius, A., Ravenschlag, K., Schubert, C. J., Rickert, D., Widdel, F., Gieseke, A., Amann, R., Jørgensen, B. B., Witte, U., and Pfannkuche, O.: A marine microbial consortium apparently mediating anaerobic oxidation of methane, Nature, 407, 623–626, 2000. Boudreau, B. P.: Diagenetic models and their implementation, Springer-Verlag, 414~pp., 1997. Chistoserdova, L., Vorholt, J. A., and Lidstrom, M. E.: A genomic view of methane oxidation by aerobic bacteria and anaerobic archaea, Genome Biology, 6(208), doi:10.1186/gb-2005-6-2-208, available at: http://genomebiology.com/2005/6/2/208, 2005. Dale, A. W., Regnier, P., and van~Cappellen, P.: Bioenergetic controls on anaerobic oxidation of methane (AOM) in coastal sediments: A theoretical analysis, Am. J. Sci., 306, 246–294, 2006. Devol, A. H., Anderson, J. J., Kuivila, K., and Murrary, J. W.: A model for coupled sulfate reduction and methane oxidation in the sediments of Saanich Inlet, Geochim. Cosmochim. Ac., 48, 993–1004, 1984. Deppenmeier, U.: Redox-driven proton translocation in methanogenic Archaea, Cell. Mol. Life Sci., 59, 1513–1533, 2002. Finke, N.: The role of volatile fatty acids and hydrogen in the degradation of organic matter in marine sediments, Ph.D thesis, University of Bremen, 2003. Girguis, P. R., Cozen, A. E., and DeLong, E. F.: Growth and population dynamics of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria in a continuous-flow bioreactor, Appl. Environ. Microb., 71(7), 3725–3733, 2005. Girguis, P. R., Orphan, V. J., Hallam, S. J., and DeLong, E. F.: Growth and methane oxidation rates of anaerobic methanotrophic archaea in a continuous-flow bioreactor, Appl. Environ. Microb., 69(9), 5472–5482, 2003. Hallam, S. J., Girguis, P. R., Preston, C. M., Richardson, P. M., and DeLong, E. F.: Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea, Appl. Environ. Microb., 69(9), 5483–5491, 2003. Hallam, S. J., Putnam, N., Preston, C. M., Detter, J. C., Rokhsar, D., Richardson, P. M., and DeLong, E. F.: Reverse methanogenesis: Testing the hypothesis with environmental genomics, Science, 305, 1457–1462, 2004. Hinrichs, K.-U., Hayes, J. M., Sylva, S. P., Brewer, P. G., and DeLong, E. F.: Methane-consuming archaebacteria in marine sediments, Nature, 398, 802–805, 1999. Hoehler, T. M., Alperin, M. J., Albert, D. B., and Martens, C. S.: Field and laboratory studies of methane oxidation in an anoxic marine sediment – evidence for a methanogen-sulfate reducer consortium, Global Biogeochem. Cy., 8, 451–463, 1994. Hoehler, T. M., Alperin, M. J., Albert, D. B., and Martens, C. S.: Thermodynamic control on hydrogen concentrations in anoxic sediments, Geochim. Cosmochim. Ac., 62, 1745–1756, 1998. Iversen, N. and Jørgensen, B. B.: Anaerobic methane oxidation rates at the sulfate-methane transition in marine sediments from Kattegat and Skagerrak (Denmark), Limnol. Oceanogr., 30, 944–955, 1985. Jackson, B. E. and McInerney, M. J.: Anaerobic microbial metabolism can proceed close to thermodynamic limits, Nature, 415, 454–456, 2002. Jin, Q. and Bethke, C. M.: A new rate law describing microbial respiration, Appl. Environ. Microb., 69(4), 2340–2348, 2003. Jin, Q. and Bethke, C. M.: The thermodynamics and kinetics of microbial metabolism, Am. J. Sci., 307, 643–677, 2007. Knittel, K., Boetius, A., Lemke, A., Eilers, H., Lochte, K., Pfannkuche, O., and Linke, P.: Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia Margin, Oregon), Geomicrobiol. J., 20, 269–294, 2003. Knittel, K., Lösekann, T., Boetius, A., Kort, R., and Amann, R.: Diversity and Distribution of Methanotrophic Archaea at Cold Seeps, Appl. Environ. Microb., 71(1), 467–479, 2005. Krüger, M., Meyerdiecks, A., Glockner, F. O., Amann, R., Widdel, F., Kube, M., Reinhardt, R., Kahnt, R., Bocher, R., Thauer, R. K., and Shima, S.: A conspicuous nickel protein in microbial mats that oxidize methane anaerobically, Nature, 426, 878–881, 2003. Martin, I., Dozin, B., Quarto, R., Cancedda, R., and Beltrame, F.: Computer-based technique for cell aggregation analysis and cell aggregation in in vitro chondrogenesis, Cytometry, 28, 141–146, 1997. Nauhaus, K., Albrecht, M., Elvert, M., Boetius, A., and Widdel, F.: In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane, Environ. Microbiol., 9(1), 187–196, 2007. Nauhaus, K., Boetius, A., Krueger, M., and Widdel, F.: In vitro demonstration of anaerobic oxidation of methane coupled to sulfate reduction from a marine gas hydrate area, Environ. Microbiol., 4, 296–305, 2002. Neretin, L., Abed, R. M. M., Schippers, A., Schubert, C., Kohls, K., and Kuypers, M. M. M.: Inorganic carbon fixation by sulfate-reducing bacteria in the Black Sea water column, Environ. Microbiol., 9, 3019–3024, 2007. Orcutt, B. N., Joye, S. B., Boetius, A., Elvert, M., and Samarkin, V. A.: Molecular biogeochemistry of sulfate reduction, methanogenesis and the anaerobic oxidation of methane at Gulf of Mexico cold seeps, Geochim. Cosmochim. Ac., 69(17), 4267–4281, 2005. Orcutt, B. N., Samarkin, V., Boetius, A., and Joye, S. B.: On the relationship between methane production and oxidation by anaerobic methanotrophic communities from cold seeps of the Gulf of Mexico, Environ. Microbiol., 10(5), 1108–1117, doi:10.1111/j.1462-2920.2007.01526.x, 2008. Orphan, V. J., Hinrichs, K.-U., Ussler~III, W., Paull, C. K., Taylor, L. T., Sylva, S. P., Hayes, J. M., and DeLong, E. F.: Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments, Appl. Environ. Microb., 67(4), 1922–1934, 2001. Orphan, V. J., House, C. H., Hinrichs, K.-U., McKeegan, K. D., and DeLong, E. F.: Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments, P. Natl. Acad. Sci. USA, 99, 7663–7668, 2002. Reeburgh, W. S.: Methane consumption in Cariaco Trench waters and sediments, Earth Planet. Sc. Lett., 28, 337–344, 1976. Reguera, G., Nevin, K. P., Nicoll, J. S., Covalla, S. F., Woodard, T. L., and Lovley, D. R.: Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells, Appl. Environ. Microb., 72(11), 7345–7348, 2006. Schink, B.: Energetics of syntrophic cooperation in methanotrophic degradation, Microbial Molecular Biology Review, 61, 262–280, 1997. Schulz, H. D.: Quanitification of Early Diagenesis: Dissolved Constituents in Marine Pore Water, in: Marine Geochemistry, edited by: Schulz, H. D. and Zabel, M., Springer, 87–128, 2000. Sørensen, K. B., Finster, K., and Ramsing, N. B.: Thermodynamic and kinetic requirements in anaerobic methane oxidizing consortia exclude hydrogen, actetate, and methanol as possible electron shuttles, Microb. Ecol., 42, 1–10, 2001. Stewart, P. S.: Diffusion in biofilms, J. Bacteriol., 185(5), 1485–1491, 2003. Strous, M. and Jetten, M. S. M.: Anaerobic oxidation of methane and ammonium, Annu. Rev. Microbiol., 58, 99–117, 2004. Stumm, W. and Morgan, J. J.: Aquatic Chemistry: An Introduction Emphasizing Chemical Equilibria in Natural Waters, John Wiley and Sons, 1022~pp., 1981. Thauer, R. K., Jungermann, K., and Decker, K.: Energy conservation in chemotrophic anaerobic bacteria, Microbiol. Rev., 41, 100–180, 1977. Treude, T., Orphan, V. J., Knittel, K., Gieseke, A., House, C. H., and Boetius, A.: Consumption of methane and CO2 by methanotrophic microbial mats from gas seeps of the anoxic Black Sea, Appl. Environ. Microb., 73, 2271–2283, 2007. Valentine, D. L. and Reeburgh, W. S.: New perspectives on anaerobic methane oxidation, Environ. Microbiol., 2(5), 477–484, 2000. Valentine, D. L.: Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review, Anton. Leeuw. Int. J. G., 81, 271–281, 2002. Wieland, A., de~Beer, D., Damgaard, L. R., Kühl, M., and van~Dusschoten, D.: Fine-scale measurement of diffusivity in a microbial mat with nuclear magnetic resonance imaging, Limnol. Oceanogr., 46(2), 248–259, 2001.