2007Environmental MicrobiologyRequires access

Methyl sulfides as intermediates in the anaerobic oxidation of methane

James Moran, Emily J. Beal, Jennifer M. Vrentas, Victoria J. Orphan, Katherine H. Freeman, Christopher H. House

Open publisher page 156 citations

Abstract

While it is clear that microbial consortia containing Archaea and sulfate-reducing bacteria (SRB) can mediate the anaerobic oxidation of methane (AOM), the interplay between these microorganisms remains unknown. The leading explanation of the AOM metabolism is 'reverse methanogenesis' by which a methanogenesis substrate is produced and transferred between species. Conceptually, the reversal of methanogenesis requires low H(2) concentrations for energetic favourability. We used (13)C-labelled CH(4) as a tracer to test the effects of elevated H(2) pressures on incubations of active AOM sediments from both the Eel River basin and Hydrate Ridge. In the presence of H(2), we observed a minimal reduction in the rate of CH(4) oxidation, and conclude H(2) does not play an interspecies role in AOM. Based on these results, as well as previous work, we propose a new model for substrate transfer in AOM. In this model, methyl sulfides produced by the Archaea from both CH(4) oxidation and CO(2) reduction are transferred to the SRB. Metabolically, CH(4) oxidation provides electrons for the energy-yielding reduction of CO(2) to a methyl group ('methylogenesis'). Methylogenesis is a dominantly reductive pathway utilizing most methanogenesis enzymes in their forward direction. Incubations of seep sediments demonstrate, as would be expected from this model, that methanethiol inhibits AOM and that CO can be substituted for CH(4) as the electron donor for methylogenesis.

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What this paper is about

While it is clear that microbial consortia containing Archaea and sulfate-reducing bacteria (SRB) can mediate the anaerobic oxidation of methane (AOM), the interplay between these microorganisms remains unknown. The leading explanation of the AOM metabolism is 'reverse methanogenesis' by which a methanogenesis substrate is produced and transferred between species. Conceptually, the reversal of methanogenesis requires low H(2) concentrations for energetic favourability. We used (13)C-labelled CH(4) as a tracer to test the effects of elevated H(2) pressures on incubations of active AOM sediments from both the Eel River basin and Hydrate Ridge. In the presence of H(2), we observed a minimal reduction in the rate of CH(4) oxidation, and conclude H(2) does not play an interspecies role in AOM. Based on these results, as well as previous work, we propose a new model for substrate transfer in AOM. In this model, methyl sulfides produced by the Archaea from both CH(4) oxidation and CO(2) reduction are transferred to the SRB. Metabolically, CH(4) oxidation provides electrons for the energy-yielding reduction of CO(2) to a methyl group ('methylogenesis'). Methylogenesis is a dominantly reductive pathway utilizing most methanogenesis enzymes in their forward direction. Incubations of seep sediments demonstrate, as would be expected from this model, that methanethiol inhibits AOM and that CO can be substituted for CH(4) as the electron donor for methylogenesis.

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Available abstract

While it is clear that microbial consortia containing Archaea and sulfate-reducing bacteria (SRB) can mediate the anaerobic oxidation of methane (AOM), the interplay between these microorganisms remains unknown. The leading explanation of the AOM metabolism is 'reverse methanogenesis' by which a methanogenesis substrate is produced and transferred between species. Conceptually, the reversal of methanogenesis requires low H(2) concentrations for energetic favourability. We used (13)C-labelled CH(4) as a tracer to test the effects of elevated H(2) pressures on incubations of active AOM sediments from both the Eel River basin and Hydrate Ridge. In the presence of H(2), we observed a minimal reduction in the rate of CH(4) oxidation, and conclude H(2) does not play an interspecies role in AOM. Based on these results, as well as previous work, we propose a new model for substrate transfer in AOM. In this model, methyl sulfides produced by the Archaea from both CH(4) oxidation and CO(2) reduction are transferred to the SRB. Metabolically, CH(4) oxidation provides electrons for the energy-yielding reduction of CO(2) to a methyl group ('methylogenesis'). Methylogenesis is a dominantly reductive pathway utilizing most methanogenesis enzymes in their forward direction. Incubations of seep sediments demonstrate, as would be expected from this model, that methanethiol inhibits AOM and that CO can be substituted for CH(4) as the electron donor for methylogenesis.

Key concepts: Methanogenesis, Anaerobic oxidation of methane, Archaea, Sulfate-reducing bacteria, Methane, Methanethiol, Substrate (aquarium), Biology

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