Archaea catalyze iron dependent anaerobic oxidation of methane
Significance Carbon and nitrogen cycles have been altered dramatically by human activities. Methane producing (methanogenic) and methane consuming (methanotrophic) microorganisms control the emission of methane, one of the most potent greenhouse gases, to the atmosphere. Earlier studies identified methanotrophic microorganisms that use methane as an electron donor and oxygen, sulfate, nitrite, and nitrate as electron acceptors. Previous research showed that methanotrophy coupled to the reduction of oxidized metals could be important in the environment. In the current paper, we identified archaea of the order Methanosarcinales, related to "Candidatus Methanoperedens nitroreducens," which couple the reduction of environmentally relevant particulate forms of iron and manganese to methane oxidation, filling one of the remaining lacunas in anaerobic methane oxidation. Anaerobic oxidation of methane (AOM) is crucial for controlling the emission of this potent greenhouse gas to the atmosphere. Nitrite nitrate and sulfate dependent methane oxidation is well documented, but AOM coupled to the reduction of oxidized metals has so far been demonstrated only in environmental samples. Here, using a freshwater enrichment culture, we show that archaea of the order Methanosarcinales, related to "Candidatus Methanoperedens nitroreducens," couple the reduction of environmentally relevant forms of Fe3+ and Mn4+ to the oxidation of methane. We obtained an enrichment culture of these archaea under anaerobic, nitrate reducing conditions with a continuous supply of methane. Via batch incubations using [13C]methane, we demonstrated that soluble ferric iron (Fe3+ as Fe citrate) and nanoparticulate forms of Fe3+ and Mn4+ supported methane oxidizing activity. CO2 and ferrous iron (Fe2+ were produced in stoichiometric amounts. Our study connects the previous finding of iron dependent AOM to microorganisms detected in numerous habitats worldwide. Consequently, it enables a better understanding of the interaction between the biogeochemical cycles of iron and methane.
Proceedings of the National Academy of Sciences