Archaea catalyze iron-dependent anaerobic oxidation of methane

Abstract

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 <i>Methanosarcinales</i>, related to "<i>Candidatus</i> 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.