The Role of Crystalline Iron Oxides in Methane Mitigation through Anaerobic Oxidation of Methane

Biological Fe(III)-dependent anaerobic oxidation of methane (AOM) is predicted to be a key methane sink in natural and anthropogenic environments. Crystalline Fe(III) is an important environmentally relevant form of Fe(III) in those environments, including aquifers, estuaries, marine sediments, and soils. However, its role in methane mitigation remains unknown. This study investigated the feasibility of crystalline Fe(III) as an electron acceptor for AOM. A culture dominated by an anaerobic methanotrophic (ANME) archaeon, Candidatus "Methanoperedens ferrireducens", was amended with magnetite and goethite. Long-term performance data indicated that both magnetite and goethite can be used as electron acceptors for AOM. The AOM rate was comparable to a control bioreactor fed with amorphous ferrihydrite. Microbial analyses suggested that Ca. "M. ferrireducens" and/or methanogens undertook Fe(III)-dependent AOM. Biotic iron reduction resulted in the formation of siderite and accumulation of dissolved Fe(II). Dissolved Fe(II) was likely toxic to Ca. "M. ferrireducens", while stimulated the growth of a potential Fe(II) oxidizer belonging to genus Chlorobium. Coexistence of Ca. "M. ferrireducens"/methanogens and Chlorobium bacteria revealed a methane-driven iron cycle. These findings suggest that crystalline Fe(III)-dependent AOM may play an important role in regulating methane flux and iron cycle in environments rich in methane and iron oxides.