Arsenate reduction coupled to anaerobic oxidation of methane by members of the Methanoperedenaceae

Abstract

Abstract Anaerobic methanotrophic ‘Candidatus Methanoperedenaceae’ play a key role in mitigating methane emissions from freshwater sediments. Members of the family are metabolically versatile, with species coupling anaerobic oxidation of methane (AOM) to the reduction of nitrate and metal oxides. Metagenomic analyses have indicated further uncharacterized metabolic diversity, including the potential for AOM coupled to arsenate reduction (As-AOM). While As-AOM has been confirmed as an important methane sink and contributor to arsenic mobilization in freshwater environments, the underlying microbiological mechanisms remain to be empirically demonstrated. In this study stoichiometric coupling of dissimilatory arsenate reduction to methane oxidation was demonstrated using enrichment cultures of the uncultured type species ‘Ca. Methanoperedens nitroreducens’. Meta-omics revealed that arsenate oxidoreductases were exclusively encoded by ‘Ca. M. nitroreducens’ and upregulated under As-AOM conditions, confirming this species was directly responsible. These findings expand our understanding of ‘Ca. Methanoperedenaceae’ physiology and demonstrate microbial mechanisms underpinning arsenic mobilization in freshwater systems, with important implications for climate and public health.