Anaerobic consortia mediate Mn(IV)-dependent anaerobic oxidation of methane

Manganese-dependent anaerobic oxidation of methane (Mn-AOM) is a major methane sink and vital to mitigating global warming. However, it is difficult for microorganisms to mediate electron transfer between the hardly dissolved CH4 and insoluble Mn(IV) minerals, leading to poor understanding of species mediating MnAOM. This study successfully enriched an anaerobic consortium mediating AOM driven by Mn-dependent respiratory growth, and for the first time, revealing a syntrophic pathway for Mn-AOM. The Mn-AOM occurrence was confirmed by long-term bioreactor performance and 13C-labelling batch experiment. Metagenomic and metatranscriptomic analyses demonstrated that the Candidatus Methanoperedens sp. BLZ1 was responsible for CH4 oxidation. The Luteitalea pratensis mediated extracellular electron transfer crossing S-layer of Ca. M. BLZ1 by conductive pili, and mediated microbial Mn(IV) reduction via multi-heme c-type cytochromes. This study offers an alternative syntrophic pathway for Mn-AOM by a microbial consortium instead of previously reported pathway by ANME alone. These outcomes provided new insight into migrating global climate change and manganese cycles.

Automated summary

Manganese-dependent anaerobic oxidation of methane (Mn-AOM) is a crucial process for methane consumption and mitigating global warming. However, the electron transfer between CH4 and insoluble Mn(IV) minerals is challenging, leading to a lack of understanding of the microorganisms involved in MnAOM. This study successfully enriched an anaerobic consortium that mediated Mn-AOM and revealed a novel pathway for this process. Through bioreactor experiments and 13C-labelling batch experiments, the occurrence of Mn-AOM was confirmed. Metagenomic and metatranscriptomic analyses identified Candidatus Methanoperedens sp. BLZ1 as responsible for CH4 oxidation. Luteitalea pratensis mediated extracellular electron transfer and microbial Mn(IV) reduction in the consortium. This study provides new insights into global climate change and manganese cycles.