Methanotrophic flexibility of Ca. Methanoperedens and its interactions with sulfate-1 reducing bacteria in the sediment of meromictic Lake Cadagno

The greenhouse gas methane is an important contributor to global warming, with freshwater sediments representing important potential methane sources. Anaerobic methane-oxidizing archaea mitigate methane release into the atmosphere by coupling the oxidation of methane to the reduction of extracellular electron acceptors or through interspecies electron transfer with microbial partners. Understanding their metabolic flexibility and microbial interactions is crucial to assess their role in global methane cycling. Here, we investigated anoxic sediments of the meromictic freshwater Lake Cadagno (Switzerland), where Ca. Methanoperedens and sulfate-reducing bacteria co-occur, with metagenomics and long-term incubations. Incubations were performed with different electron acceptors, revealing that manganese oxides supported highest CH4 oxidation potential but enriched for Ca. Methanoperedens phylotypes that were hardly present in the inoculum. Combining data from the inoculum and incubations, we obtained five Ca. Methanoperedens genomes, each harboring different extracellular electron transfer pathways. In a reconstructed Desulfobacterota QYQD01 genome we observed large multi-heme cytochromes, type IV pili, and a putative loss of hydrogenases, suggesting facultative syntrophic interactions with Ca. Methanoperedens. We also screened for putative extrachromosomal elements in the Ca. Methanoperedens genomes, including BORGs. This research deepens our understanding of the metabolic flexibility and potential interspecific interactions of Ca. Methanoperedens in freshwater lakes.