The greenhouse gas methane is an important contributor to global warming, with freshwater sediments representing important potential methane sources. Anaerobic methane-oxidising 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’ co-occur with a specific sulphate-reducing bacterium, 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 harbouring 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’. This research deepens our understanding of the metabolic flexibility and potential interspecific interactions of ‘Ca. Methanoperedens’ in freshwater lakes.