Electrogenic CH4 oxidation on a bioanode: putative extracellular electron transport system in Methylobacter sp.

Abstract

Aerobic methanotrophs are frequently detected in oxygen-limited, stratified coastal environments. Known adaptations, including high-affinity terminal oxidases and oxygen-binding bacteriohemerythrins, help explain methane oxidation at extremely low oxygen concentrations, yet their activity and ecological role under fully anoxic conditions remain uncertain. Here, we show that an anoxic, poised-anode bioelectrochemical system inoculated with a methane-oxidizing sediment enrichment produced methane-dependent current, with rapid current loss upon methane removal and recovery after re-addition. Metagenomic analysis revealed the selective enrichment of a Methylobacter population encoding a porin-cytochrome complex and numerous multiheme c-type cytochromes, suggesting extracellular electron transfer potential. A complementary phylogenomic survey across Methylococcales identified homologs of this gene cluster in multiple lineages, but with a scattered phylogenetic distribution indicative of modular acquisition. Comparative synteny further revealed conserved gene order across genomes, supporting horizontal transfer of the locus as a functional unit. Together, these results demonstrate that aerobic methanotrophs may employ extracellular electron transfer strategies to dissipate methane-derived electrons when oxygen-dependent respiration is constrained.