Genome-centric metagenomics reveals electroactive syntrophs in a conductive particle-dependent consortium from coastal sediments.

Conductive particles are common in coastal sediments, yet their role in shaping methane-producing communities and pathways remains unclear. We applied genome-resolved metagenomics to a sediment-derived consortium serially transferred for a decade and obligately dependent on granular activated carbon (GAC). We discovered a particle-obligate food web composed of electrogenic syntrophic acetate oxidizers (SAO), an electrotrophic methanogen, and necromass recyclers. The primary SAO electrogen, Candidatus Geosyntrophus acetoxidans, represents a new genus and possesses a complete acetate oxidation pathway and extracellular electron-transfer (EET) machinery, including two porin-cytochrome conduits, 43 additional multiheme cytochromes and conductive pili. A secondary SAO, a Lentimicrobium sp. with a giant PCC-cluster, supplies an alternative EET-linked acetate-oxidation route. Electrons from electrogens transfer via GAC to a Methanosarcina equipped with the heptaheme cytochrome MmcA and flagellin for electron uptake. These results provide a genomic blueprint of this particle-obligate environmental consortium and suggest an overlooked acetate-to-methane electron-transfer route in geoconductor-rich anoxic sediments.