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

Conductive particles are abundant in coastal sediments, yet the organisms and pathways that use them for methane production remain unclear. We applied long-read, genome-resolved metagenomics to a sediment-derived consortium that remained dependent on granular activated carbon (GAC) for a decade. We identified a particle-obligate food web of electrogenic syntrophic acetate oxidizers (SAO), an electrotrophic methanogen, and necromass recyclers. The dominant SAO electrogen was a new genus, Candidatus Geosyntrophus acetoxidans (<70% ANI/AAI to described taxa), encoding a streamlined extracellular electron-transfer system: one porin-cytochrome conduit (PCC), 47 multiheme cytochromes, conductive pili, and acetate uptake/utilization genes. A second SAO electrogen, Lentimicrobium sp., carried two giant PCC-like clusters, suggesting an alternative acetate-oxidation route. Electrons flowed via GAC to a Methanosarcina (<89% ANI/AAI to described taxa) equipped with the multiheme cytochrome MmcA and a Rnf/Fpo/HdrDE circuit for EET-driven CO2-reducing methanogenesis. Particle-free lines lost both partners and methanogenic activity, establishing particles as the determinant of persistence. This first genomic blueprint of a natural CIET-SAO consortium identifies potential genomic markers (distinct PCCs, MmcA) for in-situ detection and reveals a particle-bound route from acetate to methane likely operating as a fundamental electron-transfer unit in geoconductor-rich anoxic sediments.