A novel cable bacteria species with a distinct morphology and genomic potential

Cable bacteria form a group of multicellular prokaryotes that enable electron transfer over centimeter-scale distances within marine and freshwater sediments. To this end, the periplasm of these filamentous bacteria contains specialized conductive fibers, which extend along the full length of each filament and incorporate a novel Ni-containing NiBiD cofactor. Currently, the cable bacteria include two recognized genera, <i>Candidatus</i> Electrothrix and <i>Candidatus</i> Electronema, but the genetic and morphological diversity within the clade remains underexplored. Here, we report the isolation and characterization of a novel cable bacteria species from an intertidal estuarine mudflat within Yaquina Bay (Oregon, USA). A clonal enrichment culture of a single strain (designated YB6) was generated, and filaments were subjected to genomic, morphological, spectroscopic, and electrical characterization. Strain YB6 shares key physiological traits with other cable bacteria, such as long-distance electron conduction and the presence of the nickel bis(dithiolene) cofactor. At the same time, YB6 exhibits distinctive morphological features, including pronounced surface ridges that are up to three times wider than in other cable bacteria. Additionally, filaments are extensively enveloped by extracellular sheaths. Genomic analysis reveals that strain YB6 harbors metabolic pathways and genes found in both the <i>Ca</i>. Electrothrix and <i>Ca</i>. Electronema genera. Phylogenetic and phylogenomic analyses indicate that strain YB6 represents a novel species (average nucleotide identity <95%) that forms an early branch within the <i>Ca</i>. Electrothrix clade. The proposed name is <i>Ca</i>. Electrothrix yaqonensis sp. nov., honoring the Yako'n tribe of Native Americans whose ancestral lands encompassed Yaquina Bay.IMPORTANCEThis study expands our understanding of the genetic and morphological diversity of cable bacteria, a group of prokaryotes with a unique metabolism based on long-range conduction. We present the detailed morphological and genomic characterization of a novel species: <i>Ca</i>. Electrothrix yaqonensis, strain YB6, isolated from an intertidal estuarine mudflat. Importantly, the strain exhibits a distinctive ridge morphology (harboring the conductive fibers) and abundant formation of extracellular sheaths. Genomic analysis reveals that YB6 shares metabolic features with both <i>Ca</i>. Electrothrix and <i>Ca</i>. Electronema genera.