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, Candidatus Electrothrix and Candidatus 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 Ca. Electrothrix and Ca. 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 Ca. Electrothrix clade. The proposed name is Ca. Electrothrix yaqonensis sp. nov., honoring the Yako’n tribe of Native Americans whose ancestral lands encompassed Yaquina Bay.

Cable bacteria exhibit a unique metabolism involving long-distance electron transport, significantly impacting elemental cycling in various sediments. These long filamentous bacteria are distributed circumglobally, suggesting an effective mode of dispersal. However, oxygen strongly inhibits their activity, posing a challenge to their dispersal through the water column. We investigated the effective dispersal of marine cable bacteria in a compartmentalised microcosm experiment. Cable bacteria were grown in natural ‘source’ sediment, and their metabolic activity was recorded in autoclaved ‘destination’ cores, which were only accessible through oxygenated seawater. Colonisation occurred over weeks, and destination cores contained only one cable bacterium strain. Filament ‘snippets’ (fragments with a median size of ~15 cells) accumulated in the microcosm water, with about 30% of snippets attached to sediment particles. Snippet release was also observed in situ in a salt marsh creek. This provides a model for the dispersal of cable bacteria through oxygenated water: snippets are formed by filament breakage in the sediment, released into the overlying water and transported with sediment particles that likely offer protection. These insights are informative for broader theories on microbial community assembly and prokaryotic biogeography in marine sediments.