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 have acquired a unique metabolism, which induces long-distance electron transport along their centimeter-long multicellular filaments. At present, cable bacteria are thought to form a monophyletic clade with two described genera. However, their diversity has not been systematically investigated. To investigate the phylogenetic relationships within the cable bacteria clade, 16S rRNA gene sequences were compiled from literature and public databases (SILVA 138 SSU and NCBI GenBank). These were complemented with novel sequences obtained from natural sediment enrichments across a wide range of salinities (2–34). To enable taxonomic resolution at the species level, we designed a procedure to attain full-length 16S rRNA gene sequences from individual cable bacterium filaments using an optimized nested PCR protocol and Sanger sequencing. The final database contained 1,876 long 16S rRNA gene sequences (≥800 bp) originating from 92 aquatic locations, ranging from polar to tropical regions and from intertidal to deep sea sediments. The resulting phylogenetic tree reveals 90 potential species-level clades (based on a delineation value of 98.7% 16S rRNA gene sequence identity) that reside within six genus-level clusters. Hence, the diversity of cable bacteria appears to be substantially larger than the two genera and 13 species that have been officially named up to now. Particularly brackish environments with strong salinity fluctuations, as well as sediments with low free sulfide concentrations and deep sea sediments harbor a large pool of novel and undescribed cable bacteria taxa.

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.