On the Evolution and Physiology of Cable Bacteria

Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur worldwide in the surface of aquatic sediments, where they connect sulfide oxidation with oxygen or nitrate reduction via long-distance electron transport. In the absence of pure cultures, we used single-filament genome amplification and metagenomics to retrieve draft genomes of three marine Candidatus Electrothrix and one freshwater Ca. Electronema species. These genomes contain >50% of unknown genes but still largely share their core genomic makeup with sulfate-reducing and sulfur-disproportionating Desulfobulbaceae, with few genes lost and 212 unique genes conserved among cable bacteria. Last common ancestor analysis indicated gene divergence and lateral gene transfer as equally important origins of these unique genes. With support from metaproteomic data of Ca. Electronema, the genomes suggest that cable bacteria oxidize sulfide by inversing the canonical sulfate reduction pathway and fix CO2 using the Wood-Ljungdahl pathway. Cable bacteria show limited organotrophic potential, may assimilate smaller organic acids and alcohols, fix N2, and synthesize polyphosphates and polyglucose as storage compounds; several of these traits were confirmed by cell-level experimental analyses. We propose a model for electron flow from sulfide to oxygen that involves periplasmic cytochromes, type IV pili as integral components of conductive periplasmic fibers, and periplasmic oxygen reduction. This model proposes that an active cable bacterium gains energy in the anodic, sulfide-oxidizing cells, while cells in the oxic zone flare off electrons through intense cathodic oxygen respiration without energy conservation; this peculiar form of multicellularity seems unparalleled in the microbial world.