Recently, long filamentous bacteria, belonging to the family Desulfobulbaceae, were shown to induce electrical currents over long distances in the surface layer of marine sediments. These "cable bacteria" are capable of harvesting electrons from free sulfide in deeper sediment horizons and transferring these electrons along their longitudinal axes to oxygen present near the sediment-water interface. In the present work, we investigated the relationship between cable bacteria and a photosynthetic algal biofilm. In a first experiment, we investigated sediment that hosted both cable bacteria and a photosynthetic biofilm and tested the effect of an imposed diel light-dark cycle by continuously monitoring sulfide at depth. Changes in photosynthesis at the sediment surface had an immediate and repeatable effect on sulfide concentrations at depth, indicating that cable bacteria can rapidly transmit a geochemical effect to centimeters of depth in response to changing conditions at the sediment surface. We also observed a secondary response of the free sulfide at depth manifest on the time scale of hours, suggesting that cable bacteria adjust to a moving oxygen front with a regulatory or a behavioral response, such as motility. Finally, we show that on the time scale of days, the presence of an oxygenic biofilm results in a deeper and more acidic suboxic zone, indicating that a greater oxygen supply can enable cable bacteria to harvest a greater quantity of electrons from marine sediments. Rapid acclimation strategies and highly efficient electron harvesting are likely key advantages of cable bacteria, enabling their success in high sulfide generating coastal sediments.
During the degradation of organic matter, the microbial competition for terminal electron acceptors results in a characteristic vertical redox zonation in marine sediments (1, 2). Typically, oxygen and nitrate are consumed near the sediment surface, whereas sulfate, being a less energetically favorable electron acceptor, becomes utilized only in deeper sediment horizons. In the absence of porewater flushing by waves, currents, and fauna (3) or the downmixing of metal oxy/hydroxides by bioturbation (4), sulfide produced in deeper sediment layers is transported by molecular diffusion toward the sediment surface where it can be reoxidized. Molecular diffusion is a slow transport process that links centimeter-scale distances over time scales of days.Recently, however, a direct electrical connection between sulfidic and oxic sediment horizons was observed in a marine sediment, whereby electrons harvested from sulfide at depth were shunted directly to oxygen over centimeter distances (5). This novel microbial lifestyle enabling sulfur oxidation by long-distance electron transport can be distinguished by a distinct geochemical fingerprint of microsensor depth profiles (5). Close microscopic examination of sediments exhibiting this geochemical signature revealed that long filamentous bacteria belonging to the family Desulfobulbaceae were associated with the long-...