Rapid Redox Signal Transmission by “Cable Bacteria” beneath a Photosynthetic Biofilm

Abstract

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-...

The effect of oxygen availability on long‐distance electron transport in marine sediments

“…Lower oxygen availability thus seems to decrease the activity of the cable bacteria and delay the effect of e‐SOx on the sediment geochemistry. The growth of cable bacteria in a sediment covered with a photosynthetic biofilm (Malkin and Meysman ), raises the question whether the opposite also holds true (faster growth, faster acidification with more O 2 ). In such environments, O 2 saturation surpasses 100% and could induce an even faster acidification of the suboxic zone through e‐SOx.…”

Phototrophic marine benthic microbiomes: the ecophysiology of these biological entities

“…They form chains of thousands of cells that stick with one end in the anoxic layer of the sediment rich in reduced sulfur and with the other end in the oxic zone. The positioning of the cells along the vertical gradient is aided by the motility of cable bacteria (Malkin and Meysman, ; Bjerg et al ., ). Electrons obtained from the anaerobic oxidation of the reduced sulfur are transported through the chain of cells to the oxygenated top layer of the sediment where they are used to reduce oxygen to water, which has been demonstrated in isolated living cable bacteria in the laboratory (Bjerg et al ., ).…”

Motility of Electric Cable Bacteria

“…The depth distribution of cable bacteria matches the increasing separation between oxygen and pore water sulfide, and FISH and DAPI (4=,6-diamidino-2-phenylindole) staining show chromosomes in division or separation stages throughout the cable bacteria, suggesting that cells other than just apical cells are actively dividing and have to be moved actively to extend the filaments downwards (9). Additional indication of motility comes from a study of cable bacterium activity underneath a photosynthetic algal mat in an intertidal salt marsh (6). When incubated in an alternating light-dark regime, the sulfide concentration at depth increases rapidly with the transition from light to dark, as oxygen penetration declines when photosynthesis ceases (6).…”

“…All cable bacteria found so far have been shown, by single-filament sequencing of 16S rRNA or fluorescence in situ hybridization (FISH), to belong to the Desulfobulbaceae family, where no other filamentous form is known. Cable bacteria or pore water profiles indicating their presence have been reported from many different places in the world, including a salt marsh (5,6), a seasonally hypoxic basin (7), a freshwater stream (8), and a subtidal coastal mud plain (7), generally characterized by moderate to high sulfide generation and restricted bioturbation.…”

“…Additional indication of motility comes from a study of cable bacterium activity underneath a photosynthetic algal mat in an intertidal salt marsh (6). When incubated in an alternating light-dark regime, the sulfide concentration at depth increases rapidly with the transition from light to dark, as oxygen penetration declines when photosynthesis ceases (6). In the hours after darkening, sulfide concentrations at depth decrease again, suggesting that the cable bacteria recovered the lost cathodic activity, likely by moving more cells up into the oxic zone.…”