Electric coupling between distant nitrate reduction and sulfide oxidation in marine sediment

Abstract

Filamentous bacteria of the Desulfobulbaceae family can conduct electrons over centimeter-long distances thereby coupling oxygen reduction at the surface of marine sediment to sulfide oxidation in deeper anoxic layers. The ability of these cable bacteria to use alternative electron acceptors is currently unknown. Here we show that these organisms can use also nitrate or nitrite as an electron acceptor thereby coupling the reduction of nitrate to distant oxidation of sulfide. Sulfidic marine sediment was incubated with overlying nitrate-amended anoxic seawater. Within 2 months, electric coupling of spatially segregated nitrate reduction and sulfide oxidation was evident from: (1) the formation of a 4–6-mm-deep zone separating sulfide oxidation from the associated nitrate reduction, and (2) the presence of pH signatures consistent with proton consumption by cathodic nitrate reduction, and proton production by anodic sulfide oxidation. Filamentous Desulfobulbaceae with the longitudinal structures characteristic of cable bacteria were detected in anoxic, nitrate-amended incubations but not in anoxic, nitrate-free controls. Nitrate reduction by cable bacteria using long-distance electron transport to get privileged access to distant electron donors is a hitherto unknown mechanism in nitrogen and sulfur transformations, and the quantitative importance for elements cycling remains to be addressed.

Cable bacteria generate a firewall against euxinia in seasonally hypoxic basins

“…Although both cable bacteria (26) and Beggiatoaceae (19)(20)(21)(22) can use nitrate for respiration, cable bacteria reach lower population densities when nitrate is the sole electron acceptor (26). Moreover, the nitrate concentration in the bottom water was low (< 1.7 μM) during summer (Fig.…”

A Post-Genomic View of the Ecophysiology, Catabolism and Biotechnological Relevance of Sulphate-Reducing Prokaryotes

“…LDET-mediating cable bacteria affiliated with the Desulfobulbaceae have been observed in various different marine sediments (Malkin et al, 2014) and appear to be rather persistent under conditions of continuous sulphidogenesis (Larsen, Nielsen, & Schramm, 2014). Notably, Desulfobulbaceae filaments can couple sulphide oxidation via electric conduction not only to spatially distant oxygen reduction but also to nitrate reduction (Marzocchi et al, 2014). The process of LDET likely refines biogeochemical balances in various redox gradient systems and requires more research into the composition and architecture of the conductive structures, which will further define the field of electromicrobiology (Boesen & Nielsen, 2013;).…”

Rethinking Sediment Biogeochemistry After the Discovery of Electric Currents

“…As discussed below, the pool of calcite buffering the anode process may eventually determine the temporal limits when cable bacteria may operate. 14:18 Marzocchi et al (2014) recently established that electric currents and cable bacteria may develop in sediments where oxygen in the overlying water has been replaced with nitrate. Several pathways of dissimilative nitrate reduction are known, with nitrite as a universal first product and subsequent reduction to ammonium and dinitrogen as separate routes, with nitric oxide and nitrous oxide as free intermediates in the latter.…”