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

Ugo Marzocchi,Andreas Schramm,Rikke Louise Meyer,Daniela Trojan,Nils Risgaard-Petersen,Lars Peter Nielsen,Steffen Larsen,Niels Peter Revsbech

doi:10.1038/ismej.2014.19

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.

Highlights

Electric currents can couple cathodic O2 reduction (O2 þ 4H þ þ 4e À -2H2O) at the surface of marine sediment to anodic oxidation of sulfide (H2S þ 4 H2O-SO42 À þ 10H þ þ 8e À ) over distances of more than 1 cm (Nielsen et al, 2010; Risgaard-Petersen et al, 2012)
Electric coupling between NO3À reduction and SH2S oxidation The results of this study show that NO3À reduction can sustain the distant oxidation of SH2S in marine sediment as previously described for O2 (Nielsen et al, 2010)
Exposing the sediment to NO3À amended anoxic overlying water resulted in the development of geochemical traits typical of electric coupling between distant half-cell reactions such as: (1) development of a 4–7-mm-wide zone devoid of both NO3À and SH2S, consistent with the separation of SH2S oxidation from the associated NO3À reduction; (2) consumption of protons in the NO3À reduction zone and proton production at the SH2S oxidation depth consistent with the presence of cathodic NO3À reduction and anodic SH2S oxidation, respectively

Summary

Introduction

Electric currents can couple cathodic O2 reduction (O2 þ 4H þ þ 4e À -2H2O) at the surface of marine sediment to anodic oxidation of sulfide (H2S þ 4 H2O-SO42 À þ 10H þ þ 8e À ) over distances of more than 1 cm (Nielsen et al, 2010; Risgaard-Petersen et al, 2012). Comparison of NO3À and O2 effectiveness in sustaining distant sulfide oxidation In March 2012, freshly collected sediment was pre-treated as described above and incubated in three treatments where the overlying artificial seawater was maintained aerated, anoxic (NO3À -free) or anoxic in the presence of 200 mM NO3À .

Results

Conclusion