Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor

Abstract

Recently, a novel mode of sulphur oxidation was described in marine sediments, in which sulphide oxidation in deeper anoxic layers was electrically coupled to oxygen reduction at the sediment surface. Subsequent experimental evidence identified that long filamentous bacteria belonging to the family Desulfobulbaceae likely mediated the electron transport across the centimetre-scale distances. Such long-range electron transfer challenges some long-held views in microbial ecology and could have profound implications for sulphur cycling in marine sediments. But, so far, this process of electrogenic sulphur oxidation has been documented only in laboratory experiments and so its imprint on the seafloor remains unknown. Here we show that the geochemical signature of electrogenic sulphur oxidation occurs in a variety of coastal sediment environments, including a salt marsh, a seasonally hypoxic basin, and a subtidal coastal mud plain. In all cases, electrogenic sulphur oxidation was detected together with an abundance of Desulfobulbaceae filaments. Complementary laboratory experiments in intertidal sands demonstrated that mechanical disturbance by bioturbating fauna destroys the electrogenic sulphur oxidation signal. A survey of published geochemical data and 16S rRNA gene sequences identified that electrogenic sulphide oxidation is likely present in a variety of marine sediments with high sulphide generation and restricted bioturbation, such as mangrove swamps, aquaculture areas, seasonally hypoxic basins, cold sulphide seeps and possibly hydrothermal vent environments. This study shows for the first time that electrogenic sulphur oxidation occurs in a wide range of marine sediments and that bioturbation may exert a dominant control on its natural distribution.

Figure 1

Microsensor depth profiles of O₂ (red), ΣH₂S (blue) and pH (black) show the characteristic biogeochemical fingerprint of electrogenic sulphur oxidation in surface sediments from three coastal sites in the North Sea: (a) RSM, (b) BCZ and (c) MLG. In contrast, microsensor depth profiles from (d) OSF do not show the characteristic fingerprint. Representative microprofile curves are illustrated. (e) World map indicating Aarhus Harbour, the location where the electrogenic signature and Desulfobulbaceae filaments were first found in laboratory incubations (yellow cross), and the present study region (Dutch Delta area; red triangle). (f) Detailed map of individual study site locations (red triangles); full site details are given in Table 1. The world map also indicates locations where the geochemical signature of long distance electron transport have been found in literature reports (black circles) and locations where highly similar (⩾97%) 16S rRNA gene sequences to the Desulfobulbaceae filaments were retrieved from GenBank (blue squares); see Discussion for details.

Figure 2

Identification of filamentous Desulfobulbaceae bacteria present in intact sediment from sites described in Figure 1 and Table 1. (a) Abundant long filamentous bacteria taken from near the surface of sediment and gently teased apart with forceps. (b) Identification of the filaments belonging to Desulfobulbaceae using CARD–FISH (DSB 706 probe). (c) SEM image of a bacterial filament isolated from the sediment. All images shown here are from MLG. See Supplementary material for images from RSM and BCZ. (d) Phylogenetic tree of Desulfobulbaceae 16S rRNA sequences recovered from intact sediment described in Figure 1. Closely related sequences of filamentous Desulfobulbaceae from Aarhus Bay and other isolated bacteria are also included. Scale bar shows 5% sequence divergence and bootstrap support is indicated on tree branches.

Figure 3

(a) A subset of microsensor profiles from sediment collected from a heavily bioturbated sediment from an OSF that has been artificially defaunated and incubated with well-oxygenated overlying water. Despite a low concentration of free sulphide, development of a geochemical signature of long-range electron transport is evident from Day 5 onwards. (b) DOU during the incubations, average of n=3, plotted with standard error about the mean. (c) Current density calculated from these sediments and (d) percentage, p, of oxygen flux that is attributable to cathodic oxygen uptake.

Figure 4

Effect of sediment disturbance by fauna on electrogenic sulphur oxidation. Microprofiles of O₂ (red), ΣH₂S (blue) and pH (black and grey) are shown from sediment cores collected from the intertidal OSF. Different shades are used for replicate profiles for pH and ΣH₂S for image clarity, whereas a single median profile is shown for O₂. (a) Profiles from intact sediment cores. (b) Profiles from defaunated sediment cores. (c) Profiles from re-faunated sediment cores, in areas that were not visibly disrupted by mechanical disturbance caused by the re-introduced lugworms. (d) Profiles from re-faunated sediment cores, in areas that were not visibly disrupted by mechanical disturbance caused by the re-introduced lugworms.