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.

Centimeter-long electron transport in marine sediments via conductive minerals

“…Although it has been suggested that filaments of cells closely related to Desulfobulbus species accounted for conductivity to reduced marine sediments from Aarhus Bay, it is, in fact, unknown whether this is possible because the conductivity of the filaments was not demonstrated (Pfeffer et al, 2012;Reguera, 2012;Malkin et al, 2014). No long bacterial filaments were observed in the Nantucket sediments used in these studies.…”

“…The suppression of sediment conductivity with oxidation indicated that long-range electron transport through the sediments is significantly different than that through G. sulfurreducens biofilms. It is unknown how oxidizing conditions might have an impact on the previously proposed conductivity through filamentous bacteria (Pfeffer et al, 2012;Malkin et al, 2014) because the hypothesized conductivity and the mechanisms for conduction have not been documented (Reguera, 2012). …”

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

“…Moreover, electrogenic sulfur oxidation appears to be competitively successful over other microbial sulfur oxidation strategies in laboratory experiments when organic-rich coastal sediments are incubated with oxygenated overlying water (5,9). The geochemical signature of long-distance electron transport and the associated cable bacteria has also been found under natural conditions in a range of coastal habitats with organic-rich sediments (8). A literature survey combined with data mining from 16S rRNA gene sequence archives suggested that electrogenic sulfur oxidation has a cosmopolitan distribution, occurring in a range of organic rich areas, including aquaculture-impacted areas, coastal mud plains, salt marshes, seasonally hypoxic basins, mangrove swamps, and cold seeps.…”

“…In sediments with high rates of sulfate reduction, all detectable free sulfide can be removed by this process from a suboxic zone up to about 30 mm (5,7,8). Moreover, electrogenic sulfur oxidation appears to be competitively successful over other microbial sulfur oxidation strategies in laboratory experiments when organic-rich coastal sediments are incubated with oxygenated overlying water (5, 9).…”

New method for characterizing electron mediators in microbial systems using a thin-layer twin-working electrode cell

“…It also does not enable the evaluation of the electrochemical behavior of those compounds present beyond the WE's boundary layer (Bard and Faulkner, 2001). Since both electron accepting (anodic) and electron donating (cathodic) reactions may concurrently occur within close proximities where EET prevails (Malkin et al, 2014), using a single WE for the evaluation of electron mediators in microbial systems may not be ideal.…”