Electrogenic sulfide oxidation mediated by cable bacteria stimulates sulfate reduction in freshwater sediments

Abstract

Cable bacteria are filamentous members of the Desulfobulbaceae family that oxidize sulfide with oxygen or nitrate by transferring electrons over centimeter distances in sediments. Recent studies show that freshwater sediments can support populations of cable bacteria at densities comparable to those found in marine environments. This is surprising since sulfide availability is presumably low in freshwater sediments due to sulfate limitation of sulfate reduction. Here we show that cable bacteria stimulate sulfate reduction in freshwater sediment through promotion of sulfate availability. Comparing experimental freshwater sediments with and without active cable bacteria, we observed a three-to tenfold increase in sulfate concentrations and a 4.5-fold increase in sulfate reduction rates when cable bacteria were present, while abundance and community composition of sulfate-reducing microorganisms (SRM) were unaffected. Correlation and ANCOVA analysis supported the hypothesis that the stimulation of sulfate reduction activity was due to relieve of the kinetic limitations of the SRM community through the elevated sulfate concentrations in sediments with cable bacteria activity. The elevated sulfate concentration was caused by cable bacteria-driven sulfide oxidation, by sulfate production from an indigenous sulfide pool, likely through cable bacteria-mediated dissolution and oxidation of iron sulfides, and by enhanced retention of sulfate, triggered by an electric field generated by the cable bacteria. Cable bacteria in freshwater sediments may thus be an integral component of a cryptic sulfur cycle and provide a mechanism for recycling of the scarce resource sulfate, stimulating sulfate reduction. It is possible that this stimulation has implication for methanogenesis and greenhouse gas emissions.

Quantification of Cable Bacteria in Marine Sediments via qPCR

“…This long-distance electron transport enables an electrical coupling of sulfide oxidation in deeper anoxic sediment layers to oxygen reduction near the sediment surface ( Nielsen et al, 2010 ). Electrogenic sulfur oxidation (e-SOx) by cable bacteria makes an important contribution to sulfur cycling in aquatic sediments ( Risgaard-Petersen et al, 2012 ; Malkin et al, 2014 ; Burdorf et al, 2017 ; Sandfeld et al, 2020 ), and has a strong imprint on the local geochemistry of the seafloor ( Risgaard-Petersen et al, 2012 ; Meysman et al, 2015 ). The sulfide oxidizing half-reaction results in an acidification of the pore water, leading to the dissolution of minerals, such as carbonates and sulfides, thereby greatly affecting the cycling of elements like Ca, Fe, Mn, P and trace elements ( Risgaard-Petersen et al, 2012 ; Rao et al, 2016 ; Sulu-Gambari et al, 2016 ; van de Velde et al, 2016 , 2017 ).…”

Cable bacteria reduce methane emissions from rice-vegetated soils

“…The cable bacteria-mediated 93% reduction of CH 4 emission is one of the highest reported reduction efficiencies compared to studies where sulfate was added 13,16,17 . The main controlling factor in our experiments was likely the sulfate accumulation which was uniformly distributed in the upper 4 cm in pots with cable bacteria, suggesting that sulfate reduction was balanced by sulfur re-oxidation via e-SOX and eventually that ionic migration adds to the transport of sulfate 12 . The sulfate accumulation stimulated the activity of sulfate-reducing bacteria and therefore outcompeted methanogens for common substrates such as hydrogen or acetate.…”

“…Moreover, the establishment of an electric field through e-SOX causes downward migration of sulfate and minimizes its loss to the water column 6 . Hence, the electric field contributes to the e-SOX-driven accumulation of sulfate, which has recently been shown to stimulate sulfate reduction 12 .…”

Biogeochemical impact of cable bacteria on coastal Black Sea sediment

“…Rates of SO 2− 4 reduction estimated from the linear gradient of the decrease in pore water SO 2− 4 in the surface sediment with depth indeed also showed a decline during the experiment. We note, however, that a direct measurement of SO 2− 4 reduction rates (Fossing and Jørgensen, 1989;Kallmeyer et al, 2004) would provide a better indicator because SO 2− 4 estimated from pore water profiles is, in general, lower than rates estimated from tracer experiments (Sandfeld et al, 2020;Hermans et al, 2019a). Another cause for a slight underestimation of our SO 2− 4 reduction rates is due to the effect of the electric field imposed by cable bacteria, which is not taken into account in Fick's law.…”