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.
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Acknowledgements
The authors thank Lars Borregaard Pedersen, Karina Bomholt, Britta Poulsen, Susanne Nielsen, Jeanette Johansen, and Lykke Beinta Bjærge Bamdali for their skillful assistance in the lab. Ian Marshall is thanked for assistance with the bioinformatics. Three anonymous reviewers are acknowledge for their constructive criticism. This study was supported by the Danish National Research Foundation [Agreement nos. DNRF104 and DNRF136] and by a Marie Sklodowska-Curie Individual Fellowship [grant agreement No 656385] awarded to Ugo Marzocchi.
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Sandfeld, T., Marzocchi, U., Petro, C. et al. Electrogenic sulfide oxidation mediated by cable bacteria stimulates sulfate reduction in freshwater sediments. ISME J 14, 1233–1246 (2020). https://doi.org/10.1038/s41396-020-0607-5
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DOI: https://doi.org/10.1038/s41396-020-0607-5
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