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

• Published in: The ISME Journal Vol. 14; no. 5; pp. 1233 - 1246
• Main Authors: Sandfeld, Tobias, Marzocchi, Ugo, Petro, Caitlin, Schramm, Andreas, Risgaard-Petersen, Nils
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.05.2020; Nature Publishing Group
• Subjects: 631/326/47; 704/158/855; 9/10; Availability; Bacteria; Bacteria - metabolism; Biomedical and Life Sciences; Chemoautotrophic Growth; Community composition; Correlation analysis; Ecology; Electric fields; Electron Transport; Evolutionary Biology; Fresh water; Fresh Water - microbiology; Geologic Sediments - microbiology; Greenhouse effect; Greenhouse gases; Iron sulfides; Life Sciences; Marine environment; Methanogenesis; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microorganisms; Nitrates; Oxidation; Oxidation-Reduction; Oxygen; Sediments; Stimulation; Sulfate reduction; Sulfates; Sulfides; Sulfur; Sulfur - metabolism; Sulfur cycle
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-020-0607-5

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.