Fumarate disproportionation by Geobacter sulfurreducens and its involvement in biocorrosion and interspecies electron transfer

Abstract

The model electroactive bacterium Geobacter sulfurreducens can acquire electrons directly from solid donors including metals and other species. Reports on this physiology concluding that solid donors are the only electron sources were conducted with fumarate believed to serve exclusively as the terminal electron acceptor (TEA). Here, G. sulfurreducens was repeatedly transferred for adaptation within a growth medium containing only fumarate and no other solid or soluble substrate. The resulting evolved strain grew efficiently with either the C4-dicarboxylate fumarate or malate acting simultaneously as electron donor, carbon source, and electron acceptor via disproportionation. Whole-genome sequencing identified 38 mutations including one in the regulator PilR known to repress the expression of the C4-dicarboxylate antiporter DcuB essential to G. sulfurreducens when growing with fumarate. Futhermore, the PilR mutation was identical to the sole mutation previously reported in an evolved G. sulfurreducens grown in a co-culture assumed to derive energy solely from direct interspecies electron transfer, but cultivated with fumarate as the TEA. When cultivating the fumarate-adapted strain in the presence of stainless steel and fumarate, biocorrosion was observed and bacterial growth was accelerated 2.3 times. These results suggest that G. sulfurreducens can conserve energy concomitantly from C4-dicarboxylate disproportionation and the oxidation of a solid electron donor. This co-metabolic capacity confers an advantage to Geobacter for survival and colonization and explains in part why these microbes are omnipresent in different anaerobic ecosystems.