Enhancement of cell growth by uncoupling extracellular electron uptake and oxidative stress production in sediment sulfate-reducing bacteria

Microbial extracellular electron uptake (EEU) from solid electron donors has critical implications for microbial energy acquisition in energy-limited environments as well as electrochemical microbial technologies. Although EEU supplies sufficient energy to support cellular growth, additional soluble electron donors are required for most microbes to grow on electrode surfaces. Here, we demonstrated that the minimization of exogenous and endogenous oxidative stress greatly enhanced the growth rate of the sediment EEU-capable sulfate-reducing bacterium Desulfovibrio ferrophilus IS5 on an electrode without the addition of a soluble electron donor. Single-cell activity analysis by nanoscale secondary ion mass spectrometry showed that the metabolic activity of IS5 cells on the electrode was significantly enhanced following incubation in an H-type reactor, which was configured to reduce the exposure of cells to the potential oxidative stress source of the Pt counter electrode (CE). Additionally, the highest metabolic activity was observed at an electrode potential of -0.4 V (versus the standard hydrogen electrode), where electron uptake rate was not at peak. Compared to a single-chamber reactor, incubation in an H-type reactor at-0.4 V shortened the cell doubling time by 50-fold, which resulted in sufficient anabolism for cell replication (N-15/N-total > 50%). The production of strongly oxidizing species at the CE was confirmed by X-ray photoelectron spectroscopy and inductively coupled plasma mass spectrometry analyses. Transcriptome analysis revealed overexpression of antioxidative genes in cells incubated at a potential with higher current production. These results suggested that higher levels of endogenous oxidative species were produced by a more reduced electron-transport chain from trace amounts of oxygen in the reactor, thereby lowering cell activity. In conclusion, EEU may enable sediment microbes to undergo enhanced cell growth and to find niches on minerals under anaerobic energy-limited conditions, where oxidative stress is much less likely to be present.