Oxidizing Electrode Potentials Decrease Current Production and Coulombic Efficiency through Cytochrome c Inactivation in Shewanella oneidensis MR-1

Previous transcriptomic profiling of Shewanella oneidensis MR-1 had suggested that electron transfer to an anode in a bioelectrochemical system may induce a general stress response (similar to a heat-shock response) and/or an increase in protein turnover rates. Analysis of this microbe grown with a wide variety of electron acceptors also indicated that protein turnover may be related to the redox potential of the terminal electron acceptor. To investigate whether electrodes can induce stress and increase protein turnover, S. oneidensis was grown at potentiostatically poised electrodes at five redox potentials versus the standard hydrogen electrode (SHE) between -3 and +797mV(SHE). Subsequently, current production, coulombic efficiency, and transcription levels of marker genes for general stress and protein turnover were measured. Maximal current production was found at +397mV(SHE), and maximal coulombic efficiency was observed at +197mV(SHE). Both values decreased at more positive (oxidizing) potentials, that is, extracellular electron transfer of S. oneidensis is optimal at moderate electrode potentials. In contrast to previous findings, transcript measurements of a stress-marker gene indicate that extracellular electron transfer does not increase general stress in comparison with aerobic respiration. Although overall protein turnover is not related to electrode potential, increased expression of a protease suggests that protein degradation increases at oxidizing electrode potentials. Cyclic voltammetry revealed decreased activity of c-type cytochromes at the higher potentials, which indicates that oxidizing electrodes directly damage electron-transfer proteins at the electrode surface.