Hydrogen-dependent current generation and energy conservation by Shewanella oneidensis MR-1 in bioelectrochemical systems

Abstract

Bioelectrochemical systems (BESs) are engineered systems that utilize electrochemical interactions between electrochemically active bacteria (EAB) and electrodes. BESs have attracted considerable attention for their utility in biotechnological processes. In a BES, hydrogen is generated by the reduction of water on low-potential cathode electrodes. However, limited information is available on the effect of hydrogen on the metabolism and growth of EAB and current generation in BESs. Here, we investigated the effect of hydrogen on current generation by a model EAB, Shewanella oneidensis MR-1. We found that this strain utilizes hydrogen as an electron donor for electrode respiration, thereby facilitating current generation and cell growth in the presence of organic substrates. Inner membrane (IM) quinones (i.e., ubiquinone and menaquinone), IM quinone-reactive hydrogenase Hya, and IM-bound quinone reductase CymA are involved in hydrogen-dependent current generation, suggesting that the redox cycling of IM quinones catalyzed by Hya and CymA contributes to the generation of the proton motive force and the synthesis of ATP via F0F1-ATPase. These findings indicate that the evolution of hydrogen on the cathode facilitates energy metabolism and growth of hydrogen-utilizing EAB associated with anodes. The results also suggest that hydrogen cycling between cathodes and anodes can hinder quantitative evaluation of organic substrate-dependent current generation in BESs.