Hydrogen Metabolism in Shewanella oneidensis MR-1

Shewanella oneidensis MR-1 is a facultative sediment microorganism which usesdiverse compounds, such as oxygen and fumarate, as well as insolubleFe(III) and Mn(IV) as electron acceptors. The electron donor spectrumis more limited and includes metabolic end products of primaryfermenting bacteria, such as lactate, formate, and hydrogen. While theutilization of hydrogen as an electron donor has been describedpreviously, we report here the formation of hydrogen from pyruvateunder anaerobic, stationary-phase conditions in the absence of anexternal electron acceptor. Genes for the two S. oneidensisMR-1 hydrogenases, hydA, encoding a periplasmic [Fe-Fe]hydrogenase, and hyaB, encoding a periplasmic [Ni-Fe]hydrogenase, were found to be expressed only under anaerobic conditionsduring early exponential growth and into stationary-phase growth.Analyses of ΔhydA, ΔhyaB, andΔhydA ΔhyaB in-frame-deletion mutantsindicated that HydA functions primarily as a hydrogen-forminghydrogenase while HyaB has a bifunctional role and represents thedominant hydrogenase activity under the experimental conditions tested.Based on results from physiological and genetic experiments, we proposethat hydrogen is formed from pyruvate by multiple parallel pathways,one pathway involving formate as an intermediate, pyruvate-formatelyase, and formate-hydrogen lyase, comprised of HydA hydrogenase andformate dehydrogenase, and a formate-independent pathway involvingpyruvate dehydrogenase. A reverse electron transport chain ispotentially involved in a formate-hydrogen lyase-independent pathway.While pyruvate does not support a fermentative mode of growth in thismicroorganism, pyruvate, in the absence of an electron acceptor,increased cell viability in anaerobic, stationary-phase cultures,suggesting a role in the survival of S. oneidensis MR-1 understationary-phaseconditions.