Abstract
Many bacteria use hydrogen anaerobically as both a source and sink for electrons; consuming hydrogen when it is plentiful and producing it when concentrations are low enough to allow proton reduction. While this can increase an organism’s competitiveness, hydrogen uptake or excretion can also make it difficult to control electron flux to a specific product. For example, when Shewanella oneidensis strain MR-1 is used to oxidize organic molecules and recover electrons in microbial electrochemical devices, small changes in ambient hydrogen concentrations could dramatically alter the efficiency of electron capture at the anode due to this organism’s respiratory flexibility. When new three-electrode reactor designs created to minimize oxygen intrusion during anodic growth were tested with lactate-oxidizing S. oneidensis, current production decreased significantly in reactors vented to remove hydrogen produced at the counter electrode, suggesting a role for hydrogen uptake or disposal when cells used electrodes as electron acceptors. A ∆hydA∆hyaB mutant lacking both hydrogenases reversed this trend, and nearly doubled current production rates. This increase was shown to be due to the efficiency of lactate oxidation, as 90% of electrons were recovered as electricity in the ∆hydA∆hyaB mutant compared to only 50% for wild type. Experiments with Fe(III) oxide provided additional evidence that S. oneidensis generates hydrogen reducing equivalents during reduction of insoluble electron acceptors, while experiments with cells incubated with Fe(III) citrate showed increased survival of wild-type compared to ∆hydA∆hyaB in stationary phase. Together these data show how the multiple routes of electron disposal of S. oneidensis, while beneficial under changing conditions, limits the efficiency of electron recovery in electrochemical systems, and demonstrates a simple approach to increasing current production rates in systems where hydrogen is being captured as a product.
Highlights
Life began, and continues to thrive today, in anaerobic ecosystems across the planet
Shewanella oneidensis strain MR-1 is a facultative anaerobe that thrives in redox-stratified environments due to its ability to utilize a wide range of terminal electron acceptors (Nealson and Scott, 2006; Hau and Gralnick, 2007)
Shewanella species thrive in a variety of environments because they encode multiple electron transport pathways enabling the use of a wide array of terminal electron acceptors, including protons, as they become available
Summary
Continues to thrive today, in anaerobic ecosystems across the planet. Hydrogen Production by S. oneidensis is often constrained by the ability of cells to dispose of electrons generated during carbon compound oxidation; the availability of electron acceptors such as nitrate or Fe(III) controls the options for energy generation within a niche (Thauer et al, 1977). In all of these environments, hydrogenases represent a means to dispose of low-potential electrons via proton reduction, depending on ambient concentrations. When Shewanella is used to supply electrons to the anode in a device termed a “Microbial Electrolysis Cell,” a small voltage can be applied to these electrons to produce valuable cathodic hydrogen at a counter electrode (Bretschger et al, 2007; Coursolle et al, 2010)
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