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      Tracking Electron Uptake from a Cathode into Shewanella Cells: Implications for Energy Acquisition from Solid-Substrate Electron Donors

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          ABSTRACT

          While typically investigated as a microorganism capable of extracellular electron transfer to minerals or anodes, Shewanella oneidensis MR-1 can also facilitate electron flow from a cathode to terminal electron acceptors, such as fumarate or oxygen, thereby providing a model system for a process that has significant environmental and technological implications. This work demonstrates that cathodic electrons enter the electron transport chain of S. oneidensis when oxygen is used as the terminal electron acceptor. The effect of electron transport chain inhibitors suggested that a proton gradient is generated during cathode oxidation, consistent with the higher cellular ATP levels measured in cathode-respiring cells than in controls. Cathode oxidation also correlated with an increase in the cellular redox (NADH/FMNH 2) pool determined with a bioluminescence assay, a proton uncoupler, and a mutant of proton-pumping NADH oxidase complex I. This work suggested that the generation of NADH/FMNH 2 under cathodic conditions was linked to reverse electron flow mediated by complex I. A decrease in cathodic electron uptake was observed in various mutant strains, including those lacking the extracellular electron transfer components necessary for anodic-current generation. While no cell growth was observed under these conditions, here we show that cathode oxidation is linked to cellular energy acquisition, resulting in a quantifiable reduction in the cellular decay rate. This work highlights a potential mechanism for cell survival and/or persistence on cathodes, which might extend to environments where growth and division are severely limited.

          IMPORTANCE

          The majority of our knowledge of the physiology of extracellular electron transfer derives from studies of electrons moving to the exterior of the cell. The physiological mechanisms and/or consequences of the reverse processes are largely uncharacterized. This report demonstrates that when coupled to oxygen reduction, electrode oxidation can result in cellular energy acquisition. This respiratory process has potentially important implications for how microorganisms persist in energy-limited environments, such as reduced sediments under changing redox conditions. From an applied perspective, this work has important implications for microbially catalyzed processes on electrodes, particularly with regard to understanding models of cellular conversion of electrons from cathodes to microbially synthesized products.

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          Most cited references 68

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          Exoelectrogenic bacteria that power microbial fuel cells.

           Bruce Logan (2009)
          There has been an increase in recent years in the number of reports of microorganisms that can generate electrical current in microbial fuel cells. Although many new strains have been identified, few strains individually produce power densities as high as strains from mixed communities. Enriched anodic biofilms have generated power densities as high as 6.9 W per m(2) (projected anode area), and therefore are approaching theoretical limits. To understand bacterial versatility in mechanisms used for current generation, this Progress article explores the underlying reasons for exocellular electron transfer, including cellular respiration and possible cell-cell communication.
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            Microbial electrosynthesis - revisiting the electrical route for microbial production.

            Microbial electrocatalysis relies on microorganisms as catalysts for reactions occurring at electrodes. Microbial fuel cells and microbial electrolysis cells are well known in this context; both use microorganisms to oxidize organic or inorganic matter at an anode to generate electrical power or H(2), respectively. The discovery that electrical current can also drive microbial metabolism has recently lead to a plethora of other applications in bioremediation and in the production of fuels and chemicals. Notably, the microbial production of chemicals, called microbial electrosynthesis, provides a highly attractive, novel route for the generation of valuable products from electricity or even wastewater. This Review addresses the principles, challenges and opportunities of microbial electrosynthesis, an exciting new discipline at the nexus of microbiology and electrochemistry.
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              Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor.

              Microbes that couple growth to the reduction of manganese could play an important role in the biogeochemistry of certain anaerobic environments. Such a bacterium, Alteromonas putrefaciens MR-1, couples its growth to the reduction of manganese oxides only under anaerobic conditions. The characteristics of this reduction are consistent with a biological, and not an indirect chemical, reduction of manganese, which suggest that this bacterium uses manganic oxide as a terminal electron acceptor. It can also utilize a large number of other compounds as terminal electron acceptors; this versatility could provide a distinct advantage in environments where electron-acceptor concentrations may vary.
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                Author and article information

                Affiliations
                [a ]Department of Earth Sciences, University of Southern California, Los Angeles, California, USA
                [b ]Department of Microbiology, University of Minnesota, St. Paul, Minnesota, USA
                [c ]BioTechnology Institute, University of Minnesota, St. Paul, Minnesota, USA
                [d ]Department of Physics and Astronomy, University of Southern California, Los Angeles, California, USA
                [e ]Global Research Center for Environment and Energy Based on Nanomaterials Science, National Institute for Materials Science (NIMS), Tsukuba, Ibaraki, Japan
                [f ]Department of Biological Sciences, University of Southern California, Los Angeles, California, USA
                [g ]Department of Chemistry, University of Southern California, Los Angeles, California, USA
                University of California, Irvine
                Author notes
                Address correspondence to Annette R. Rowe, annettrr@ 123456usc.edu .

                This work is C-DEBI contribution 417 and NAI-LU contribution 125.

                This article is a direct contribution from a Fellow of the American Academy of Microbiology. Solicited external reviewers: Caroline Ajo-Franklin, Lawrence Berkeley National Laboratory; Buz Barstow, Princeton University.

                Contributors
                Role: Editor,
                University of California, Irvine
                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                27 February 2018
                Jan-Feb 2018
                : 9
                : 1
                29487241 5829830 mBio02203-17 10.1128/mBio.02203-17
                Copyright © 2018 Rowe et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                Counts
                supplementary-material: 10, Figures: 7, Tables: 1, Equations: 0, References: 69, Pages: 19, Words: 12804
                Product
                Funding
                Funded by: NSF;
                Award ID: OCE award 0939564
                Award Recipient :
                Funded by: JSPS;
                Award ID: NNA13AA92A
                Award Recipient : Award Recipient :
                Funded by: DOE;
                Award ID: DE-FG02-13ER16415
                Award Recipient : Award Recipient :
                Funded by: ONR;
                Award ID: N000141310552
                Award Recipient : Award Recipient :
                Funded by: AOR;
                Award ID: GA9550-06-01-0292
                Award Recipient :
                Funded by: NASA;
                Award ID: NNA13AA92A
                Award Recipient : Award Recipient : Award Recipient :
                Categories
                Research Article
                Custom metadata
                January/February 2018

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