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Electromicrobiology: realities, grand challenges, goals and predictions

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Microbial Biotechnology

John Wiley and Sons Inc.

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      Electromicrobiology is a subdiscipline of microbiology that involves extracellular electron transfer (EET) to (or from) insoluble electron active redox compounds located outside the outer membrane of the cell. These interactions can often be studied using electrochemical techniques which have provided novel insights into microbial physiology in recent years. The mechanisms (and variations) of outward EET are well understood for two model systems, Shewanella and Geobacter, both of which employ multihaem cytochromes to provide an electron conduit to the cell exterior. In contrast, little is known of the intricacies of inward EET, even in these model systems. Given the number of labs now working on EET, it seems likely that most of the mechanistic details will be understood in a few years for the model systems, and the many applications of electromicrobiology will continue to move forward. But emerging work, using electrodes as electron acceptors and donors is providing an abundance of new types of microbes capable of EET inward and/or outward: microbes that are clearly different from our known systems. The extent of this very diverse, and perhaps widely distributed and biogeochemically important ability needs to be determined to understand the mechanisms, importance, and raison d'etre of EET for microbial biology.

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      Most cited references 46

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      Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms.

      Shewanella oneidensis MR-1 produced electrically conductive pilus-like appendages called bacterial nanowires in direct response to electron-acceptor limitation. Mutants deficient in genes for c-type decaheme cytochromes MtrC and OmcA, and those that lacked a functional Type II secretion pathway displayed nanowires that were poorly conductive. These mutants were also deficient in their ability to reduce hydrous ferric oxide and in their ability to generate current in a microbial fuel cell. Nanowires produced by the oxygenic phototrophic cyanobacterium Synechocystis PCC6803 and the thermophilic, fermentative bacterium Pelotomaculum thermopropionicum reveal that electrically conductive appendages are not exclusive to dissimilatory metal-reducing bacteria and may, in fact, represent a common bacterial strategy for efficient electron transfer and energy distribution.
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        Shewanella secretes flavins that mediate extracellular electron transfer.

        Bacteria able to transfer electrons to metals are key agents in biogeochemical metal cycling, subsurface bioremediation, and corrosion processes. More recently, these bacteria have gained attention as the transfer of electrons from the cell surface to conductive materials can be used in multiple applications. In this work, we adapted electrochemical techniques to probe intact biofilms of Shewanella oneidensis MR-1 and Shewanella sp. MR-4 grown by using a poised electrode as an electron acceptor. This approach detected redox-active molecules within biofilms, which were involved in electron transfer to the electrode. A combination of methods identified a mixture of riboflavin and riboflavin-5'-phosphate in supernatants from biofilm reactors, with riboflavin representing the dominant component during sustained incubations (>72 h). Removal of riboflavin from biofilms reduced the rate of electron transfer to electrodes by >70%, consistent with a role as a soluble redox shuttle carrying electrons from the cell surface to external acceptors. Differential pulse voltammetry and cyclic voltammetry revealed a layer of flavins adsorbed to electrodes, even after soluble components were removed, especially in older biofilms. Riboflavin adsorbed quickly to other surfaces of geochemical interest, such as Fe(III) and Mn(IV) oxy(hydr)oxides. This in situ demonstration of flavin production, and sequestration at surfaces, requires the paradigm of soluble redox shuttles in geochemistry to be adjusted to include binding and modification of surfaces. Moreover, the known ability of isoalloxazine rings to act as metal chelators, along with their electron shuttling capacity, suggests that extracellular respiration of minerals by Shewanella is more complex than originally conceived.
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          Towards environmental systems biology of Shewanella.

          Bacteria of the genus Shewanella are known for their versatile electron-accepting capacities, which allow them to couple the decomposition of organic matter to the reduction of the various terminal electron acceptors that they encounter in their stratified environments. Owing to their diverse metabolic capabilities, shewanellae are important for carbon cycling and have considerable potential for the remediation of contaminated environments and use in microbial fuel cells. Systems-level analysis of the model species Shewanella oneidensis MR-1 and other members of this genus has provided new insights into the signal-transduction proteins, regulators, and metabolic and respiratory subsystems that govern the remarkable versatility of the shewanellae.

            Author and article information

            [ 1 ] Department of Earth SciencesUniversity of Southern California Los Angeles CAUSA
            Author notes
            [* ]For correspondence. E‐mail knealson@ . Tel. +1 213‐821‐2271; Fax +1 213‐740‐8801.
            Microb Biotechnol
            Microb Biotechnol
            Microbial Biotechnology
            John Wiley and Sons Inc. (Hoboken )
            10 August 2016
            September 2016
            : 9
            : 5 , Microbial Biotechnology‐2020 ( doiID: 10.1111/mbt2.2016.9.issue-5 )
            : 595-600
            27506517 4993177 10.1111/1751-7915.12400 MBT212400
            © 2016 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology.

            This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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