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      Extracellular electron transfer mechanisms between microorganisms and minerals.

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          Abstract

          Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is neither physically permeable to minerals nor electrically conductive, microorganisms have evolved strategies to exchange electrons with extracellular minerals. In this Review, we discuss the molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species. Microorganisms that have extracellular electron transfer capability can be used for biotechnological applications, including bioremediation, biomining and the production of biofuels and nanomaterials.

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          Most cited references 126

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          Extracellular electron transfer via microbial nanowires.

          Microbes that can transfer electrons to extracellular electron acceptors, such as Fe(iii) oxides, are important in organic matter degradation and nutrient cycling in soils and sediments. Previous investigations on electron transfer to Fe(iii) have focused on the role of outer-membrane c-type cytochromes. However, some Fe(iii) reducers lack c-cytochromes. Geobacter species, which are the predominant Fe(iii) reducers in many environments, must directly contact Fe(iii) oxides to reduce them, and produce monolateral pili that were proposed, on the basis of the role of pili in other organisms, to aid in establishing contact with the Fe(iii) oxides. Here we report that a pilus-deficient mutant of Geobacter sulfurreducens could not reduce Fe(iii) oxides but could attach to them. Conducting-probe atomic force microscopy revealed that the pili were highly conductive. These results indicate that the pili of G. sulfurreducens might serve as biological nanowires, transferring electrons from the cell surface to the surface of Fe(iii) oxides. Electron transfer through pili indicates possibilities for other unique cell-surface and cell-cell interactions, and for bioengineering of novel conductive materials.
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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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              Humic substances as electron acceptors for microbial respiration

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                Author and article information

                Journal
                Nat. Rev. Microbiol.
                Nature reviews. Microbiology
                Springer Nature
                1740-1534
                1740-1526
                October 2016
                : 14
                : 10
                Affiliations
                [1 ] Department of Biological Sciences and Technology, School of Environmental Studies, China University of Geoscience in Wuhan, Wuhan, Hubei 430074, China.
                [2 ] Department of Geology and Environmental Earth Science, Miami University, Oxford, Ohio 45056, USA.
                [3 ] State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China.
                [4 ] Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48823, USA.
                [5 ] The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington 99164, USA.
                [6 ] School of Space and Earth Sciences, Peking University, Beijing 100871, China.
                [7 ] College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China.
                [8 ] Department of Chemistry, University of Science and Technology of China, Hefei 230026, China.
                [9 ] Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99352, USA.
                Article
                nrmicro.2016.93
                10.1038/nrmicro.2016.93
                27573579

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