title: Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components.
abstract: Bacterial nanowires offer an extracellular electron transport (EET) pathway for linking the respiratory chain of bacteria to external surfaces, including oxidized metals in the environment and engineered electrodes in renewable energy devices. Despite the global, environmental, and technological consequences of this biotic-abiotic interaction, the composition, physiological relevance, and electron transport mechanisms of bacterial nanowires remain unclear. We report, to our knowledge, the first in vivo observations of the formation and respiratory impact of nanowires in the model metal-reducing microbe Shewanella oneidensis MR-1. Live fluorescence measurements, immunolabeling, and quantitative gene expression analysis point to S. oneidensis MR-1 nanowires as extensions of the outer membrane and periplasm that include the multiheme cytochromes responsible for EET, rather than pilin-based structures as previously thought. These membrane extensions are associated with outer membrane vesicles, structures ubiquitous in Gram-negative bacteria, and are consistent with bacterial nanowires that mediate long-range EET by the previously proposed multistep redox hopping mechanism. Redox-functionalized membrane and vesicular extensions may represent a general microbial strategy for electron transport and energy distribution.
authors.affiliation: Department of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089;
authors.forename: Sahand
authors.initials: S
authors.lastname: Pirbadian
authors.affiliation: Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA 16802;
authors.forename: Sarah E
authors.initials: SE
authors.lastname: Barchinger
authors.affiliation: Department of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089;
authors.forename: Kar Man
authors.initials: KM
authors.lastname: Leung
authors.affiliation: Department of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089;
authors.forename: Hye Suk
authors.initials: HS
authors.lastname: Byun
authors.affiliation: Department of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089;
authors.forename: Yamini
authors.initials: Y
authors.lastname: Jangir
authors.affiliation: Department of Biological Sciences, University of Wisconsin, Milwaukee, WI 53211;
authors.forename: Rachida A
authors.initials: RA
authors.lastname: Bouhenni
authors.affiliation: Pacific Northwest National Laboratory, Richland, WA 99354;
authors.forename: Samantha B
authors.initials: SB
authors.lastname: Reed
authors.affiliation: Pacific Northwest National Laboratory, Richland, WA 99354;
authors.forename: Margaret F
authors.initials: MF
authors.lastname: Romine
authors.affiliation: Department of Biological Sciences, University of Wisconsin, Milwaukee, WI 53211;
authors.forename: Daad A
authors.initials: DA
authors.lastname: Saffarini
authors.affiliation: Pacific Northwest National Laboratory, Richland, WA 99354;
authors.forename: Liang
authors.initials: L
authors.lastname: Shi
authors.affiliation: Department of Civil and Environmental Engineering, Rensselaer Polytechnic Institute, Troy, NY 12180;
authors.forename: Yuri A
authors.initials: YA
authors.lastname: Gorby
authors.affiliation: Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA 16802; Department of Chemistry, Pennsylvania State University, University Park, PA 16802; and.
authors.forename: John H
authors.initials: JH
authors.lastname: Golbeck
authors.affiliation: Department of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089; Molecular and Computational Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089 mnaggar@usc.edu.
authors.forename: Mohamed Y
authors.initials: MY
authors.lastname: El-Naggar
mesh_terms: D001425:Bacterial Outer Membrane Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D056804:Biofuels; D003574:Cytochrome c Group / Q000235:genetics / Q000378:metabolism; D004579:Electron Transport / Q000502:physiology; D015964:Gene Expression Regulation, Bacterial; D018625:Microscopy, Atomic Force; D008956:Models, Chemical; D053770:Nanowires / Q000648:ultrastructure*; D010084:Oxidation-Reduction; D019897:Periplasm / Q000235:genetics / Q000502:physiology*; D020592:Shewanella / Q000378:metabolism* / Q000648:ultrastructure*
chemical_list: D001425:Bacterial Outer Membrane Proteins; D056804:Biofuels; D003574:Cytochrome c Group; C114590:omc A protein, Shewanella putrefaciens; C433527:MtrC protein, Shewanella
keywords: bioelectronics; extracellular electron transfer; membrane cytochromes; respiration