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The ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryo-tomography

Poorna Subramanian, Sahand Pirbadian, Mohamed Y. El-Naggar, Grant J. Jensen
doi: https://doi.org/10.1101/103242
Poorna Subramanian
aDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125
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Sahand Pirbadian
bDepartment of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089
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Mohamed Y. El-Naggar
bDepartment of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089
cDepartment of Chemistry, University of Southern California, Los Angeles, CA 90089
dMolecular and Computational Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089
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  • For correspondence: jensen@caltech.edu mnaggar@usc.edu
Grant J. Jensen
aDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125
eHoward Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125
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  • For correspondence: jensen@caltech.edu mnaggar@usc.edu
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Abstract:

Bacterial nanowires have garnered recent interest as a proposed Extracellular Electron Transfer (EET) pathway that links the bacterial electron transport chain to solid-phase electron acceptors away from the cell. In vivo fluorescence Light Microscopy (fLM) imaging recently showed that Shewanella oneidensis MR-1 nanowires are extensions of the outer membrane that contain EET components. However, their fine structure and distribution of cytochrome electron carriers remained unclear, making it difficult to evaluate the electron transport mechanism along the nanowires. Here, we report high-resolution images of nanowires using Electron Cryo-Tomography (ECT). We developed a robust method for fLM imaging of nanowire growth on electron microscopy grids and used correlative light and electron microscopy to identify and image the same nanowires by ECT. Our results confirm that S. oneidensis nanowires are outer membrane extensions, and further reveal that nanowires are dynamic chains of interconnected Outer Membrane Vesicles (OMVs) with variable dimensions, curvature, and extent of tubulation. Junction densities that potentially stabilize OMV chains are seen between neighboring vesicles in cryotomograms. Our ECT results also provide the first hints of the positions and packing of periplasmic and outer membrane proteins consistent with cytochromes. We observe tight packing of putative cytochromes along lateral patches that extend tens of nanometers, but not across the micrometer scale of whole nanowires. We therefore propose that electron transfer along nanowires involves a combination of direct hopping and diffusive events that link neighboring redox proteins.

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Posted January 28, 2017.
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The ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryo-tomography
Poorna Subramanian, Sahand Pirbadian, Mohamed Y. El-Naggar, Grant J. Jensen
bioRxiv 103242; doi: https://doi.org/10.1101/103242
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The ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryo-tomography
Poorna Subramanian, Sahand Pirbadian, Mohamed Y. El-Naggar, Grant J. Jensen
bioRxiv 103242; doi: https://doi.org/10.1101/103242

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