Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography
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. Recent studies showed that Shewanella oneidensis MR-1 produces outer membrane (OM) and periplasmic extensions that contain EET components and hinted at their possible role as bacterial nanowires. However, their fine structure and distribution of cytochrome electron carriers under native conditions remained unclear, making it difficult to evaluate the potential electron transport (ET) mechanism along OM extensions. Here, we report high-resolution images of S. oneidensis OM extensions, using electron cryotomography (ECT). We developed a robust method for fluorescence light microscopy imaging of OM extension growth on electron microscopy grids and used correlative light and electron microscopy to identify and image the same structures by ECT. Our results reveal that S. oneidensis OM extensions 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. By comparing wild type and a cytochrome gene deletion mutant, our ECT results provide the likely positions and packing of periplasmic and outer membrane proteins consistent with cytochromes.more »
- Authors:
-
- Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125,
- Department of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089,
- Department of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089,, Department of Chemistry, 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,
- Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125,, Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125
- Publication Date:
- Research Org.:
- Univ. of Southern California, Los Angeles, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1426853
- Alternate Identifier(s):
- OSTI ID: 1540273
- Grant/Contract Number:
- FG02-13ER16415; SC0010609
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 14; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Science & Technology; Other Topics; extracellular electron transport; electron cryotomography; membrane cytochromes; bacterial nanowires; Shewanella
Citation Formats
Subramanian, Poorna, Pirbadian, Sahand, El-Naggar, Mohamed Y., and Jensen, Grant J. Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography. United States: N. p., 2018.
Web. doi:10.1073/pnas.1718810115.
Subramanian, Poorna, Pirbadian, Sahand, El-Naggar, Mohamed Y., & Jensen, Grant J. Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography. United States. https://doi.org/10.1073/pnas.1718810115
Subramanian, Poorna, Pirbadian, Sahand, El-Naggar, Mohamed Y., and Jensen, Grant J. Mon .
"Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography". United States. https://doi.org/10.1073/pnas.1718810115.
@article{osti_1426853,
title = {Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography},
author = {Subramanian, Poorna and Pirbadian, Sahand and El-Naggar, Mohamed Y. and Jensen, Grant J.},
abstractNote = {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. Recent studies showed that Shewanella oneidensis MR-1 produces outer membrane (OM) and periplasmic extensions that contain EET components and hinted at their possible role as bacterial nanowires. However, their fine structure and distribution of cytochrome electron carriers under native conditions remained unclear, making it difficult to evaluate the potential electron transport (ET) mechanism along OM extensions. Here, we report high-resolution images of S. oneidensis OM extensions, using electron cryotomography (ECT). We developed a robust method for fluorescence light microscopy imaging of OM extension growth on electron microscopy grids and used correlative light and electron microscopy to identify and image the same structures by ECT. Our results reveal that S. oneidensis OM extensions 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. By comparing wild type and a cytochrome gene deletion mutant, our ECT results provide the likely positions and packing of periplasmic and outer membrane proteins consistent with cytochromes. Based on the observed cytochrome packing density, we propose a plausible ET path along the OM extensions involving a combination of direct hopping and cytochrome diffusion. Furthermore, a mean-field calculation, informed by the observed ECT cytochrome density, supports this proposal by revealing ET rates on par with a fully packed cytochrome network.},
doi = {10.1073/pnas.1718810115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 14,
volume = 115,
place = {United States},
year = {Mon Mar 19 00:00:00 EDT 2018},
month = {Mon Mar 19 00:00:00 EDT 2018}
}
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https://doi.org/10.1073/pnas.1718810115
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