A bacterial membrane sculpting protein with BAR domain-like activity

  1. Daniel A Phillips  Is a corresponding author
  2. Lori A Zacharoff  Is a corresponding author
  3. Cheri M Hampton
  4. Grace W Chong
  5. Anthony P Malanoski
  6. Lauren Ann Metskas
  7. Shuai Xu
  8. Lina J Bird
  9. Brian J Eddie
  10. Aleksandr E Miklos
  11. Grant J Jensen
  12. Lawrence F Drummy
  13. Mohamed Y El-Naggar
  14. Sarah M Glaven
  1. Oak Ridge Institute for Science and Education / US Army DEVCOM Chemical Biological Center, United States
  2. University of Southern California, United States
  3. Wright-Patterson Air Force Base, United States
  4. US Naval Research Laboratory, United States
  5. California Institute of Technology, United States
  6. US Army DEVCOM Chemical Biological Center, United States

Abstract

Bin/Amphiphysin/RVS (BAR) domain proteins belong to a superfamily of coiled-coil proteins influencing membrane curvature in eukaryotes and are associated with vesicle biogenesis, vesicle-mediated protein trafficking, and intracellular signaling. Here we report a bacterial protein with BAR domain-like activity, BdpA, from Shewanella oneidensis MR-1, known to produce redox-active membrane vesicles and micrometer-scale outer membrane extensions (OMEs). BdpA is required for uniform size distribution of membrane vesicles and influences scaffolding of OMEs into a consistent diameter and curvature. Cryogenic transmission electron microscopy reveals a strain lacking BdpA produces lobed, disordered OMEs rather than membrane tubules or narrow chains produced by the wild type strain. Overexpression of BdpA promotes OME formation during planktonic growth of S. oneidensis where they are not typically observed. Heterologous expression results in OME production in Marinobacter atlanticus and Escherichia coli. Based on the ability of BdpA to alter membrane architecture in vivo, we propose that BdpA and its homologs comprise a newly identified class of bacterial BAR domain-like proteins.

Data availability

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE [1] partner repository with the dataset identifier PXD020577.

The following data sets were generated

Article and author information

Author details

  1. Daniel A Phillips

    Oak Ridge Institute for Science and Education / US Army DEVCOM Chemical Biological Center, Aberdeen Proving Grounds, United States
    For correspondence
    daniel.a.phillips62.ctr@army.mil
    Competing interests
    Daniel A Phillips, DP and SG hold the patent US10793865B2 on Transferrable mechanism of generating inducible.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2759-5246
  2. Lori A Zacharoff

    Department of Physics and Astronomy, University of Southern California, Los Angeles, United States
    For correspondence
    zacharof@usc.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8657-0968
  3. Cheri M Hampton

    Materials and Manufacturing Directorate, Wright-Patterson Air Force Base, Dayton, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0069-8712
  4. Grace W Chong

    Department of Biological Sciences, University of Southern California, Los Angeles, United States
    Competing interests
    No competing interests declared.
  5. Anthony P Malanoski

    Center for Bio/Molecular Science and Engineering, US Naval Research Laboratory, Washington, United States
    Competing interests
    No competing interests declared.
  6. Lauren Ann Metskas

    Biological Sciences, Chemistry, California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8073-6960
  7. Shuai Xu

    Department of Physics and Astronomy, University of Southern California, Los Angeles, United States
    Competing interests
    No competing interests declared.
  8. Lina J Bird

    Center for Bio/Molecular Science and Engineering, US Naval Research Laboratory, Washington, United States
    Competing interests
    No competing interests declared.
  9. Brian J Eddie

    Center for Bio/Molecular Science and Engineering, US Naval Research Laboratory, Washington, United States
    Competing interests
    No competing interests declared.
  10. Aleksandr E Miklos

    BioSciences Division, BioChemistry Branch, US Army DEVCOM Chemical Biological Center, Aberdeen Proving Ground, United States
    Competing interests
    No competing interests declared.
  11. Grant J Jensen

    Biology and Bioengineering, California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1556-4864
  12. Lawrence F Drummy

    Materials and Manufacturing Directorate, Wright-Patterson Air Force Base, Dayton, United States
    Competing interests
    No competing interests declared.
  13. Mohamed Y El-Naggar

    Department of Physics and Astronomy, Biological Sciences, and Chemistry, University of Southern California, Los Angeles, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5599-6309
  14. Sarah M Glaven

    Center for Bio/Molecular Science and Engineering, US Naval Research Laboratory, Washington, United States
    Competing interests
    Sarah M Glaven, DP and SG hold the patent US10793865B2 on Transferrable mechanism of generating inducible.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0857-3391

Funding

U.S. Department of Defense

  • Sarah M Glaven

Office of Naval Research (N00014-18-1-2632)

  • Mohamed Y El-Naggar

National Science Foundation (DEB-1542527)

  • Mohamed Y El-Naggar

U.S. Department of Energy (DE-FG02-13ER16415)

  • Mohamed Y El-Naggar

National Institute of General Medical Sciences (GM122588)

  • Grant J Jensen

U.S. Army Combat Capabilities Development Command (PE 0601102A Project VR9)

  • Aleksandr E Miklos

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Karina B Xavier, Instituto Gulbenkian de Ciência, Portugal

Version history

  1. Preprint posted: January 31, 2020 (view preprint)
  2. Received: June 15, 2020
  3. Accepted: October 12, 2021
  4. Accepted Manuscript published: October 13, 2021 (version 1)
  5. Version of Record published: December 20, 2021 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Daniel A Phillips
  2. Lori A Zacharoff
  3. Cheri M Hampton
  4. Grace W Chong
  5. Anthony P Malanoski
  6. Lauren Ann Metskas
  7. Shuai Xu
  8. Lina J Bird
  9. Brian J Eddie
  10. Aleksandr E Miklos
  11. Grant J Jensen
  12. Lawrence F Drummy
  13. Mohamed Y El-Naggar
  14. Sarah M Glaven
(2021)
A bacterial membrane sculpting protein with BAR domain-like activity
eLife 10:e60049.
https://doi.org/10.7554/eLife.60049

Share this article

https://doi.org/10.7554/eLife.60049

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