A bacterial membrane sculpting protein with BAR domain-like activity
Creators
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1.
United States Department of the Army
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2.
Oak Ridge Associated Universities
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3.
University of Southern California
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4.
Wright-Patterson Air Force Base
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5.
United States Naval Research Laboratory
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6.
California Institute of Technology
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7.
Brigham Young University
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. Cryo-TEM reveals that 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.
Additional Information
© 2021 Phillips et al. 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. Preprint posted: January 31, 2020 (view preprint); Received: June 15, 2020; Accepted: October 12, 2021; Accepted Manuscript published: October 13, 2021 (version 1); Version of Record published: December 20, 2021 (version 2). We thank Dr Jeffrey Gralnick for helpful discussions and advice, as well as the S. oneidensis JG1194 strain; Dr Adam Meyer and Dr Chris Voigt for the DAPG-inducible Marionette promoter; Dr Annie Moradian and Dr Mike Sweredoski and the California Institute of Technology Proteome Exploration Lab for useful discussions on the preparation and analysis of proteomics data. Some of the cryo-TEM work was done in the Beckman Institute Resource Center for Transmission Electron Microscopy at Caltech. This work was supported by the United States Department of Defense Synthetic Biology for Military Environments (SBME) Applied Research for the Advancement of Science and Technology Priorities (ARAP) program. DP and AEM were partially supported by the U.S. Army via the Surface Science Initiative Program (PE 0601102 A Project VR9) at the Combat Capabilities Development Command (CCDC) Chemical Biological Center. Work in ME-N's lab was supported by the U.S. Office of Naval Research Multidisciplinary University Research Initiative Grant No. N00014-18-1-2632. LAZ was partially supported by the National Science Foundation grant DEB-1542527. GWC was also supported by the National Science Foundation Graduate Research Fellowship Program (grant DGE1418060). SX was supported by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy through grant DE-FG02-13ER16415. Work in GJJ's lab was supported by the National Institute of Health (GM122588 to GJJ). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions: Daniel A Phillips, Conceptualization, DP and LZ conceived the study independently then combined projects when complementary data on BdpA was discovered., Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing – original draft, Writing – review and editing; Lori A Zacharoff, Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing – original draft, Writing – review and editing; Cheri M Hampton, Formal analysis, Investigation, Methodology, Visualization, Writing – review and editing; Grace W Chong, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – review and editing; Anthony P Malanoski, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review and editing; Lauren Ann Metskas, Investigation, Methodology, Visualization, Writing – review and editing; Shuai Xu, Lina J Bird, Resources, Writing – review and editing; Brian J Eddie, Data curation, Formal analysis, Investigation, Validation, Writing – original draft, Writing – review and editing; Aleksandr E Miklos, Funding acquisition, Investigation, Software, Visualization; Grant J Jensen, Funding acquisition, Supervision, Writing – review and editing; Lawrence F Drummy, Investigation, Methodology, Supervision, Validation, Visualization, Writing – review and editing; Mohamed Y El-Naggar, Sarah M Glaven, Formal analysis, Funding acquisition, Project administration, Resources, Supervision, Writing – original draft, Writing – review and editing. Competing interests: Daniel A Phillips: along with SG holds the patent US10793865B2 on "Transferrable mechanism of generating inducible, BAR domain protein-mediated bacterial outer membrane extensions". Sarah M Glaven: along with DP holds the patent US10793865B2 on "Transferrable mechanism of generating inducible, BAR domain protein-mediated bacterial outer membrane extensions". The other authors declare that no competing interests exist. 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.Attached Files
Published - elife-60049-v2.pdf
Submitted - 2020.01.30.926147v3.full.pdf
Supplemental Material - elife-60049-supp1-v2.xlsx
Supplemental Material - elife-60049-supp2-v2.docx
Supplemental Material - elife-60049-transrepform1-v2.docx
Supplemental Material - elife-60049-video1.mp4
Supplemental Material - elife-60049-video2.mp4
Supplemental Material - elife-60049-video3.mp4
Supplemental Material - elife-60049-video4.mp4
Supplemental Material - elife-60049-video5.mp4
Supplemental Material - elife-60049-video6.mp4
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Additional details
Additional titles
- Alternative title
- A Prokaryotic Membrane Sculpting BAR Domain Protein
Identifiers
- PMCID
- PMC8687657
- Eprint ID
- 101068
- Resolver ID
- CaltechAUTHORS:20200203-093321992
Related works
- Describes
- 10.1101/2020.01.30.926147 (DOI)
- https://www.ebi.ac.uk/pride/archive/projects/PXD020577 (URL)
Funding
- Department of Defense
- Army Research Office (ARO)
- PE 0601102
- Office of Naval Research (ONR)
- N00014-18-1-2632
- NSF
- DEB-1542527
- NSF Graduate Research Fellowship
- DGE-1418060
- Department of Energy (DOE)
- DE-FG02-13ER16415
- NIH
- GM122588
Dates
- Created
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2020-02-03Created from EPrint's datestamp field
- Updated
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2022-01-28Created from EPrint's last_modified field
Caltech Custom Metadata
- Caltech groups
- Division of Biology and Biological Engineering (BBE)