1. Microbiology and Infectious Disease
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Lipoprotein DolP supports proper folding of BamA in the bacterial outer membrane, promoting fitness upon envelope stress

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Cite this article as: eLife 2021;10:e67817 doi: 10.7554/eLife.67817

Abstract

Integral outer membrane proteins (OMPs) are crucial for the maintenance of the proteobacterial envelope permeability barrier to some antibiotics and detergents. In Enterobacteria, envelope stress caused by unfolded OM proteins (OMPs) activates the sigmaE (σE) transcriptional response. σE upregulates OMP-biogenesis factors, including the b-barrel assembly machinery (BAM) that catalyzes OMP folding. Here we report that DolP (formerly YraP), a σE-upregulated and poorly understood OM lipoprotein, is crucial for fitness in cells that undergo envelope stress. We demonstrate that DolP interacts with the BAM complex by associating to OM-assembled BamA. We provide evidence that DolP is important for proper folding of BamA that overaccumulates in the OM, thus supporting OMP biogenesis and OM integrity. Notably, mid-cell recruitment of DolP had been linked to regulation of septal peptidoglycan remodelling by an unknown mechanism. We now reveal that, during envelope stress, DolP loses its association with the mid-cell, thereby suggesting a mechanistic link between envelope stress caused by impaired OMP biogenesis and the regulation of a late step of cell division.

Data availability

All data generated and analysed during this study are available in the manuscript and supporting files. Source data related to the CRISPRi screen are provided in the supporting files.

Article and author information

Author details

  1. David Ranava

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5841-7699
  2. Yiying Yang

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Luis Orenday-Tapia

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1134-0823
  4. François Rousset

    Microbiology Department, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Catherine Turlan

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Violette Morales

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Lun Cui

    Microbiology Department, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Cyril Moulin

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Carine Froment

    Institute of Pharmacology and Structural Biology, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Gladys Munoz

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Jérôme Rech

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Julien Marcoux

    Institute of Pharmacology and Structural Biology, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7321-7436
  13. Anne Caumont-Sarcos

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  14. Cécile Albenne

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  15. David Bikard

    Synthetic Biology Laboratory, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5729-1211
  16. Raffaele Ieva

    Laboratory of Microbiology and Molecular Genetics, CNRS, Toulouse, France
    For correspondence
    raffaele.ieva@univ-tlse3.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3405-0650

Funding

Centre National de la Recherche Scientifique (ATIP-Avenir)

  • Raffaele Ieva

Agence Nationale de la Recherche (ANR-10-INBS-08)

  • Julien Marcoux

Agence Nationale de la Recherche (ANR-10-LABX-62-IBEID)

  • David Bikard

Fondation pour la Recherche Médicale (PostDoc Fellowship)

  • David Ranava

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

Reviewing Editor

  1. Bavesh D Kana, University of the Witwatersrand, South Africa

Publication history

  1. Received: February 24, 2021
  2. Accepted: April 4, 2021
  3. Accepted Manuscript published: April 13, 2021 (version 1)
  4. Version of Record published: April 28, 2021 (version 2)

Copyright

© 2021, Ranava et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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