Defining the function of OmpA in the Rcs stress response

  1. Kilian Dekoninck
  2. Juliette Létoquart
  3. Cédric Laguri
  4. Pascal Demange
  5. Robin Bevernaegie
  6. Jean-Pierre Simorre
  7. Olivia Dehu
  8. Bogdan I Iorga
  9. Benjamin Elias
  10. Seung-Hyun Cho  Is a corresponding author
  11. Jean-Francois Collet  Is a corresponding author
  1. Universite catholique de Louvain, Belgium
  2. Université Grenoble Alpes, CNRS, CEA, France
  3. Université Paul Sabatier, France
  4. Université Grenoble Alpes, France

Abstract

OmpA, a protein commonly found in the outer membrane of Gram-negative bacteria, has served as a paradigm for the study of b-barrel proteins for several decades. In Escherichia coli, OmpA was previously reported to form complexes with RcsF, a surface-exposed lipoprotein that triggers the Rcs stress response when damage occurs in the outer membrane and the peptidoglycan. How OmpA interacts with RcsF and whether this interaction allows RcsF to reach the surface has remained unclear. Here, we integrated in vivo and in vitro approaches to establish that RcsF interacts with the C-terminal, periplasmic domain of OmpA, not with the N-terminal b-barrel, thus implying that RcsF does not reach the bacterial surface via OmpA. Our results suggest a novel function for OmpA in the cell envelope: OmpA competes with the inner membrane protein IgaA, the downstream Rcs component, for RcsF binding across the periplasm, thereby regulating the Rcs response.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 3, 4A, 4B, 5B, 5D and 6 supplement 1.

Article and author information

Author details

  1. Kilian Dekoninck

    de Duve Institute, Universite catholique de Louvain, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5093-1343
  2. Juliette Létoquart

    de Duve Institute, Universite catholique de Louvain, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  3. Cédric Laguri

    IBS, Université Grenoble Alpes, CNRS, CEA, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Pascal Demange

    IPBS, Université Paul Sabatier, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Robin Bevernaegie

    MOST, Universite catholique de Louvain, Louvain-la-Neuve, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1605-9253
  6. Jean-Pierre Simorre

    Institut de Biologie Structurale, Université Grenoble Alpes, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Olivia Dehu

    de Duve Institute, Universite catholique de Louvain, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  8. Bogdan I Iorga

    de Duve Institute, Universite catholique de Louvain, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0392-1350
  9. Benjamin Elias

    MOST, Universite catholique de Louvain, Louvain-la-Neuve, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5037-3313
  10. Seung-Hyun Cho

    de Duve Institute, Universite catholique de Louvain, Brussels, Belgium
    For correspondence
    seung.cho@uclouvain.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5548-4239
  11. Jean-Francois Collet

    de Duve Institute, Universite catholique de Louvain, Brussels, Belgium
    For correspondence
    jean-francois.collet@uclouvain.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8069-7036

Funding

Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture

  • Kilian Dekoninck
  • Robin Bevernaegie

Fonds De La Recherche Scientifique - FNRS

  • Kilian Dekoninck
  • Juliette Létoquart
  • Robin Bevernaegie
  • Olivia Dehu
  • Benjamin Elias
  • Seung-Hyun Cho

FRFS-WELBIO

  • Jean-Francois Collet

FRISBI (ANR-10-INBS-05-02)

  • Cédric Laguri
  • Jean-Pierre Simorre

GRAL

  • Cédric Laguri
  • Jean-Pierre Simorre

CBH-EUR-GS (ANR-17-EURE-0003)

  • Cédric Laguri
  • Jean-Pierre Simorre

Fédération Wallonie-Bruxelles (ARC 17/22-087)

  • Jean-Francois Collet

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

Reviewing Editor

  1. Michael T Laub, Massachusetts Institute of Technology, United States

Publication history

  1. Received: July 8, 2020
  2. Accepted: September 26, 2020
  3. Accepted Manuscript published: September 28, 2020 (version 1)
  4. Version of Record published: October 13, 2020 (version 2)

Copyright

© 2020, Dekoninck 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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  1. Kilian Dekoninck
  2. Juliette Létoquart
  3. Cédric Laguri
  4. Pascal Demange
  5. Robin Bevernaegie
  6. Jean-Pierre Simorre
  7. Olivia Dehu
  8. Bogdan I Iorga
  9. Benjamin Elias
  10. Seung-Hyun Cho
  11. Jean-Francois Collet
(2020)
Defining the function of OmpA in the Rcs stress response
eLife 9:e60861.
https://doi.org/10.7554/eLife.60861

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