The alternative sigma factor σX mediates competence shut-off at the cell pole in Streptococcus pneumoniae

  1. Calum HG Johnston
  2. Anne-Lise Soulet
  3. Matthieu Bergé
  4. Marc Prudhomme
  5. David De Lemos
  6. Patrice Polard  Is a corresponding author
  1. CNRS, France
  2. University of Geneva, Switzerland
  3. Université Paul Sabatier, France

Abstract

Competence is a widespread bacterial differentiation program driving antibiotic resistance and virulence in many pathogens. Here, we studied the spatiotemporal localization dynamics of the key regulators that master the two intertwined and transient transcription waves defining competence in Streptococcus pneumoniae. The first wave relies on the stress-inducible phosphorelay between ComD and ComE proteins, and the second on the alternative sigma factor σX, which directs the expression of the DprA protein that turns off competence through interaction with phosphorylated ComE. We found that ComD, σX and DprA stably co-localize at one pole in competent cells, with σX physically conveying DprA next to ComD. Through this polar DprA targeting function, σX mediates the timely shut-off of the pneumococcal competence cycle, preserving cell fitness. Altogether, this study unveils an unprecedented role for a transcription σ factor in spatially coordinating the negative feedback loop of its own genetic circuit.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Calum HG Johnston

    LMGM-UMR5100, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Anne-Lise Soulet

    LMGM-UMR5100, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthieu Bergé

    Department Microbiology and Molecular Medicine, Institute of Genetics and Genomics in Geneva, University of Geneva, Geneva, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0910-6114
  4. Marc Prudhomme

    LMGM-UMR5100, Université Paul Sabatier, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  5. David De Lemos

    LMGM-UMR5100, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Patrice Polard

    LMGM-UMR5100, CNRS, Toulouse, France
    For correspondence
    Patrice.Polard@ibcg.biotoul.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0365-4347

Funding

Agence Nationale de la Recherche (ANR-10-BLAN-1331)

  • Patrice Polard

Agence Nationale de la Recherche (ANR-13-BSV8-0022)

  • Patrice Polard

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

Reviewing Editor

  1. Melanie Blokesch, Ecole Polytechnique Fédérale de Lausanne, Switzerland

Publication history

  1. Received: September 8, 2020
  2. Accepted: October 31, 2020
  3. Accepted Manuscript published: November 2, 2020 (version 1)
  4. Version of Record published: November 13, 2020 (version 2)

Copyright

© 2020, Johnston 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. Calum HG Johnston
  2. Anne-Lise Soulet
  3. Matthieu Bergé
  4. Marc Prudhomme
  5. David De Lemos
  6. Patrice Polard
(2020)
The alternative sigma factor σX mediates competence shut-off at the cell pole in Streptococcus pneumoniae
eLife 9:e62907.
https://doi.org/10.7554/eLife.62907

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