1. Microbiology and Infectious Disease
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Unbiased homeologous recombination during pneumococcal transformation allows for multiple chromosomal integration events

  1. Jun Kurushima
  2. Nathalie Campo
  3. Renske van Raaphorst
  4. Guillaume Cerckel
  5. Patrice Polard
  6. Jan-Willem Veening  Is a corresponding author
  1. University of Lausanne, Switzerland
  2. Laboratoire de Microbiologie et Genetique Moleculaires, France
  3. Université catholique de Louvain, Belgium
  4. CNRS, France
Research Article
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Cite this article as: eLife 2020;9:e58771 doi: 10.7554/eLife.58771

Abstract

The spread of antimicrobial resistance and vaccine escape in the human pathogen Streptococcus pneumoniae can be largely attributed to competence-induced transformation. Here, we studied this process at the single-cell level. We show that within isogenic populations, all cells become naturally competent and bind exogenous DNA. We find that transformation is highly efficient and that the chromosomal location of the integration site or whether the transformed gene is encoded on the leading or lagging strand has limited influence on recombination efficiency. Indeed, we have observed multiple recombination events in single recipients in real-time. However, because of saturation and because a single stranded donor DNA replaces the original allele, transformation efficiency has an upper threshold of approximately 50% of the population. The fixed mechanism of transformation results in a fail-safe strategy for the population as half of the population generally keeps an intact copy of the original genome.

Article and author information

Author details

  1. Jun Kurushima

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Nathalie Campo

    UMR 5100, Laboratoire de Microbiologie et Genetique Moleculaires, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2917-930X
  3. Renske van Raaphorst

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Guillaume Cerckel

    Biochemistry and Molecular Genetics of Bacteria (BBGM), Institut des Sciences de la Vie, Université catholique de Louvain, Louvain-la-Neuve, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  5. Patrice Polard

    LMGM-UMR5100, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0365-4347
  6. Jan-Willem Veening

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    For correspondence
    Jan-Willem.Veening@unil.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3162-6634

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_172861)

  • Jan-Willem Veening

European Commission (771534- PneumoCaTChER.)

  • Jan-Willem Veening

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

  • Patrice Polard

Naito Foundation

  • Jun Kurushima

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (40AR40_185533)

  • Jan-Willem Veening

Agence Nationale de la Recherche (EXStasis-17-CE13-0031-01)

  • 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. Petra Anne Levin, Washington University in St. Louis, United States

Publication history

  1. Received: May 11, 2020
  2. Accepted: September 22, 2020
  3. Accepted Manuscript published: September 23, 2020 (version 1)
  4. Version of Record published: October 16, 2020 (version 2)

Copyright

© 2020, Kurushima 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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