Pirating conserved phage mechanisms promotes promiscuous staphylococcal pathogenicity island transfer

  1. Janine Bowring
  2. Maan M Neamah
  3. Jorge Donderis
  4. Ignacio Mir-Sanchis
  5. Christian Alite
  6. J Rafael Ciges-Tomas
  7. Elisa Maiques
  8. Iltyar Medmedov
  9. Alberto Marina
  10. Jose R Penades  Is a corresponding author
  1. Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, United Kingdom
  2. Instituto de Biomedicina de Valencia (IBV-CSIC), Spain
  3. The University of Chicago, United States

Abstract

Targeting conserved and essential processes is a successful strategy to combat enemies. Remarkably, the clinically important Staphylococcus aureus pathogenicity islands (SaPIs) use this tactic to spread in nature. SaPIs reside passively in the host chromosome, under the control of the SaPI-encoded master repressor, Stl. It has been assumed that SaPI de-repression is effected by specific phage proteins that bind to Stl, initiating the SaPI cycle. Different SaPIs encode different Stl repressors, so each targets a specific phage protein for its de-repression. Broadening this narrow vision, we report here that SaPIs ensure their promiscuous transfer by targeting conserved phage mechanisms. This is accomplished because the SaPI Stl repressors have acquired different domains to interact with unrelated proteins, encoded by different phages, but in all cases performing the same conserved function. This elegant strategy allows intra- and inter-generic SaPI transfer, highlighting these elements as one of nature’s most fascinating subcellular parasites.

Article and author information

Author details

  1. Janine Bowring

    Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Maan M Neamah

    Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7068-8416
  3. Jorge Donderis

    Instituto de Biomedicina de Valencia (IBV-CSIC), Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Ignacio Mir-Sanchis

    Department of Biochemistry and Molecular Biology, The University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6536-0045
  5. Christian Alite

    Instituto de Biomedicina de Valencia (IBV-CSIC), Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. J Rafael Ciges-Tomas

    Instituto de Biomedicina de Valencia (IBV-CSIC), Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Elisa Maiques

    Instituto de Biomedicina de Valencia (IBV-CSIC), Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Iltyar Medmedov

    Instituto de Biomedicina de Valencia (IBV-CSIC), Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Alberto Marina

    Instituto de Biomedicina de Valencia (IBV-CSIC), Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1334-5273
  10. Jose R Penades

    Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom
    For correspondence
    joser.penades@glasgow.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6439-5262

Funding

Wellcome (201531/Z/16/Z)

  • Jose R Penades

Biotechnology and Biological Sciences Research Council (BB/N002873/1)

  • Jose R Penades

Medical Research Council (MR/M003876/1)

  • Jose R Penades

Ministerio de Economía y Competitividad (BIO2013-42619-P)

  • Alberto Marina

Ministerio de Economía y Competitividad (BIO2016-78571-P)

  • Alberto Marina

ERC Advanced Grant 2014 (Proposal n{degree sign} 670932 Dut-signal)

  • Jose R Penades

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

Copyright

© 2017, Bowring 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. Janine Bowring
  2. Maan M Neamah
  3. Jorge Donderis
  4. Ignacio Mir-Sanchis
  5. Christian Alite
  6. J Rafael Ciges-Tomas
  7. Elisa Maiques
  8. Iltyar Medmedov
  9. Alberto Marina
  10. Jose R Penades
(2017)
Pirating conserved phage mechanisms promotes promiscuous staphylococcal pathogenicity island transfer
eLife 6:e26487.
https://doi.org/10.7554/eLife.26487

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https://doi.org/10.7554/eLife.26487