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Staphylococcal phages and pathogenicity islands drive plasmid evolution

Author

Listed:
  • Suzanne Humphrey

    (Institute of Infection, Immunity and Inflammation, University of Glasgow)

  • Álvaro San Millán

    (Centro Nacional de Biotecnología–CSIC)

  • Macarena Toll-Riera

    (Institute of Integrative Biology, ETH Zurich)

  • John Connolly

    (Institute of Infection, Immunity and Inflammation, University of Glasgow)

  • Alejandra Flor-Duro

    (Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana-FISABIO)

  • John Chen

    (Department of Microbiology and Immunology, Yong Loo Lin School of Medicine, National University of Singapore)

  • Carles Ubeda

    (Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana-FISABIO
    Centers of Biomedical Research Network (CIBER) in Epidemiology and Public Health)

  • R. Craig MacLean

    (University of Oxford)

  • José R. Penadés

    (Institute of Infection, Immunity and Inflammation, University of Glasgow
    Departamento de Ciencias Biomédicas, Facultad de Ciencias de la Salud, Universidad CEU Cardenal Herrera
    MRC Centre for Molecular Bacteriology and Infection, Imperial College London)

Abstract

Conjugation has classically been considered the main mechanism driving plasmid transfer in nature. Yet bacteria frequently carry so-called non-transmissible plasmids, raising questions about how these plasmids spread. Interestingly, the size of many mobilisable and non-transmissible plasmids coincides with the average size of phages (~40 kb) or that of a family of pathogenicity islands, the phage-inducible chromosomal islands (PICIs, ~11 kb). Here, we show that phages and PICIs from Staphylococcus aureus can mediate intra- and inter-species plasmid transfer via generalised transduction, potentially contributing to non-transmissible plasmid spread in nature. Further, staphylococcal PICIs enhance plasmid packaging efficiency, and phages and PICIs exert selective pressures on plasmids via the physical capacity of their capsids, explaining the bimodal size distribution observed for non-conjugative plasmids. Our results highlight that transducing agents (phages, PICIs) have important roles in bacterial plasmid evolution and, potentially, in antimicrobial resistance transmission.

Suggested Citation

  • Suzanne Humphrey & Álvaro San Millán & Macarena Toll-Riera & John Connolly & Alejandra Flor-Duro & John Chen & Carles Ubeda & R. Craig MacLean & José R. Penadés, 2021. "Staphylococcal phages and pathogenicity islands drive plasmid evolution," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26101-5
    DOI: 10.1038/s41467-021-26101-5
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    References listed on IDEAS

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    1. Sheetal R. Modi & Henry H. Lee & Catherine S. Spina & James J. Collins, 2013. "Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome," Nature, Nature, vol. 499(7457), pages 219-222, July.
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    Cited by:

    1. Alvah Zorea & David Pellow & Liron Levin & Shai Pilosof & Jonathan Friedman & Ron Shamir & Itzhak Mizrahi, 2024. "Plasmids in the human gut reveal neutral dispersal and recombination that is overpowered by inflammatory diseases," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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