Staphylococcal phages and pathogenicity islands drive plasmid evolution

Suzanne Humphrey, Álvaro San Millán, Macarena Toll-Riera, John Connolly, Alejandra Flor-Duro, John Chen, Carles Ubeda, R. Craig MacLean and José R. Penadés ()
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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
R. Craig MacLean: University of Oxford
José R. Penadés: Institute of Infection, Immunity and Inflammation, University of Glasgow

Nature Communications, 2021, vol. 12, issue 1, 1-15

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-26101-5

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