Staphylococcal phages and pathogenicity islands drive plasmid evolution

Humphrey, S., San Millán, Á., Toll-Riera, M., Connolly, J., Flor-Duro, A., Chen, J., Ubeda, C., MacLean, R. C. and Penadés, J. R. (2021) Staphylococcal phages and pathogenicity islands drive plasmid evolution. Nature Communications, 12, 5845. (doi: 10.1038/s41467-021-26101-5) (PMID:34615859) (PMCID:PMC8494744)

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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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Penades, Prof Jose R and Humphrey, Dr Suzie and Connolly, Mr John
Authors: Humphrey, S., San Millán, Á., Toll-Riera, M., Connolly, J., Flor-Duro, A., Chen, J., Ubeda, C., MacLean, R. C., and Penadés, J. R.
College/School:College of Medical Veterinary and Life Sciences > Institute of Infection Immunity and Inflammation
Journal Name:Nature Communications
Publisher:Nature Research
ISSN:2041-1723
ISSN (Online):2041-1723
Copyright Holders:Copyright © 2021 The Authors
First Published:First published in Nature Communications 12: 5845
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
170721Molecular biology of the PICIs, a novel and widespread family of mobile genetic elements involved in bacterial virulenceJose R PenadesMedical Research Council (MRC)MR/M003876/1III - Bacteriology - Dr J Penades
304055Deciphering Gram-negative phage-inducible chromosomal island strategies for spreading in natureJose R PenadesMedical Research Council (MRC)MRS00940X/1III - Bacteriology
172242Understanding a novel mechanim involving pathogenity islands in the transfer of unlinked chromosomal virulence genesJose R PenadesBiotechnology and Biological Sciences Research Council (BBSRC)BB/N002873/1Institute of Infection, Immunity & Inflammation
302971Helper and satellite pathogenicity islands: the discovery of two novel subcellular elements with a huge impact on bacterial pathogenesis and evolutionJose R PenadesBiotechnology and Biological Sciences Research Council (BBSRC)BB/S003835/1III - Bacteriology
172321DUT-SignalJose R PenadesEuropean Research Council (ERC)670932Institute of Infection, Immunity & Inflammation
173671Prof. R. Fitzgerald. Wellcome Trust Award 201531/Z/16/Z - Understanding bacterial host adaptation to combat infectious diseasesJose R PenadesWellcome Trust (WELLCOTR)R44516 - WT 201531/Z/16/ZInstitute of Infection, Immunity & Inflammation