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)

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 Connolly, Mr John and Humphrey, Dr Suzie
• 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 > School of Infection & Immunity
• 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

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
170721		Molecular biology of the PICIs, a novel and widespread family of mobile genetic elements involved in bacterial virulence	Jose R Penades	Medical Research Council (MRC)	MR/M003876/1	III - Bacteriology - Dr J Penades
304055		Deciphering Gram-negative phage-inducible chromosomal island strategies for spreading in nature	Jose R Penades	Medical Research Council (MRC)	MRS00940X/1	III - Bacteriology
172242		Understanding a novel mechanim involving pathogenity islands in the transfer of unlinked chromosomal virulence genes	Jose R Penades	Biotechnology and Biological Sciences Research Council (BBSRC)	BB/N002873/1	Institute of Infection, Immunity & Inflammation
302971		Helper and satellite pathogenicity islands: the discovery of two novel subcellular elements with a huge impact on bacterial pathogenesis and evolution	Jose R Penades	Biotechnology and Biological Sciences Research Council (BBSRC)	BB/S003835/1	III - Bacteriology
172321		DUT-Signal	Jose R Penades	European Research Council (ERC)	670932	Institute of Infection, Immunity & Inflammation
173671		Prof. R. Fitzgerald. Wellcome Trust Award 201531/Z/16/Z - Understanding bacterial host adaptation to combat infectious diseases	Jose R Penades	Wellcome Trust (WELLCOTR)	R44516 - WT 201531/Z/16/Z	Institute of Infection, Immunity & Inflammation