Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis

Ibarra-Chávez, R., Brady, A., Chen, J., Penadés, J. R. and Haag, A. F. (2022) Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis. PLoS Genetics, 18(3), e1010146. (doi: 10.1371/journal.pgen.1010146) (PMID:35344558) (PMCID:PMC8989297)

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Abstract

Phage-inducible chromosomal islands (PICIs) are a widespread family of highly mobile genetic elements that disseminate virulence and toxin genes among bacterial populations. Since their life cycle involves induction by helper phages, they are important players in phage evolution and ecology. PICIs can interfere with the lifecycle of their helper phages at different stages resulting frequently in reduced phage production after infection of a PICI-containing strain. Since phage defense systems have been recently shown to be beneficial for the acquisition of exogenous DNA via horizontal gene transfer, we hypothesized that PICIs could provide a similar benefit to their hosts and tested the impact of PICIs in recipient strains on host cell viability, phage propagation and transfer of genetic material. Here we report an important role for PICIs in bacterial evolution by promoting the survival of phage-mediated transductants of chromosomal or plasmid DNA. The presence of PICIs generates favorable conditions for population diversification and the inheritance of genetic material being transferred, such as antibiotic resistance and virulence genes. Our results show that by interfering with phage reproduction, PICIs can protect the bacterial population from phage attack, increasing the overall survival of the bacterial population as well as the transduced cells. Moreover, our results also demonstrate that PICIs reduce the frequency of lysogenization after temperate phage infection, creating a more genetically diverse bacterial population with increased bet-hedging opportunities to adapt to new niches. In summary, our results identify a new role for the PICIs and highlight them as important drivers of bacterial evolution.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Penades, Prof Jose R and Ibarra Chavez, Mr Rodrigo and Brady, Aisling and Haag, Dr Andreas
Creator Roles:
Ibarra-Chávez, R.Formal analysis, Investigation, Writing – original draft, Writing – review and editing
Brady, A.Formal analysis, Investigation
Penadés, J. R.Conceptualization, Formal analysis, Funding acquisition, Writing – original draft, Writing – review and editing
Haag, A. F.Conceptualization, Formal analysis, Investigation, Writing – original draft, Writing – review and editing
Authors: Ibarra-Chávez, R., Brady, A., Chen, J., Penadés, J. R., and Haag, A. F.
College/School:College of Medical Veterinary and Life Sciences > School of Infection & Immunity
Journal Name:PLoS Genetics
Publisher:Public Library of Science
ISSN:1553-7390
ISSN (Online):1553-7404
Published Online:28 March 2022
Copyright Holders:Copyright © 2022 Ibarra-Chávez et al.
First Published:First published in PLoS Genetics 18(3): e1010146
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
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