Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
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Published version
OA Location
Author(s)
Ibarra-Chávez, Rodrigo
Brady, Aisling
Chen, John
Penadés, José R
Haag, Andreas F
Type
Journal Article
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.
Date Issued
2022-03-28
Date Acceptance
2022-03-14
Citation
PLoS Genetics, 2022, 18 (3)
ISSN
1553-7390
Publisher
Public Library of Science (PLoS)
Journal / Book Title
PLoS Genetics
Volume
18
Issue
3
Copyright Statement
© 2022 Ibarra-Chávez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
License URL
Sponsor
Biotechnology and Biological Sciences Research Council (BBSRC)
Medical Research Council (MRC)
Medical Research Council (MRC)
Biotechnology and Biological Sciences Research Cou
Identifier
https://www.ncbi.nlm.nih.gov/pubmed/35344558
PII: PGENETICS-D-21-00720
Grant Number
BB/V002376/1
MR/V000772/1
MR/S00940X/2
BB/V009583/1
Subjects
Developmental Biology
0604 Genetics
Publication Status
Published
Coverage Spatial
United States
Article Number
ARTN e1010146