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

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 c...

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Autores principales: Ibarra-Chávez, Rodrigo, Brady, Aisling, Chen, John, Penadés, José R., Haag, Andreas F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8989297/
https://www.ncbi.nlm.nih.gov/pubmed/35344558
http://dx.doi.org/10.1371/journal.pgen.1010146
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author Ibarra-Chávez, Rodrigo
Brady, Aisling
Chen, John
Penadés, José R.
Haag, Andreas F.
author_facet Ibarra-Chávez, Rodrigo
Brady, Aisling
Chen, John
Penadés, José R.
Haag, Andreas F.
author_sort Ibarra-Chávez, Rodrigo
collection PubMed
description 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.
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spelling pubmed-89892972022-04-08 Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis Ibarra-Chávez, Rodrigo Brady, Aisling Chen, John Penadés, José R. Haag, Andreas F. PLoS Genet Research Article 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. Public Library of Science 2022-03-28 /pmc/articles/PMC8989297/ /pubmed/35344558 http://dx.doi.org/10.1371/journal.pgen.1010146 Text en © 2022 Ibarra-Chávez et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ibarra-Chávez, Rodrigo
Brady, Aisling
Chen, John
Penadés, José R.
Haag, Andreas F.
Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
title Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
title_full Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
title_fullStr Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
title_full_unstemmed Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
title_short Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
title_sort phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8989297/
https://www.ncbi.nlm.nih.gov/pubmed/35344558
http://dx.doi.org/10.1371/journal.pgen.1010146
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