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Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase
Gene transfer agents (GTAs) are prophage-like entities found in many bacterial genomes that cannot propagate themselves and instead package approximately 5 to 15 kbp fragments of the host genome that can then be transferred to related recipient cells. Although suggested to facilitate horizontal gene...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9632790/ https://www.ncbi.nlm.nih.gov/pubmed/36327213 http://dx.doi.org/10.1371/journal.pbio.3001790 |
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author | Gozzi, Kevin Tran, Ngat T. Modell, Joshua W. Le, Tung B. K. Laub, Michael T. |
author_facet | Gozzi, Kevin Tran, Ngat T. Modell, Joshua W. Le, Tung B. K. Laub, Michael T. |
author_sort | Gozzi, Kevin |
collection | PubMed |
description | Gene transfer agents (GTAs) are prophage-like entities found in many bacterial genomes that cannot propagate themselves and instead package approximately 5 to 15 kbp fragments of the host genome that can then be transferred to related recipient cells. Although suggested to facilitate horizontal gene transfer (HGT) in the wild, no clear physiological role for GTAs has been elucidated. Here, we demonstrate that the α-proteobacterium Caulobacter crescentus produces bona fide GTAs. The production of Caulobacter GTAs is tightly regulated by a newly identified transcription factor, RogA, that represses gafYZ, the direct activators of GTA synthesis. Cells lacking rogA or expressing gafYZ produce GTAs harboring approximately 8.3 kbp fragment of the genome that can, after cell lysis, be transferred into recipient cells. Notably, we find that GTAs promote the survival of Caulobacter in stationary phase and following DNA damage by providing recipient cells a template for homologous recombination-based repair. This function may be broadly conserved in other GTA-producing organisms and explain the prevalence of this unusual HGT mechanism. |
format | Online Article Text |
id | pubmed-9632790 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-96327902022-11-04 Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase Gozzi, Kevin Tran, Ngat T. Modell, Joshua W. Le, Tung B. K. Laub, Michael T. PLoS Biol Research Article Gene transfer agents (GTAs) are prophage-like entities found in many bacterial genomes that cannot propagate themselves and instead package approximately 5 to 15 kbp fragments of the host genome that can then be transferred to related recipient cells. Although suggested to facilitate horizontal gene transfer (HGT) in the wild, no clear physiological role for GTAs has been elucidated. Here, we demonstrate that the α-proteobacterium Caulobacter crescentus produces bona fide GTAs. The production of Caulobacter GTAs is tightly regulated by a newly identified transcription factor, RogA, that represses gafYZ, the direct activators of GTA synthesis. Cells lacking rogA or expressing gafYZ produce GTAs harboring approximately 8.3 kbp fragment of the genome that can, after cell lysis, be transferred into recipient cells. Notably, we find that GTAs promote the survival of Caulobacter in stationary phase and following DNA damage by providing recipient cells a template for homologous recombination-based repair. This function may be broadly conserved in other GTA-producing organisms and explain the prevalence of this unusual HGT mechanism. Public Library of Science 2022-11-03 /pmc/articles/PMC9632790/ /pubmed/36327213 http://dx.doi.org/10.1371/journal.pbio.3001790 Text en © 2022 Gozzi 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 Gozzi, Kevin Tran, Ngat T. Modell, Joshua W. Le, Tung B. K. Laub, Michael T. Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase |
title | Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase |
title_full | Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase |
title_fullStr | Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase |
title_full_unstemmed | Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase |
title_short | Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase |
title_sort | prophage-like gene transfer agents promote caulobacter crescentus survival and dna repair during stationary phase |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9632790/ https://www.ncbi.nlm.nih.gov/pubmed/36327213 http://dx.doi.org/10.1371/journal.pbio.3001790 |
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