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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...

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Autores principales: Gozzi, Kevin, Tran, Ngat T., Modell, Joshua W., Le, Tung B. K., Laub, Michael T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
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.
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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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