Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase

<jats:p>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 h...

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Main Authors: Gozzi, Kevin, Tran, Ngat T, Modell, Joshua W, Le, Tung BK, Laub, Michael T
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022
Online Access:https://hdl.handle.net/1721.1/146543
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author Gozzi, Kevin
Tran, Ngat T
Modell, Joshua W
Le, Tung BK
Laub, Michael T
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Gozzi, Kevin
Tran, Ngat T
Modell, Joshua W
Le, Tung BK
Laub, Michael T
author_sort Gozzi, Kevin
collection MIT
description <jats:p>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 <jats:italic>Caulobacter crescentus</jats:italic> produces bona fide GTAs. The production of <jats:italic>Caulobacter</jats:italic> GTAs is tightly regulated by a newly identified transcription factor, RogA, that represses <jats:italic>gafYZ</jats:italic>, the direct activators of GTA synthesis. Cells lacking <jats:italic>rogA</jats:italic> or expressing <jats:italic>gafYZ</jats:italic> 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 <jats:italic>Caulobacter</jats:italic> 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.</jats:p>
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spelling mit-1721.1/1465432022-11-19T03:09:41Z 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 BK Laub, Michael T Massachusetts Institute of Technology. Department of Biology <jats:p>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 <jats:italic>Caulobacter crescentus</jats:italic> produces bona fide GTAs. The production of <jats:italic>Caulobacter</jats:italic> GTAs is tightly regulated by a newly identified transcription factor, RogA, that represses <jats:italic>gafYZ</jats:italic>, the direct activators of GTA synthesis. Cells lacking <jats:italic>rogA</jats:italic> or expressing <jats:italic>gafYZ</jats:italic> 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 <jats:italic>Caulobacter</jats:italic> 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.</jats:p> 2022-11-18T18:12:53Z 2022-11-18T18:12:53Z 2022-11 2022-11-18T18:05:57Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/146543 Gozzi, Kevin, Tran, Ngat T, Modell, Joshua W, Le, Tung BK and Laub, Michael T. 2022. "Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase." PLOS Biology, 20 (11). en 10.1371/journal.pbio.3001790 PLOS Biology Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Public Library of Science (PLoS) PLoS
spellingShingle Gozzi, Kevin
Tran, Ngat T
Modell, Joshua W
Le, Tung BK
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
url https://hdl.handle.net/1721.1/146543
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