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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Main Authors: Kevin Gozzi, Ngat T Tran, Joshua W Modell, Tung B K Le, Michael T Laub
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-11-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3001790
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author Kevin Gozzi
Ngat T Tran
Joshua W Modell
Tung B K Le
Michael T Laub
author_facet Kevin Gozzi
Ngat T Tran
Joshua W Modell
Tung B K Le
Michael T Laub
author_sort Kevin Gozzi
collection DOAJ
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 doaj.art-8d0c2b5c5faf46e3b6293110c09daf3e2022-12-22T04:38:51ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-11-012011e300179010.1371/journal.pbio.3001790Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase.Kevin GozziNgat T TranJoshua W ModellTung B K LeMichael T LaubGene 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.https://doi.org/10.1371/journal.pbio.3001790
spellingShingle Kevin Gozzi
Ngat T Tran
Joshua W Modell
Tung B K Le
Michael T Laub
Prophage-like gene transfer agents promote Caulobacter crescentus survival and DNA repair during stationary phase.
PLoS Biology
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://doi.org/10.1371/journal.pbio.3001790
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