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...
Main Authors: | , , , , |
---|---|
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 |
_version_ | 1797984275964887040 |
---|---|
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. |
first_indexed | 2024-04-11T07:00:12Z |
format | Article |
id | doaj.art-8d0c2b5c5faf46e3b6293110c09daf3e |
institution | Directory Open Access Journal |
issn | 1544-9173 1545-7885 |
language | English |
last_indexed | 2024-04-11T07:00:12Z |
publishDate | 2022-11-01 |
publisher | Public Library of Science (PLoS) |
record_format | Article |
series | PLoS Biology |
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 |
work_keys_str_mv | AT kevingozzi prophagelikegenetransferagentspromotecaulobactercrescentussurvivalanddnarepairduringstationaryphase AT ngatttran prophagelikegenetransferagentspromotecaulobactercrescentussurvivalanddnarepairduringstationaryphase AT joshuawmodell prophagelikegenetransferagentspromotecaulobactercrescentussurvivalanddnarepairduringstationaryphase AT tungbkle prophagelikegenetransferagentspromotecaulobactercrescentussurvivalanddnarepairduringstationaryphase AT michaeltlaub prophagelikegenetransferagentspromotecaulobactercrescentussurvivalanddnarepairduringstationaryphase |