PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria

ABSTRACT PprA, a radiation-induced Deinococcus-specific protein, was previously shown to be required for cell survival and accurate chromosome segregation after exposure to ionizing radiation. Here, we used an in vivo approach to determine, by shotgun proteomics, putative PprA partners coimmunopreci...

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Autores principales:	Alice Devigne, Philippe Guérin, Johnny Lisboa, Sophie Quevillon-Cheruel, Jean Armengaud, Suzanne Sommer, Claire Bouthier de la Tour, Pascale Servant
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Deinococcus radiodurans PprA DNA gyrase DNA decatenation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b6efba7c41834047ad4acc86701fc45f
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spelling	oai:doaj.org-article:b6efba7c41834047ad4acc86701fc45f2021-11-15T15:21:38ZPprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria10.1128/mSphere.00036-152379-5042https://doaj.org/article/b6efba7c41834047ad4acc86701fc45f2016-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00036-15https://doaj.org/toc/2379-5042ABSTRACT PprA, a radiation-induced Deinococcus-specific protein, was previously shown to be required for cell survival and accurate chromosome segregation after exposure to ionizing radiation. Here, we used an in vivo approach to determine, by shotgun proteomics, putative PprA partners coimmunoprecipitating with PprA when cells were exposed to gamma rays. Among them, we found the two subunits of DNA gyrase and, thus, chose to focus our work on characterizing the activities of the deinococcal DNA gyrase in the presence or absence of PprA. Loss of PprA rendered cells hypersensitive to novobiocin, an inhibitor of the B subunit of DNA gyrase. We showed that treatment of bacteria with novobiocin resulted in induction of the radiation desiccation response (RDR) regulon and in defects in chromosome segregation that were aggravated by the absence of PprA. In vitro, the deinococcal DNA gyrase, like other bacterial DNA gyrases, possesses DNA negative supercoiling and decatenation activities. These two activities are inhibited in vitro by novobiocin and nalidixic acid, whereas PprA specifically stimulates the decatenation activity of DNA gyrase. Together, these results suggest that PprA plays a major role in chromosome decatenation via its interaction with the deinococcal DNA gyrase when D. radiodurans cells are recovering from exposure to ionizing radiation. IMPORTANCE D. radiodurans is one of the most radiation-resistant organisms known. This bacterium is able to cope with high levels of DNA lesions generated by exposure to extreme doses of ionizing radiation and to reconstruct a functional genome from hundreds of radiation-induced chromosomal fragments. Here, we identified partners of PprA, a radiation-induced Deinococcus-specific protein, previously shown to be required for radioresistance. Our study leads to three main findings: (i) PprA interacts with DNA gyrase after irradiation, (ii) treatment of cells with novobiocin results in defects in chromosome segregation that are aggravated by the absence of PprA, and (iii) PprA stimulates the decatenation activity of DNA gyrase. Our results extend the knowledge of how D. radiodurans cells survive exposure to extreme doses of gamma irradiation and point out the link between DNA repair, chromosome segregation, and DNA gyrase activities in the radioresistant D. radiodurans bacterium.Alice DevignePhilippe GuérinJohnny LisboaSophie Quevillon-CheruelJean ArmengaudSuzanne SommerClaire Bouthier de la TourPascale ServantAmerican Society for MicrobiologyarticleDeinococcus radioduransPprADNA gyraseDNA decatenationMicrobiologyQR1-502ENmSphere, Vol 1, Iss 1 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Deinococcus radiodurans PprA DNA gyrase DNA decatenation Microbiology QR1-502
spellingShingle	Deinococcus radiodurans PprA DNA gyrase DNA decatenation Microbiology QR1-502 Alice Devigne Philippe Guérin Johnny Lisboa Sophie Quevillon-Cheruel Jean Armengaud Suzanne Sommer Claire Bouthier de la Tour Pascale Servant PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria
description	ABSTRACT PprA, a radiation-induced Deinococcus-specific protein, was previously shown to be required for cell survival and accurate chromosome segregation after exposure to ionizing radiation. Here, we used an in vivo approach to determine, by shotgun proteomics, putative PprA partners coimmunoprecipitating with PprA when cells were exposed to gamma rays. Among them, we found the two subunits of DNA gyrase and, thus, chose to focus our work on characterizing the activities of the deinococcal DNA gyrase in the presence or absence of PprA. Loss of PprA rendered cells hypersensitive to novobiocin, an inhibitor of the B subunit of DNA gyrase. We showed that treatment of bacteria with novobiocin resulted in induction of the radiation desiccation response (RDR) regulon and in defects in chromosome segregation that were aggravated by the absence of PprA. In vitro, the deinococcal DNA gyrase, like other bacterial DNA gyrases, possesses DNA negative supercoiling and decatenation activities. These two activities are inhibited in vitro by novobiocin and nalidixic acid, whereas PprA specifically stimulates the decatenation activity of DNA gyrase. Together, these results suggest that PprA plays a major role in chromosome decatenation via its interaction with the deinococcal DNA gyrase when D. radiodurans cells are recovering from exposure to ionizing radiation. IMPORTANCE D. radiodurans is one of the most radiation-resistant organisms known. This bacterium is able to cope with high levels of DNA lesions generated by exposure to extreme doses of ionizing radiation and to reconstruct a functional genome from hundreds of radiation-induced chromosomal fragments. Here, we identified partners of PprA, a radiation-induced Deinococcus-specific protein, previously shown to be required for radioresistance. Our study leads to three main findings: (i) PprA interacts with DNA gyrase after irradiation, (ii) treatment of cells with novobiocin results in defects in chromosome segregation that are aggravated by the absence of PprA, and (iii) PprA stimulates the decatenation activity of DNA gyrase. Our results extend the knowledge of how D. radiodurans cells survive exposure to extreme doses of gamma irradiation and point out the link between DNA repair, chromosome segregation, and DNA gyrase activities in the radioresistant D. radiodurans bacterium.
format	article
author	Alice Devigne Philippe Guérin Johnny Lisboa Sophie Quevillon-Cheruel Jean Armengaud Suzanne Sommer Claire Bouthier de la Tour Pascale Servant
author_facet	Alice Devigne Philippe Guérin Johnny Lisboa Sophie Quevillon-Cheruel Jean Armengaud Suzanne Sommer Claire Bouthier de la Tour Pascale Servant
author_sort	Alice Devigne
title	PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria
title_short	PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria
title_full	PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria
title_fullStr	PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria
title_full_unstemmed	PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria
title_sort	ppra protein is involved in chromosome segregation via its physical and functional interaction with dna gyrase in irradiated <named-content content-type="genus-species">deinococcus radiodurans</named-content> bacteria
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/b6efba7c41834047ad4acc86701fc45f
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PprA Protein Is Involved in Chromosome Segregation via Its Physical and Functional Interaction with DNA Gyrase in Irradiated <named-content content-type="genus-species">Deinococcus radiodurans</named-content> Bacteria

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