The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>

ABSTRACT ParB proteins bind centromere-like DNA sequences called parS sites and are involved in plasmid and chromosome segregation in bacteria. We previously showed that the opportunistic human pathogen Streptococcus pneumoniae contains four parS sequences located close to the origin of replication...

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Autores principales:	Laetitia Attaiech, Anita Minnen, Morten Kjos, Stephan Gruber, Jan-Willem Veening
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a6f556e3b72e4740b30225ede98554ac
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spelling	oai:doaj.org-article:a6f556e3b72e4740b30225ede98554ac2021-11-15T15:41:27ZThe ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>10.1128/mBio.00662-152150-7511https://doaj.org/article/a6f556e3b72e4740b30225ede98554ac2015-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00662-15https://doaj.org/toc/2150-7511ABSTRACT ParB proteins bind centromere-like DNA sequences called parS sites and are involved in plasmid and chromosome segregation in bacteria. We previously showed that the opportunistic human pathogen Streptococcus pneumoniae contains four parS sequences located close to the origin of replication which are bound by ParB. Using chromatin immunoprecipitation (ChIP), we found here that ParB spreads out from one of these parS sites, parS(−1.6°), for more than 5 kb and occupies the nearby comCDE operon, which drives competence development. Competence allows S. pneumoniae to take up DNA from its environment, thereby mediating horizontal gene transfer, and is also employed as a general stress response. Mutating parS(−1.6°) or deleting parB resulted in transcriptional up-regulation of comCDE and ssbB (a gene belonging to the competence regulon), demonstrating that ParB acts as a repressor of competence. However, genome-wide transcription analysis showed that ParB is not a global transcriptional regulator. Different factors, such as the composition of the growth medium and antibiotic-induced stress, can trigger the sensitive switch driving competence. This work shows that the ParB-parS chromosome segregation machinery also influences this developmental process. IMPORTANCE Streptococcus pneumoniae (pneumococcus) is an important human pathogen responsible for more than a million deaths each year. Like all other organisms, S. pneumoniae must be able to segregate its chromosomes properly. Not only is understanding the molecular mechanisms underlying chromosome segregation in S. pneumoniae therefore of fundamental importance, but also, this knowledge might offer new leads for ways to target this pathogen. Here, we identified a link between the pneumococcal chromosome segregation system and the competence-developmental system. Competence allows S. pneumoniae to take up and integrate exogenous DNA in its chromosome. This process plays a crucial role in successful adaptation to—and escape from—host defenses, antibiotic treatments, and vaccination strategies. We show that the chromosome segregation protein ParB acts as a repressor of competence. To the best of our knowledge, this is the first example of a ParB protein controlling bacterial competence.Laetitia AttaiechAnita MinnenMorten KjosStephan GruberJan-Willem VeeningAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 4 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Laetitia Attaiech Anita Minnen Morten Kjos Stephan Gruber Jan-Willem Veening The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>
description	ABSTRACT ParB proteins bind centromere-like DNA sequences called parS sites and are involved in plasmid and chromosome segregation in bacteria. We previously showed that the opportunistic human pathogen Streptococcus pneumoniae contains four parS sequences located close to the origin of replication which are bound by ParB. Using chromatin immunoprecipitation (ChIP), we found here that ParB spreads out from one of these parS sites, parS(−1.6°), for more than 5 kb and occupies the nearby comCDE operon, which drives competence development. Competence allows S. pneumoniae to take up DNA from its environment, thereby mediating horizontal gene transfer, and is also employed as a general stress response. Mutating parS(−1.6°) or deleting parB resulted in transcriptional up-regulation of comCDE and ssbB (a gene belonging to the competence regulon), demonstrating that ParB acts as a repressor of competence. However, genome-wide transcription analysis showed that ParB is not a global transcriptional regulator. Different factors, such as the composition of the growth medium and antibiotic-induced stress, can trigger the sensitive switch driving competence. This work shows that the ParB-parS chromosome segregation machinery also influences this developmental process. IMPORTANCE Streptococcus pneumoniae (pneumococcus) is an important human pathogen responsible for more than a million deaths each year. Like all other organisms, S. pneumoniae must be able to segregate its chromosomes properly. Not only is understanding the molecular mechanisms underlying chromosome segregation in S. pneumoniae therefore of fundamental importance, but also, this knowledge might offer new leads for ways to target this pathogen. Here, we identified a link between the pneumococcal chromosome segregation system and the competence-developmental system. Competence allows S. pneumoniae to take up and integrate exogenous DNA in its chromosome. This process plays a crucial role in successful adaptation to—and escape from—host defenses, antibiotic treatments, and vaccination strategies. We show that the chromosome segregation protein ParB acts as a repressor of competence. To the best of our knowledge, this is the first example of a ParB protein controlling bacterial competence.
format	article
author	Laetitia Attaiech Anita Minnen Morten Kjos Stephan Gruber Jan-Willem Veening
author_facet	Laetitia Attaiech Anita Minnen Morten Kjos Stephan Gruber Jan-Willem Veening
author_sort	Laetitia Attaiech
title	The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>
title_short	The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>
title_full	The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>
title_fullStr	The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>
title_full_unstemmed	The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>
title_sort	parb-<italic toggle="yes">pars</italic> chromosome segregation system modulates competence development in <named-content content-type="genus-species">streptococcus pneumoniae</named-content>
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/a6f556e3b72e4740b30225ede98554ac
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The ParB-<italic toggle="yes">parS</italic> Chromosome Segregation System Modulates Competence Development in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>

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