Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators

ABSTRACT Bacterial ParA and ParB proteins are best known for their contribution to plasmid and chromosome segregation, but they may also contribute to other cell functions. In segregation, ParA interacts with ParB, which binds to parS centromere-analogous sites. In transcription, plasmid Par protein...

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Autores principales:	Jong Hwan Baek, Seesandra V. Rajagopala, Dhruba K. Chattoraj
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ae984da185684dd28a663ca0a5f7f080
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spelling	oai:doaj.org-article:ae984da185684dd28a663ca0a5f7f0802021-11-15T15:47:38ZChromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators10.1128/mBio.01061-142150-7511https://doaj.org/article/ae984da185684dd28a663ca0a5f7f0802014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01061-14https://doaj.org/toc/2150-7511ABSTRACT Bacterial ParA and ParB proteins are best known for their contribution to plasmid and chromosome segregation, but they may also contribute to other cell functions. In segregation, ParA interacts with ParB, which binds to parS centromere-analogous sites. In transcription, plasmid Par proteins can serve as repressors by specifically binding to their own promoters and, additionally, in the case of ParB, by spreading from a parS site to nearby promoters. Here, we have asked whether chromosomal Par proteins can likewise control transcription. Analysis of genome-wide ParB1 binding in Vibrio cholerae revealed preferential binding to the three known parS1 sites and limited spreading of ParB1 beyond the parS1 sites. Comparison of wild-type transcriptomes with those of ΔparA1, ΔparB1, and ΔparAB1 mutants revealed that two out of 20 genes (VC0067 and VC0069) covered by ParB1 spreading are repressed by both ParB1 and ParA1. A third gene (VC0076) at the outskirts of the spreading area and a few genes further away were also repressed, particularly the gene for an outer membrane protein, ompU (VC0633). Since ParA1 or ParB1 binding was not evident near VC0076 and ompU genes, the repression may require participation of additional factors. Indeed, both ParA1 and ParB1 proteins were found to interact with several V. cholerae proteins in bacterial and yeast two-hybrid screens. These studies demonstrate that chromosomal Par proteins can repress genes unlinked to parS and can do so without direct binding to the cognate promoter DNA. IMPORTANCE Directed segregation of chromosomes is essential for their maintenance in dividing cells. Many bacteria have genes (par) that were thought to be dedicated to segregation based on analogy to their roles in plasmid maintenance. It is becoming clear that chromosomal par genes are pleiotropic and that they contribute to diverse processes such as DNA replication, cell division, cell growth, and motility. One way to explain the pleiotropy is to suggest that Par proteins serve as or control other transcription factors. We tested this model by determining how Par proteins affect genome-wide transcription activity. We found that genes implicated in drug resistance, stress response, and pathogenesis were repressed by Par. Unexpectedly, the repression did not involve direct Par binding to cognate promoter DNA, indicating that the repression may involve Par interactions with other regulators. This pleiotropy highlights the degree of integration of chromosomal Par proteins into cellular control circuitries.Jong Hwan BaekSeesandra V. RajagopalaDhruba K. ChattorajAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Jong Hwan Baek Seesandra V. Rajagopala Dhruba K. Chattoraj Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators
description	ABSTRACT Bacterial ParA and ParB proteins are best known for their contribution to plasmid and chromosome segregation, but they may also contribute to other cell functions. In segregation, ParA interacts with ParB, which binds to parS centromere-analogous sites. In transcription, plasmid Par proteins can serve as repressors by specifically binding to their own promoters and, additionally, in the case of ParB, by spreading from a parS site to nearby promoters. Here, we have asked whether chromosomal Par proteins can likewise control transcription. Analysis of genome-wide ParB1 binding in Vibrio cholerae revealed preferential binding to the three known parS1 sites and limited spreading of ParB1 beyond the parS1 sites. Comparison of wild-type transcriptomes with those of ΔparA1, ΔparB1, and ΔparAB1 mutants revealed that two out of 20 genes (VC0067 and VC0069) covered by ParB1 spreading are repressed by both ParB1 and ParA1. A third gene (VC0076) at the outskirts of the spreading area and a few genes further away were also repressed, particularly the gene for an outer membrane protein, ompU (VC0633). Since ParA1 or ParB1 binding was not evident near VC0076 and ompU genes, the repression may require participation of additional factors. Indeed, both ParA1 and ParB1 proteins were found to interact with several V. cholerae proteins in bacterial and yeast two-hybrid screens. These studies demonstrate that chromosomal Par proteins can repress genes unlinked to parS and can do so without direct binding to the cognate promoter DNA. IMPORTANCE Directed segregation of chromosomes is essential for their maintenance in dividing cells. Many bacteria have genes (par) that were thought to be dedicated to segregation based on analogy to their roles in plasmid maintenance. It is becoming clear that chromosomal par genes are pleiotropic and that they contribute to diverse processes such as DNA replication, cell division, cell growth, and motility. One way to explain the pleiotropy is to suggest that Par proteins serve as or control other transcription factors. We tested this model by determining how Par proteins affect genome-wide transcription activity. We found that genes implicated in drug resistance, stress response, and pathogenesis were repressed by Par. Unexpectedly, the repression did not involve direct Par binding to cognate promoter DNA, indicating that the repression may involve Par interactions with other regulators. This pleiotropy highlights the degree of integration of chromosomal Par proteins into cellular control circuitries.
format	article
author	Jong Hwan Baek Seesandra V. Rajagopala Dhruba K. Chattoraj
author_facet	Jong Hwan Baek Seesandra V. Rajagopala Dhruba K. Chattoraj
author_sort	Jong Hwan Baek
title	Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators
title_short	Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators
title_full	Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators
title_fullStr	Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators
title_full_unstemmed	Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators
title_sort	chromosome segregation proteins of <named-content content-type="genus-species">vibrio cholerae</named-content> as transcription regulators
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/ae984da185684dd28a663ca0a5f7f080
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Chromosome Segregation Proteins of <named-content content-type="genus-species">Vibrio cholerae</named-content> as Transcription Regulators

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