Identification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>

ABSTRACT Vibrio cholerae is naturally competent when grown on chitin. It is known that expression of the major regulator of competence, TfoX, is controlled by chitin; however, the molecular mechanisms underlying this requirement for chitin have remained unclear. In the present study, we identify and...

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Autores principales: Ankur B. Dalia, David W. Lazinski, Andrew Camilli
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:d8f2e0800583445f93cff91b975832f72021-11-15T15:45:11ZIdentification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>10.1128/mBio.01028-132150-7511https://doaj.org/article/d8f2e0800583445f93cff91b975832f72014-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01028-13https://doaj.org/toc/2150-7511ABSTRACT Vibrio cholerae is naturally competent when grown on chitin. It is known that expression of the major regulator of competence, TfoX, is controlled by chitin; however, the molecular mechanisms underlying this requirement for chitin have remained unclear. In the present study, we identify and characterize a membrane-bound transcriptional regulator that positively regulates the small RNA (sRNA) TfoR, which posttranscriptionally enhances tfoX translation. We show that this regulation of the tfoR promoter is direct by performing electrophoretic mobility shift assays and by heterologous expression of this system in Escherichia coli. This transcriptional regulator was recently identified independently and was named “TfoS” (S. Yamamoto et al., Mol. Microbiol., in press, doi:10.1111/mmi.12462). Using a constitutively active form of TfoS, we demonstrate that the activity of this regulator is sufficient to promote competence in V. cholerae in the absence of chitin. Also, TfoS contains a large periplasmic domain, which we hypothesized interacts with chitin to regulate TfoS activity. In the heterologous host E. coli, we demonstrate that chitin oligosaccharides are sufficient to activate TfoS activity at the tfoR promoter. Collectively, these data characterize TfoS as a novel chitin-sensing transcriptional regulator that represents the direct link between chitin and natural competence in V. cholerae. IMPORTANCE Naturally competent bacteria can take up exogenous DNA from the environment and integrate it into their genome by homologous recombination. This ability to take up exogenous DNA is shared by diverse bacterial species and serves as a mechanism to acquire new genes to enhance the fitness of the organism. Several members of the family Vibrionaceae become naturally competent when grown on chitin; however, a molecular understanding of how chitin activates competence is lacking. Here, we identify a novel membrane-bound transcriptional regulator that is required for natural transformation in the human pathogen Vibrio cholerae. We demonstrate that this regulator senses chitin oligosaccharides to activate the competence cascade, thus, uncovering the molecular link between chitin and natural competence in this Vibrio species.Ankur B. DaliaDavid W. LazinskiAndrew CamilliAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 1 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Ankur B. Dalia
David W. Lazinski
Andrew Camilli
Identification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>
description ABSTRACT Vibrio cholerae is naturally competent when grown on chitin. It is known that expression of the major regulator of competence, TfoX, is controlled by chitin; however, the molecular mechanisms underlying this requirement for chitin have remained unclear. In the present study, we identify and characterize a membrane-bound transcriptional regulator that positively regulates the small RNA (sRNA) TfoR, which posttranscriptionally enhances tfoX translation. We show that this regulation of the tfoR promoter is direct by performing electrophoretic mobility shift assays and by heterologous expression of this system in Escherichia coli. This transcriptional regulator was recently identified independently and was named “TfoS” (S. Yamamoto et al., Mol. Microbiol., in press, doi:10.1111/mmi.12462). Using a constitutively active form of TfoS, we demonstrate that the activity of this regulator is sufficient to promote competence in V. cholerae in the absence of chitin. Also, TfoS contains a large periplasmic domain, which we hypothesized interacts with chitin to regulate TfoS activity. In the heterologous host E. coli, we demonstrate that chitin oligosaccharides are sufficient to activate TfoS activity at the tfoR promoter. Collectively, these data characterize TfoS as a novel chitin-sensing transcriptional regulator that represents the direct link between chitin and natural competence in V. cholerae. IMPORTANCE Naturally competent bacteria can take up exogenous DNA from the environment and integrate it into their genome by homologous recombination. This ability to take up exogenous DNA is shared by diverse bacterial species and serves as a mechanism to acquire new genes to enhance the fitness of the organism. Several members of the family Vibrionaceae become naturally competent when grown on chitin; however, a molecular understanding of how chitin activates competence is lacking. Here, we identify a novel membrane-bound transcriptional regulator that is required for natural transformation in the human pathogen Vibrio cholerae. We demonstrate that this regulator senses chitin oligosaccharides to activate the competence cascade, thus, uncovering the molecular link between chitin and natural competence in this Vibrio species.
format article
author Ankur B. Dalia
David W. Lazinski
Andrew Camilli
author_facet Ankur B. Dalia
David W. Lazinski
Andrew Camilli
author_sort Ankur B. Dalia
title Identification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_short Identification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_full Identification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_fullStr Identification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_full_unstemmed Identification of a Membrane-Bound Transcriptional Regulator That Links Chitin and Natural Competence in <named-content content-type="genus-species">Vibrio cholerae</named-content>
title_sort identification of a membrane-bound transcriptional regulator that links chitin and natural competence in <named-content content-type="genus-species">vibrio cholerae</named-content>
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/d8f2e0800583445f93cff91b975832f7
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