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CytR Is a Global Positive Regulator of Competence, Type VI Secretion, and Chitinases in Vibrio cholerae.

Watve SS, Thomas J, Hammer BK - PLoS ONE (2015)

Bottom Line: Through high-throughput RNA sequencing (RNA-seq), we show that CytR positively regulates the majority of competence genes, the three type VI secretion operons, and the four known or predicted chitinases.We used transcriptional reporters and phenotypic analysis to determine the individual contributions of quorum sensing, which is controlled by the transcription factors HapR and QstR; chitin utilization that is mediated by TfoX; and pyrimidine starvation that is orchestrated by CytR, toward each of these processes.We find that in V. cholerae, CytR is a global regulator of multiple behaviors affecting fitness and adaptability in the environment.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, Atlanta, Georgia, United States of America.

ABSTRACT
The facultative pathogen Vibrio cholerae transitions between its human host and aquatic reservoirs where it colonizes chitinous surfaces. Growth on chitin induces expression of chitin utilization genes, genes involved in DNA uptake by natural transformation, and a type VI secretion system that allows contact-dependent killing of neighboring bacteria. We have previously shown that the transcription factor CytR, thought to primarily regulate the pyrimidine nucleoside scavenging response, is required for natural competence in V. cholerae. Through high-throughput RNA sequencing (RNA-seq), we show that CytR positively regulates the majority of competence genes, the three type VI secretion operons, and the four known or predicted chitinases. We used transcriptional reporters and phenotypic analysis to determine the individual contributions of quorum sensing, which is controlled by the transcription factors HapR and QstR; chitin utilization that is mediated by TfoX; and pyrimidine starvation that is orchestrated by CytR, toward each of these processes. We find that in V. cholerae, CytR is a global regulator of multiple behaviors affecting fitness and adaptability in the environment.

No MeSH data available.


Related in: MedlinePlus

CytR and TfoX co-regulate natural competence, chitinase expression and the type VI secretion system.Panel A: V. cholerae C6706 is capable of natural transformation in LB medium lacking chitin if tfoX is constitutively expressed (TfoX*, bar 1) but not if tfoX is under control of its native promoter (TfoX+, bars 3 and 4). No transformants were detected in the absence of CytR (CytR-, bars 2 and 4). Transformation frequency is expressed as the number of kanamycin resistant cfu mL-1 divided by total cfu mL-1. The limit of detection (d.l.) is 1 x 10−8. Data are shown as mean ± standard deviation from three independent biological replicates. Panel B: Heat map of genes differentially regulated by CytR in the absence (TfoX+, column 1) or presence (TfoX*, column 2) of TfoX induction, and genes differentially regulated by TfoX in the absence (CytR-, column 3) or presence (CytR+, column 4) of a functional cytR gene. The majority of known competence genes are positively regulated by both TfoX and CytR and can be classified into four distinct regulatory classes (see text for details). CytR and TfoX positively regulate the three known T6SS gene clusters as well as four chitinase genes. CytR negatively regulates nucleoside uptake and catabolism genes in a TfoX-independent manner.
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pone.0138834.g001: CytR and TfoX co-regulate natural competence, chitinase expression and the type VI secretion system.Panel A: V. cholerae C6706 is capable of natural transformation in LB medium lacking chitin if tfoX is constitutively expressed (TfoX*, bar 1) but not if tfoX is under control of its native promoter (TfoX+, bars 3 and 4). No transformants were detected in the absence of CytR (CytR-, bars 2 and 4). Transformation frequency is expressed as the number of kanamycin resistant cfu mL-1 divided by total cfu mL-1. The limit of detection (d.l.) is 1 x 10−8. Data are shown as mean ± standard deviation from three independent biological replicates. Panel B: Heat map of genes differentially regulated by CytR in the absence (TfoX+, column 1) or presence (TfoX*, column 2) of TfoX induction, and genes differentially regulated by TfoX in the absence (CytR-, column 3) or presence (CytR+, column 4) of a functional cytR gene. The majority of known competence genes are positively regulated by both TfoX and CytR and can be classified into four distinct regulatory classes (see text for details). CytR and TfoX positively regulate the three known T6SS gene clusters as well as four chitinase genes. CytR negatively regulates nucleoside uptake and catabolism genes in a TfoX-independent manner.

Mentions: In Escherichia coli, the cytidine repressor CytR negatively regulates a small set of pyrimidine nucleoside scavenging and metabolism genes, including uridine dephosphorylase, udp [17]. In Vibrio cholerae (El Tor strain C6706), we recently demonstrated that in addition to repressing udp, CytR also positively regulates competence genes comEA and pilA, and the chitinase gene chiA-1 [16]. We now find that CytR is required for expression of the majority of known competence genes, the three Type VI secretion system (T6SS) clusters, and four known chitinase genes (Fig 1B).


CytR Is a Global Positive Regulator of Competence, Type VI Secretion, and Chitinases in Vibrio cholerae.

Watve SS, Thomas J, Hammer BK - PLoS ONE (2015)

CytR and TfoX co-regulate natural competence, chitinase expression and the type VI secretion system.Panel A: V. cholerae C6706 is capable of natural transformation in LB medium lacking chitin if tfoX is constitutively expressed (TfoX*, bar 1) but not if tfoX is under control of its native promoter (TfoX+, bars 3 and 4). No transformants were detected in the absence of CytR (CytR-, bars 2 and 4). Transformation frequency is expressed as the number of kanamycin resistant cfu mL-1 divided by total cfu mL-1. The limit of detection (d.l.) is 1 x 10−8. Data are shown as mean ± standard deviation from three independent biological replicates. Panel B: Heat map of genes differentially regulated by CytR in the absence (TfoX+, column 1) or presence (TfoX*, column 2) of TfoX induction, and genes differentially regulated by TfoX in the absence (CytR-, column 3) or presence (CytR+, column 4) of a functional cytR gene. The majority of known competence genes are positively regulated by both TfoX and CytR and can be classified into four distinct regulatory classes (see text for details). CytR and TfoX positively regulate the three known T6SS gene clusters as well as four chitinase genes. CytR negatively regulates nucleoside uptake and catabolism genes in a TfoX-independent manner.
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Related In: Results  -  Collection

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pone.0138834.g001: CytR and TfoX co-regulate natural competence, chitinase expression and the type VI secretion system.Panel A: V. cholerae C6706 is capable of natural transformation in LB medium lacking chitin if tfoX is constitutively expressed (TfoX*, bar 1) but not if tfoX is under control of its native promoter (TfoX+, bars 3 and 4). No transformants were detected in the absence of CytR (CytR-, bars 2 and 4). Transformation frequency is expressed as the number of kanamycin resistant cfu mL-1 divided by total cfu mL-1. The limit of detection (d.l.) is 1 x 10−8. Data are shown as mean ± standard deviation from three independent biological replicates. Panel B: Heat map of genes differentially regulated by CytR in the absence (TfoX+, column 1) or presence (TfoX*, column 2) of TfoX induction, and genes differentially regulated by TfoX in the absence (CytR-, column 3) or presence (CytR+, column 4) of a functional cytR gene. The majority of known competence genes are positively regulated by both TfoX and CytR and can be classified into four distinct regulatory classes (see text for details). CytR and TfoX positively regulate the three known T6SS gene clusters as well as four chitinase genes. CytR negatively regulates nucleoside uptake and catabolism genes in a TfoX-independent manner.
Mentions: In Escherichia coli, the cytidine repressor CytR negatively regulates a small set of pyrimidine nucleoside scavenging and metabolism genes, including uridine dephosphorylase, udp [17]. In Vibrio cholerae (El Tor strain C6706), we recently demonstrated that in addition to repressing udp, CytR also positively regulates competence genes comEA and pilA, and the chitinase gene chiA-1 [16]. We now find that CytR is required for expression of the majority of known competence genes, the three Type VI secretion system (T6SS) clusters, and four known chitinase genes (Fig 1B).

Bottom Line: Through high-throughput RNA sequencing (RNA-seq), we show that CytR positively regulates the majority of competence genes, the three type VI secretion operons, and the four known or predicted chitinases.We used transcriptional reporters and phenotypic analysis to determine the individual contributions of quorum sensing, which is controlled by the transcription factors HapR and QstR; chitin utilization that is mediated by TfoX; and pyrimidine starvation that is orchestrated by CytR, toward each of these processes.We find that in V. cholerae, CytR is a global regulator of multiple behaviors affecting fitness and adaptability in the environment.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, Atlanta, Georgia, United States of America.

ABSTRACT
The facultative pathogen Vibrio cholerae transitions between its human host and aquatic reservoirs where it colonizes chitinous surfaces. Growth on chitin induces expression of chitin utilization genes, genes involved in DNA uptake by natural transformation, and a type VI secretion system that allows contact-dependent killing of neighboring bacteria. We have previously shown that the transcription factor CytR, thought to primarily regulate the pyrimidine nucleoside scavenging response, is required for natural competence in V. cholerae. Through high-throughput RNA sequencing (RNA-seq), we show that CytR positively regulates the majority of competence genes, the three type VI secretion operons, and the four known or predicted chitinases. We used transcriptional reporters and phenotypic analysis to determine the individual contributions of quorum sensing, which is controlled by the transcription factors HapR and QstR; chitin utilization that is mediated by TfoX; and pyrimidine starvation that is orchestrated by CytR, toward each of these processes. We find that in V. cholerae, CytR is a global regulator of multiple behaviors affecting fitness and adaptability in the environment.

No MeSH data available.


Related in: MedlinePlus