The response regulator ComE in Streptococcus mutans functions both as a transcription activator of mutacin production and repressor of CSP biosynthesis

Jens Kreth, David C I Hung, Justin Merritt, Julie Perry, Lin Zhu, Steven D. Goodman, Dennis G. Cvitkovitch, Wenyuan Shi, Fengxia Qi

Research output: Contribution to journalArticle

58 Citations (Scopus)

Abstract

In Streptococcus pneumoniae, competence and bacteriocin genes are controlled by two two-component systems, ComED and BlpRH, respectively. In Streptococcus mutans, both functions are controlled by the ComED system. Recent studies in S. mutans revealed a potential ComE binding site characterized by two 11 bp direct repeats shared by each of the bacteriocin genes responsive to the competence-stimulating peptide (CSP). Interestingly, this sequence was not found in the upstream region of the CSP structural gene comC. Since comC is suggested to be part of a CSP-responsive and ComE-dependent autoregulatory loop, it was of interest to determine how it was possible that the ComED system could simultaneously regulate bacteriocin expression and natural competence. Using the intergenic region IGS1499, shared by the CSP-responsive bacteriocin nlmC and comC, it was demonstrated that both genes are likely to be regulated by a bifunctional ComE. In a comE null mutant, comC gene expression was increased similarly to a fully induced wild-type. In contrast, nlmC gene expression was nearly abolished. Deletion of ComD exerted a similar effect on both genes to that observed with the comE null mutation. Electrophoretic mobility shift assays (EMSAs) with purified ComE revealed specific shift patterns dependent on the presence of one or both direct repeats in the nlmC-comC promoter region. The two direct repeats were also required for the promoter activity of both nlmC and comC. These results suggest that gene regulation of comC in S. mutans is fundamentally different from that reported for S. pneumoniae, which implicates a unique regulatory mechanism that allows the coordination of bacteriocin production with competence development.

Original languageEnglish (US)
Pages (from-to)1799-1807
Number of pages9
JournalMicrobiology
Volume153
Issue number6
DOIs
StatePublished - Jun 2007
Externally publishedYes

Fingerprint

Peptide Biosynthesis
Streptococcus mutans
Mental Competency
Bacteriocins
Nucleic Acid Repetitive Sequences
Genes
Peptides
Streptococcus pneumoniae
Gene Expression
Intergenic DNA
Electrophoretic Mobility Shift Assay
Genetic Promoter Regions
Binding Sites
Mutation

ASJC Scopus subject areas

  • Microbiology

Cite this

The response regulator ComE in Streptococcus mutans functions both as a transcription activator of mutacin production and repressor of CSP biosynthesis. / Kreth, Jens; Hung, David C I; Merritt, Justin; Perry, Julie; Zhu, Lin; Goodman, Steven D.; Cvitkovitch, Dennis G.; Shi, Wenyuan; Qi, Fengxia.

In: Microbiology, Vol. 153, No. 6, 06.2007, p. 1799-1807.

Research output: Contribution to journalArticle

Kreth, Jens ; Hung, David C I ; Merritt, Justin ; Perry, Julie ; Zhu, Lin ; Goodman, Steven D. ; Cvitkovitch, Dennis G. ; Shi, Wenyuan ; Qi, Fengxia. / The response regulator ComE in Streptococcus mutans functions both as a transcription activator of mutacin production and repressor of CSP biosynthesis. In: Microbiology. 2007 ; Vol. 153, No. 6. pp. 1799-1807.
@article{f85f4732294447caac647b7da2a3165e,
title = "The response regulator ComE in Streptococcus mutans functions both as a transcription activator of mutacin production and repressor of CSP biosynthesis",
abstract = "In Streptococcus pneumoniae, competence and bacteriocin genes are controlled by two two-component systems, ComED and BlpRH, respectively. In Streptococcus mutans, both functions are controlled by the ComED system. Recent studies in S. mutans revealed a potential ComE binding site characterized by two 11 bp direct repeats shared by each of the bacteriocin genes responsive to the competence-stimulating peptide (CSP). Interestingly, this sequence was not found in the upstream region of the CSP structural gene comC. Since comC is suggested to be part of a CSP-responsive and ComE-dependent autoregulatory loop, it was of interest to determine how it was possible that the ComED system could simultaneously regulate bacteriocin expression and natural competence. Using the intergenic region IGS1499, shared by the CSP-responsive bacteriocin nlmC and comC, it was demonstrated that both genes are likely to be regulated by a bifunctional ComE. In a comE null mutant, comC gene expression was increased similarly to a fully induced wild-type. In contrast, nlmC gene expression was nearly abolished. Deletion of ComD exerted a similar effect on both genes to that observed with the comE null mutation. Electrophoretic mobility shift assays (EMSAs) with purified ComE revealed specific shift patterns dependent on the presence of one or both direct repeats in the nlmC-comC promoter region. The two direct repeats were also required for the promoter activity of both nlmC and comC. These results suggest that gene regulation of comC in S. mutans is fundamentally different from that reported for S. pneumoniae, which implicates a unique regulatory mechanism that allows the coordination of bacteriocin production with competence development.",
author = "Jens Kreth and Hung, {David C I} and Justin Merritt and Julie Perry and Lin Zhu and Goodman, {Steven D.} and Cvitkovitch, {Dennis G.} and Wenyuan Shi and Fengxia Qi",
year = "2007",
month = "6",
doi = "10.1099/mic.0.2007/005975-0",
language = "English (US)",
volume = "153",
pages = "1799--1807",
journal = "Microbiology",
issn = "1350-0872",
publisher = "Society for General Microbiology",
number = "6",

}

TY - JOUR

T1 - The response regulator ComE in Streptococcus mutans functions both as a transcription activator of mutacin production and repressor of CSP biosynthesis

AU - Kreth, Jens

AU - Hung, David C I

AU - Merritt, Justin

AU - Perry, Julie

AU - Zhu, Lin

AU - Goodman, Steven D.

AU - Cvitkovitch, Dennis G.

AU - Shi, Wenyuan

AU - Qi, Fengxia

PY - 2007/6

Y1 - 2007/6

N2 - In Streptococcus pneumoniae, competence and bacteriocin genes are controlled by two two-component systems, ComED and BlpRH, respectively. In Streptococcus mutans, both functions are controlled by the ComED system. Recent studies in S. mutans revealed a potential ComE binding site characterized by two 11 bp direct repeats shared by each of the bacteriocin genes responsive to the competence-stimulating peptide (CSP). Interestingly, this sequence was not found in the upstream region of the CSP structural gene comC. Since comC is suggested to be part of a CSP-responsive and ComE-dependent autoregulatory loop, it was of interest to determine how it was possible that the ComED system could simultaneously regulate bacteriocin expression and natural competence. Using the intergenic region IGS1499, shared by the CSP-responsive bacteriocin nlmC and comC, it was demonstrated that both genes are likely to be regulated by a bifunctional ComE. In a comE null mutant, comC gene expression was increased similarly to a fully induced wild-type. In contrast, nlmC gene expression was nearly abolished. Deletion of ComD exerted a similar effect on both genes to that observed with the comE null mutation. Electrophoretic mobility shift assays (EMSAs) with purified ComE revealed specific shift patterns dependent on the presence of one or both direct repeats in the nlmC-comC promoter region. The two direct repeats were also required for the promoter activity of both nlmC and comC. These results suggest that gene regulation of comC in S. mutans is fundamentally different from that reported for S. pneumoniae, which implicates a unique regulatory mechanism that allows the coordination of bacteriocin production with competence development.

AB - In Streptococcus pneumoniae, competence and bacteriocin genes are controlled by two two-component systems, ComED and BlpRH, respectively. In Streptococcus mutans, both functions are controlled by the ComED system. Recent studies in S. mutans revealed a potential ComE binding site characterized by two 11 bp direct repeats shared by each of the bacteriocin genes responsive to the competence-stimulating peptide (CSP). Interestingly, this sequence was not found in the upstream region of the CSP structural gene comC. Since comC is suggested to be part of a CSP-responsive and ComE-dependent autoregulatory loop, it was of interest to determine how it was possible that the ComED system could simultaneously regulate bacteriocin expression and natural competence. Using the intergenic region IGS1499, shared by the CSP-responsive bacteriocin nlmC and comC, it was demonstrated that both genes are likely to be regulated by a bifunctional ComE. In a comE null mutant, comC gene expression was increased similarly to a fully induced wild-type. In contrast, nlmC gene expression was nearly abolished. Deletion of ComD exerted a similar effect on both genes to that observed with the comE null mutation. Electrophoretic mobility shift assays (EMSAs) with purified ComE revealed specific shift patterns dependent on the presence of one or both direct repeats in the nlmC-comC promoter region. The two direct repeats were also required for the promoter activity of both nlmC and comC. These results suggest that gene regulation of comC in S. mutans is fundamentally different from that reported for S. pneumoniae, which implicates a unique regulatory mechanism that allows the coordination of bacteriocin production with competence development.

UR - http://www.scopus.com/inward/record.url?scp=34250710054&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34250710054&partnerID=8YFLogxK

U2 - 10.1099/mic.0.2007/005975-0

DO - 10.1099/mic.0.2007/005975-0

M3 - Article

C2 - 17526837

AN - SCOPUS:34250710054

VL - 153

SP - 1799

EP - 1807

JO - Microbiology

JF - Microbiology

SN - 1350-0872

IS - 6

ER -