Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence Genes
ABSTRACT In Streptococcus mutans, an oral colonizer associated with dental caries, development of competence for natural genetic transformation is triggered by either of two types of peptide pheromones, competence-stimulating peptides (CSPs) (18 amino acids [aa]) or SigX-inducing peptides (XIPs) (7...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2016-04-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00038-15 |
| _version_ | 1829465778468945920 |
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| author | R. Khan H. V. Rukke H. Høvik H. A. Åmdal T. Chen D. A. Morrison F. C. Petersen |
| author_facet | R. Khan H. V. Rukke H. Høvik H. A. Åmdal T. Chen D. A. Morrison F. C. Petersen |
| author_sort | R. Khan |
| collection | DOAJ |
| description | ABSTRACT In Streptococcus mutans, an oral colonizer associated with dental caries, development of competence for natural genetic transformation is triggered by either of two types of peptide pheromones, competence-stimulating peptides (CSPs) (18 amino acids [aa]) or SigX-inducing peptides (XIPs) (7 aa). Competence induced by CSP is a late response to the pheromone that requires the response regulator ComE and the XIP-encoding gene comS. XIP binds to ComR to allow expression of the alternative sigma factor SigX and the effector genes it controls. While these regulatory links are established, the precise set of effectors controlled by each regulator is poorly defined. To improve the definition of all three regulons, we used a high-resolution tiling array to map global changes in gene expression in the early and late phases of the CSP response. The early phase of the CSP response was limited to increased gene expression at four loci associated with bacteriocin production and immunity. In the late phase, upregulated regions expanded to a total of 29 loci, including comS and genes required for DNA uptake and recombination. The results indicate that the entire late response to CSP depends on the expression of comS and that the immediate transcriptional response to CSP, mediated by ComE, is restricted to just four bacteriocin-related loci. Comparison of the new data with published transcriptome data permitted the identification of all of the operons in each regulon: 4 for ComE, 2 for ComR, and 21 for SigX. Finally, a core set of 27 panstreptococcal competence genes was identified within the SigX regulon by comparison of transcriptome data from diverse streptococcal species. IMPORTANCE S. mutans has the hard surfaces of the oral cavity as its natural habitat, where it depends on its ability to form biofilms in order to survive. The comprehensive identification of S. mutans regulons activated in response to peptide pheromones provides an important basis for understanding how S. mutans can transition from individual to social behavior. Our study placed 27 of the 29 transcripts activated during competence within three major regulons and revealed a core set of 27 panstreptococcal competence-activated genes within the SigX regulon. |
| first_indexed | 2024-12-13T17:00:22Z |
| format | Article |
| id | doaj.art-cbad80e3dc6546c1b6ff7206a82d1870 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-13T17:00:22Z |
| publishDate | 2016-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-cbad80e3dc6546c1b6ff7206a82d18702022-12-21T23:37:49ZengAmerican Society for MicrobiologymSystems2379-50772016-04-011210.1128/mSystems.00038-15Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence GenesR. Khan0H. V. Rukke1H. Høvik2H. A. Åmdal3T. Chen4D. A. Morrison5F. C. Petersen6Department of Oral Biology, Faculty of Dentistry, University of Oslo, Oslo, NorwayDepartment of Oral Biology, Faculty of Dentistry, University of Oslo, Oslo, NorwayDepartment of Oral Biology, Faculty of Dentistry, University of Oslo, Oslo, NorwayDepartment of Oral Biology, Faculty of Dentistry, University of Oslo, Oslo, NorwayThe Forsyth Institute, Cambridge, Massachusetts, USADepartment of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois, USADepartment of Oral Biology, Faculty of Dentistry, University of Oslo, Oslo, NorwayABSTRACT In Streptococcus mutans, an oral colonizer associated with dental caries, development of competence for natural genetic transformation is triggered by either of two types of peptide pheromones, competence-stimulating peptides (CSPs) (18 amino acids [aa]) or SigX-inducing peptides (XIPs) (7 aa). Competence induced by CSP is a late response to the pheromone that requires the response regulator ComE and the XIP-encoding gene comS. XIP binds to ComR to allow expression of the alternative sigma factor SigX and the effector genes it controls. While these regulatory links are established, the precise set of effectors controlled by each regulator is poorly defined. To improve the definition of all three regulons, we used a high-resolution tiling array to map global changes in gene expression in the early and late phases of the CSP response. The early phase of the CSP response was limited to increased gene expression at four loci associated with bacteriocin production and immunity. In the late phase, upregulated regions expanded to a total of 29 loci, including comS and genes required for DNA uptake and recombination. The results indicate that the entire late response to CSP depends on the expression of comS and that the immediate transcriptional response to CSP, mediated by ComE, is restricted to just four bacteriocin-related loci. Comparison of the new data with published transcriptome data permitted the identification of all of the operons in each regulon: 4 for ComE, 2 for ComR, and 21 for SigX. Finally, a core set of 27 panstreptococcal competence genes was identified within the SigX regulon by comparison of transcriptome data from diverse streptococcal species. IMPORTANCE S. mutans has the hard surfaces of the oral cavity as its natural habitat, where it depends on its ability to form biofilms in order to survive. The comprehensive identification of S. mutans regulons activated in response to peptide pheromones provides an important basis for understanding how S. mutans can transition from individual to social behavior. Our study placed 27 of the 29 transcripts activated during competence within three major regulons and revealed a core set of 27 panstreptococcal competence-activated genes within the SigX regulon.https://journals.asm.org/doi/10.1128/mSystems.00038-15CSPStreptococcusXIPgenetic competencenatural transformation systemspheromone |
| spellingShingle | R. Khan H. V. Rukke H. Høvik H. A. Åmdal T. Chen D. A. Morrison F. C. Petersen Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence Genes mSystems CSP Streptococcus XIP genetic competence natural transformation systems pheromone |
| title | Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence Genes |
| title_full | Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence Genes |
| title_fullStr | Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence Genes |
| title_full_unstemmed | Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence Genes |
| title_short | Comprehensive Transcriptome Profiles of <named-content content-type="genus-species">Streptococcus mutans</named-content> UA159 Map Core Streptococcal Competence Genes |
| title_sort | comprehensive transcriptome profiles of named content content type genus species streptococcus mutans named content ua159 map core streptococcal competence genes |
| topic | CSP Streptococcus XIP genetic competence natural transformation systems pheromone |
| url | https://journals.asm.org/doi/10.1128/mSystems.00038-15 |
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