Regulation of PI-2b Pilus Expression in Hypervirulent Streptococcus agalactiae ST-17 BM110
The widely spread Streptococcus agalactiae (also known as Group B Streptococcus, GBS) "hypervirulent" ST17 clone is strongly associated with neonatal meningitis. The PI-2b locus is mainly found in ST17 strains but is also present in a few non ST17 human isolates such as the ST-7 prototype...
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| creator | Périchon, Bruno Szili, Noémi du Merle, Laurence Rosinski-Chupin, Isabelle Gominet, Myriam Bellais, Samuel Poyart, Claire Trieu-Cuot, Patrick Dramsi, Shaynoor |
| description | The widely spread Streptococcus agalactiae (also known as Group B Streptococcus, GBS) "hypervirulent" ST17 clone is strongly associated with neonatal meningitis. The PI-2b locus is mainly found in ST17 strains but is also present in a few non ST17 human isolates such as the ST-7 prototype strain A909. Here, we analysed the expression of the PI-2b pilus in the ST17 strain BM110 as compared to the non ST17 A909. Comparative genome analyses revealed the presence of a 43-base pair (bp) hairpin-like structure in the upstream region of PI-2b operon in all 26 ST17 genomes, which was absent in the 8 non-ST17 strains carrying the PI-2b locus. Deletion of this 43-bp sequence in strain BM110 resulted in a 3- to 5-fold increased transcription of PI-2b. Characterization of PI-2b promoter region in A909 and BM110 strains was carried out by RNAseq, primer extension, qRT-PCR and transcriptional fusions with gfp as reporter gene. Our results indicate the presence of a single promoter (Ppi2b) with a transcriptional start site (TSS) mapped 37 bases upstream of the start codon of the first PI-2b gene. The large operon of 16 genes located upstream of PI-2b codes for the group B carbohydrate (also known as antigen B), a major constituent of the bacterial cell wall. We showed that the hairpin sequence located between antigen B and PI-2b operons is a transcriptional terminator. In A909, increased expression of PI-2b probably results from read-through transcription from antigen B operon. In addition, we showed that an extended 5' promoter region is required for maximal transcription of gfp as a reporter gene in S. agalactiae from Ppi2b promoter. Gene reporter assays performed in Lactococcus lactis strain NZ9000, a related non-pathogenic Gram-positive species, revealed that GBS-specific regulatory factors are required to drive PI-2b transcription. PI-2b expression is up-regulated in the BM110ΔcovR mutant as compared to the parental BM110 strain, but this effect is probably indirect. Collectively, our results indicate that PI-2b expression is regulated in GBS ST17 strains, which may confer a selective advantage in the human host either by reducing host immune responses and/or increasing their dissemination potential. |
| doi_str_mv | 10.1371/journal.pone.0169840 |
| format | Article |
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The PI-2b locus is mainly found in ST17 strains but is also present in a few non ST17 human isolates such as the ST-7 prototype strain A909. Here, we analysed the expression of the PI-2b pilus in the ST17 strain BM110 as compared to the non ST17 A909. Comparative genome analyses revealed the presence of a 43-base pair (bp) hairpin-like structure in the upstream region of PI-2b operon in all 26 ST17 genomes, which was absent in the 8 non-ST17 strains carrying the PI-2b locus. Deletion of this 43-bp sequence in strain BM110 resulted in a 3- to 5-fold increased transcription of PI-2b. Characterization of PI-2b promoter region in A909 and BM110 strains was carried out by RNAseq, primer extension, qRT-PCR and transcriptional fusions with gfp as reporter gene. Our results indicate the presence of a single promoter (Ppi2b) with a transcriptional start site (TSS) mapped 37 bases upstream of the start codon of the first PI-2b gene. The large operon of 16 genes located upstream of PI-2b codes for the group B carbohydrate (also known as antigen B), a major constituent of the bacterial cell wall. We showed that the hairpin sequence located between antigen B and PI-2b operons is a transcriptional terminator. In A909, increased expression of PI-2b probably results from read-through transcription from antigen B operon. In addition, we showed that an extended 5' promoter region is required for maximal transcription of gfp as a reporter gene in S. agalactiae from Ppi2b promoter. Gene reporter assays performed in Lactococcus lactis strain NZ9000, a related non-pathogenic Gram-positive species, revealed that GBS-specific regulatory factors are required to drive PI-2b transcription. PI-2b expression is up-regulated in the BM110ΔcovR mutant as compared to the parental BM110 strain, but this effect is probably indirect. Collectively, our results indicate that PI-2b expression is regulated in GBS ST17 strains, which may confer a selective advantage in the human host either by reducing host immune responses and/or increasing their dissemination potential.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0169840</identifier><identifier>PMID: 28107386</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Appendages (Animal anatomy) ; Bacteria ; Biofilms ; Biology ; Biology and Life Sciences ; Blood-brain barrier ; Carbohydrates ; Cell walls ; Clonal deletion ; Codon, Initiator ; Drug resistance ; Fimbriae Proteins ; Fimbriae Proteins - genetics ; Fimbriae, Bacterial ; Fimbriae, Bacterial - metabolism ; Gene Deletion ; Gene expression ; Genes, Bacterial ; Genetic aspects ; Genomes ; Genomics ; Immune response ; Lactococcus lactis ; Life Sciences ; Loci ; Medicine and health sciences ; Meningitis ; Neonates ; Operon ; Operons ; Physiological aspects ; Proteins ; Reporter gene ; Strains (organisms) ; Streptococcus ; Streptococcus agalactiae ; Streptococcus agalactiae - genetics ; Streptococcus agalactiae - pathogenicity ; Streptococcus infections ; Transcription ; Transcription (Genetics) ; Transcription, Genetic ; Virulence ; Virulence - genetics</subject><ispartof>PloS one, 2017-01, Vol.12 (1), p.e0169840-e0169840</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Périchon et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2017 Périchon et al 2017 Périchon et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c829t-a24c79661ab8463a02012c8a7e6929a1cc8dbc12ac0a376cdcd53fc9750f8b4f3</citedby><cites>FETCH-LOGICAL-c829t-a24c79661ab8463a02012c8a7e6929a1cc8dbc12ac0a376cdcd53fc9750f8b4f3</cites><orcidid>0000-0001-8323-3878 ; 0000-0002-5464-0949 ; 0000-0002-2768-9587</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5249243/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5249243/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28107386$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://pasteur.hal.science/pasteur-01570205$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Ton-That, Hung</contributor><creatorcontrib>Périchon, Bruno</creatorcontrib><creatorcontrib>Szili, Noémi</creatorcontrib><creatorcontrib>du Merle, Laurence</creatorcontrib><creatorcontrib>Rosinski-Chupin, Isabelle</creatorcontrib><creatorcontrib>Gominet, Myriam</creatorcontrib><creatorcontrib>Bellais, Samuel</creatorcontrib><creatorcontrib>Poyart, Claire</creatorcontrib><creatorcontrib>Trieu-Cuot, Patrick</creatorcontrib><creatorcontrib>Dramsi, Shaynoor</creatorcontrib><title>Regulation of PI-2b Pilus Expression in Hypervirulent Streptococcus agalactiae ST-17 BM110</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The widely spread Streptococcus agalactiae (also known as Group B Streptococcus, GBS) "hypervirulent" ST17 clone is strongly associated with neonatal meningitis. The PI-2b locus is mainly found in ST17 strains but is also present in a few non ST17 human isolates such as the ST-7 prototype strain A909. Here, we analysed the expression of the PI-2b pilus in the ST17 strain BM110 as compared to the non ST17 A909. Comparative genome analyses revealed the presence of a 43-base pair (bp) hairpin-like structure in the upstream region of PI-2b operon in all 26 ST17 genomes, which was absent in the 8 non-ST17 strains carrying the PI-2b locus. Deletion of this 43-bp sequence in strain BM110 resulted in a 3- to 5-fold increased transcription of PI-2b. Characterization of PI-2b promoter region in A909 and BM110 strains was carried out by RNAseq, primer extension, qRT-PCR and transcriptional fusions with gfp as reporter gene. Our results indicate the presence of a single promoter (Ppi2b) with a transcriptional start site (TSS) mapped 37 bases upstream of the start codon of the first PI-2b gene. The large operon of 16 genes located upstream of PI-2b codes for the group B carbohydrate (also known as antigen B), a major constituent of the bacterial cell wall. We showed that the hairpin sequence located between antigen B and PI-2b operons is a transcriptional terminator. In A909, increased expression of PI-2b probably results from read-through transcription from antigen B operon. In addition, we showed that an extended 5' promoter region is required for maximal transcription of gfp as a reporter gene in S. agalactiae from Ppi2b promoter. Gene reporter assays performed in Lactococcus lactis strain NZ9000, a related non-pathogenic Gram-positive species, revealed that GBS-specific regulatory factors are required to drive PI-2b transcription. PI-2b expression is up-regulated in the BM110ΔcovR mutant as compared to the parental BM110 strain, but this effect is probably indirect. Collectively, our results indicate that PI-2b expression is regulated in GBS ST17 strains, which may confer a selective advantage in the human host either by reducing host immune responses and/or increasing their dissemination potential.</description><subject>Appendages (Animal anatomy)</subject><subject>Bacteria</subject><subject>Biofilms</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Blood-brain barrier</subject><subject>Carbohydrates</subject><subject>Cell walls</subject><subject>Clonal deletion</subject><subject>Codon, Initiator</subject><subject>Drug resistance</subject><subject>Fimbriae Proteins</subject><subject>Fimbriae Proteins - genetics</subject><subject>Fimbriae, Bacterial</subject><subject>Fimbriae, Bacterial - metabolism</subject><subject>Gene Deletion</subject><subject>Gene expression</subject><subject>Genes, Bacterial</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Immune response</subject><subject>Lactococcus lactis</subject><subject>Life Sciences</subject><subject>Loci</subject><subject>Medicine and health sciences</subject><subject>Meningitis</subject><subject>Neonates</subject><subject>Operon</subject><subject>Operons</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Reporter gene</subject><subject>Strains (organisms)</subject><subject>Streptococcus</subject><subject>Streptococcus agalactiae</subject><subject>Streptococcus agalactiae - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest advanced technologies & aerospace journals</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials science collection</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Périchon, Bruno</au><au>Szili, Noémi</au><au>du Merle, Laurence</au><au>Rosinski-Chupin, Isabelle</au><au>Gominet, Myriam</au><au>Bellais, Samuel</au><au>Poyart, Claire</au><au>Trieu-Cuot, Patrick</au><au>Dramsi, Shaynoor</au><au>Ton-That, Hung</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of PI-2b Pilus Expression in Hypervirulent Streptococcus agalactiae ST-17 BM110</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-01-20</date><risdate>2017</risdate><volume>12</volume><issue>1</issue><spage>e0169840</spage><epage>e0169840</epage><pages>e0169840-e0169840</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The widely spread Streptococcus agalactiae (also known as Group B Streptococcus, GBS) "hypervirulent" ST17 clone is strongly associated with neonatal meningitis. The PI-2b locus is mainly found in ST17 strains but is also present in a few non ST17 human isolates such as the ST-7 prototype strain A909. Here, we analysed the expression of the PI-2b pilus in the ST17 strain BM110 as compared to the non ST17 A909. Comparative genome analyses revealed the presence of a 43-base pair (bp) hairpin-like structure in the upstream region of PI-2b operon in all 26 ST17 genomes, which was absent in the 8 non-ST17 strains carrying the PI-2b locus. Deletion of this 43-bp sequence in strain BM110 resulted in a 3- to 5-fold increased transcription of PI-2b. Characterization of PI-2b promoter region in A909 and BM110 strains was carried out by RNAseq, primer extension, qRT-PCR and transcriptional fusions with gfp as reporter gene. Our results indicate the presence of a single promoter (Ppi2b) with a transcriptional start site (TSS) mapped 37 bases upstream of the start codon of the first PI-2b gene. The large operon of 16 genes located upstream of PI-2b codes for the group B carbohydrate (also known as antigen B), a major constituent of the bacterial cell wall. We showed that the hairpin sequence located between antigen B and PI-2b operons is a transcriptional terminator. In A909, increased expression of PI-2b probably results from read-through transcription from antigen B operon. In addition, we showed that an extended 5' promoter region is required for maximal transcription of gfp as a reporter gene in S. agalactiae from Ppi2b promoter. Gene reporter assays performed in Lactococcus lactis strain NZ9000, a related non-pathogenic Gram-positive species, revealed that GBS-specific regulatory factors are required to drive PI-2b transcription. PI-2b expression is up-regulated in the BM110ΔcovR mutant as compared to the parental BM110 strain, but this effect is probably indirect. Collectively, our results indicate that PI-2b expression is regulated in GBS ST17 strains, which may confer a selective advantage in the human host either by reducing host immune responses and/or increasing their dissemination potential.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28107386</pmid><doi>10.1371/journal.pone.0169840</doi><tpages>e0169840</tpages><orcidid>https://orcid.org/0000-0001-8323-3878</orcidid><orcidid>https://orcid.org/0000-0002-5464-0949</orcidid><orcidid>https://orcid.org/0000-0002-2768-9587</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2017-01, Vol.12 (1), p.e0169840-e0169840 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1860295812 |
| source | MEDLINE; Free E-Journal (出版社公開部分のみ）; PLoS_OA刊; DOAJ Directory of Open Access Journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Appendages (Animal anatomy) Bacteria Biofilms Biology Biology and Life Sciences Blood-brain barrier Carbohydrates Cell walls Clonal deletion Codon, Initiator Drug resistance Fimbriae Proteins Fimbriae Proteins - genetics Fimbriae, Bacterial Fimbriae, Bacterial - metabolism Gene Deletion Gene expression Genes, Bacterial Genetic aspects Genomes Genomics Immune response Lactococcus lactis Life Sciences Loci Medicine and health sciences Meningitis Neonates Operon Operons Physiological aspects Proteins Reporter gene Strains (organisms) Streptococcus Streptococcus agalactiae Streptococcus agalactiae - genetics Streptococcus agalactiae - pathogenicity Streptococcus infections Transcription Transcription (Genetics) Transcription, Genetic Virulence Virulence - genetics |
| title | Regulation of PI-2b Pilus Expression in Hypervirulent Streptococcus agalactiae ST-17 BM110 |
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