Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism
The O-antigen of Salmonella lipopolysaccharide is a major antigenic determinant and its chemical composition forms the basis for Salmonella serotyping. Modifications of the O-antigen that can affect the serotype include those carried out by the products of glycosyltransferase operons (gtr), which ar...
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| Veröffentlicht in: | Molecular microbiology 2010-07, Vol.77 (2), p.337-353 |
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| creator | Broadbent, S.E Davies, M.R van der Woude, M.W |
| description | The O-antigen of Salmonella lipopolysaccharide is a major antigenic determinant and its chemical composition forms the basis for Salmonella serotyping. Modifications of the O-antigen that can affect the serotype include those carried out by the products of glycosyltransferase operons (gtr), which are present on specific Salmonella and phage genomes. Here we show that expression of the gtr genes encoded by phage P22 that confers the O1 serotype is under the control of phase variation. This phase variation occurs by a novel epigenetic mechanism requiring OxyR in conjunction with the DNA methyltransferase Dam. OxyR is an activator or a repressor of the system depending on which of its two binding sites in the gtr regulatory region is occupied. Binding is decreased by methylation at Dam target sequences in either site, and this confers heritability of the expression state to the system. Most Salmonella gtr operons share the key regulatory elements that are identified here as essential for this epigenetic phase variation. |
| doi_str_mv | 10.1111/j.1365-2958.2010.07203.x |
| format | Article |
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Modifications of the O-antigen that can affect the serotype include those carried out by the products of glycosyltransferase operons (gtr), which are present on specific Salmonella and phage genomes. Here we show that expression of the gtr genes encoded by phage P22 that confers the O1 serotype is under the control of phase variation. This phase variation occurs by a novel epigenetic mechanism requiring OxyR in conjunction with the DNA methyltransferase Dam. OxyR is an activator or a repressor of the system depending on which of its two binding sites in the gtr regulatory region is occupied. Binding is decreased by methylation at Dam target sequences in either site, and this confers heritability of the expression state to the system. Most Salmonella gtr operons share the key regulatory elements that are identified here as essential for this epigenetic phase variation.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2010.07203.x</identifier><identifier>PMID: 20487280</identifier><language>eng</language><publisher>Oxford, UK: Oxford, UK : Blackwell Publishing Ltd</publisher><subject>Antigens ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteriology ; Bacteriophage P22 ; Base Sequence ; Biological and medical sciences ; Deoxyribonucleic acid ; DNA ; DNA Methylation ; DNA, Bacterial - metabolism ; Epigenesis, Genetic ; Fundamental and applied biological sciences. Psychology ; Gene expression ; Gene Expression Regulation, Bacterial ; Genes ; Glycosyltransferases - genetics ; Microbiology ; Miscellaneous ; Molecular Sequence Data ; Multigene Family ; Mutagenesis, Site-Directed ; O Antigens - metabolism ; Operon ; Phage P22 ; Promoter Regions, Genetic ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; Salmonella ; Salmonella typhimurium - genetics ; Salmonella typhimurium - metabolism ; Salmonella typhimurium - virology ; Sequence Analysis, DNA ; Site-Specific DNA-Methyltransferase (Adenine-Specific) - metabolism</subject><ispartof>Molecular microbiology, 2010-07, Vol.77 (2), p.337-353</ispartof><rights>2010 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>Copyright Blackwell Publishing Ltd. 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Modifications of the O-antigen that can affect the serotype include those carried out by the products of glycosyltransferase operons (gtr), which are present on specific Salmonella and phage genomes. Here we show that expression of the gtr genes encoded by phage P22 that confers the O1 serotype is under the control of phase variation. This phase variation occurs by a novel epigenetic mechanism requiring OxyR in conjunction with the DNA methyltransferase Dam. OxyR is an activator or a repressor of the system depending on which of its two binding sites in the gtr regulatory region is occupied. Binding is decreased by methylation at Dam target sequences in either site, and this confers heritability of the expression state to the system. Most Salmonella gtr operons share the key regulatory elements that are identified here as essential for this epigenetic phase variation.</description><subject>Antigens</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Bacteriophage P22</subject><subject>Base Sequence</subject><subject>Biological and medical sciences</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Methylation</subject><subject>DNA, Bacterial - metabolism</subject><subject>Epigenesis, Genetic</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genes</subject><subject>Glycosyltransferases - genetics</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family</subject><subject>Mutagenesis, Site-Directed</subject><subject>O Antigens - metabolism</subject><subject>Operon</subject><subject>Phage P22</subject><subject>Promoter Regions, Genetic</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Salmonella</subject><subject>Salmonella typhimurium - genetics</subject><subject>Salmonella typhimurium - metabolism</subject><subject>Salmonella typhimurium - virology</subject><subject>Sequence Analysis, DNA</subject><subject>Site-Specific DNA-Methyltransferase (Adenine-Specific) - metabolism</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqNkkuPFCEQxztG466rX0GJifHUIw00j4Mmm_W1ya6arJt4IzQNM0xoaGFmnbn50aV3xvFxUThAqn7_ooqqqgINnDVlvVjOGkzbGomWzxAsVsgQxLPNner44LhbHUPRwhpz9OWoepDzEsIGQ4rvV0cIEs4Qh8fV908LlQ24UcmplYsB6BhWKfoMzGZMJufJFi24Un6IwXivgHdjHKPfZqX1ouh6A4bYO-v0LsLcBJNBtwUKvP5wCgazWmz9ravuzWhCb8KqWIs2uDw8rO5Z5bN5tD9Pquu3bz6fva8vPr47Pzu9qDVtOK57xhQxlmPKGcPQMCKY6FSpkDCKLdaaNB23gkCuVNdba3gLGWaUWdx1xOCT6tUu7rjuBtPrkkRSXo7JDSptZVRO_ukJbiHn8UYiAQUWsAR4vg-Q4te1ySs5uKynHwkmrrNkLWkxL_vfJGkZRoiRQj79i1zGdQrlHySFQlBIUVMgvoN0ijknYw9JN1BO4yCXcuq6nLoup3GQt-MgN0X6-PeiD8Kf_S_Asz2gslbeJhW0y784JDjBZEr05Y775rzZ_ncC8vLyfLoV_ZOd3qoo1TyVN66v0DSPDadYEIp_AKur3Lk</recordid><startdate>201007</startdate><enddate>201007</enddate><creator>Broadbent, S.E</creator><creator>Davies, M.R</creator><creator>van der Woude, M.W</creator><general>Oxford, UK : Blackwell Publishing Ltd</general><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>FBQ</scope><scope>24P</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>201007</creationdate><title>Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism</title><author>Broadbent, S.E ; Davies, M.R ; van der Woude, M.W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6183-d77a4ef83687730e74979ba0954763f3cc41b8f9408aabdffe85073767f3bb4e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Antigens</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Bacteriophage P22</topic><topic>Base Sequence</topic><topic>Biological and medical sciences</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA Methylation</topic><topic>DNA, Bacterial - metabolism</topic><topic>Epigenesis, Genetic</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genes</topic><topic>Glycosyltransferases - genetics</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>Molecular Sequence Data</topic><topic>Multigene Family</topic><topic>Mutagenesis, Site-Directed</topic><topic>O Antigens - metabolism</topic><topic>Operon</topic><topic>Phage P22</topic><topic>Promoter Regions, Genetic</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>Salmonella</topic><topic>Salmonella typhimurium - genetics</topic><topic>Salmonella typhimurium - metabolism</topic><topic>Salmonella typhimurium - virology</topic><topic>Sequence Analysis, DNA</topic><topic>Site-Specific DNA-Methyltransferase (Adenine-Specific) - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Broadbent, S.E</creatorcontrib><creatorcontrib>Davies, M.R</creatorcontrib><creatorcontrib>van der Woude, M.W</creatorcontrib><collection>AGRIS</collection><collection>Wiley Online Library Open Access</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Broadbent, S.E</au><au>Davies, M.R</au><au>van der Woude, M.W</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2010-07</date><risdate>2010</risdate><volume>77</volume><issue>2</issue><spage>337</spage><epage>353</epage><pages>337-353</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>The O-antigen of Salmonella lipopolysaccharide is a major antigenic determinant and its chemical composition forms the basis for Salmonella serotyping. Modifications of the O-antigen that can affect the serotype include those carried out by the products of glycosyltransferase operons (gtr), which are present on specific Salmonella and phage genomes. Here we show that expression of the gtr genes encoded by phage P22 that confers the O1 serotype is under the control of phase variation. This phase variation occurs by a novel epigenetic mechanism requiring OxyR in conjunction with the DNA methyltransferase Dam. OxyR is an activator or a repressor of the system depending on which of its two binding sites in the gtr regulatory region is occupied. Binding is decreased by methylation at Dam target sequences in either site, and this confers heritability of the expression state to the system. Most Salmonella gtr operons share the key regulatory elements that are identified here as essential for this epigenetic phase variation.</abstract><cop>Oxford, UK</cop><pub>Oxford, UK : Blackwell Publishing Ltd</pub><pmid>20487280</pmid><doi>10.1111/j.1365-2958.2010.07203.x</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Molecular microbiology, 2010-07, Vol.77 (2), p.337-353 |
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| subjects | Antigens Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Bacteriophage P22 Base Sequence Biological and medical sciences Deoxyribonucleic acid DNA DNA Methylation DNA, Bacterial - metabolism Epigenesis, Genetic Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Regulation, Bacterial Genes Glycosyltransferases - genetics Microbiology Miscellaneous Molecular Sequence Data Multigene Family Mutagenesis, Site-Directed O Antigens - metabolism Operon Phage P22 Promoter Regions, Genetic Repressor Proteins - genetics Repressor Proteins - metabolism Salmonella Salmonella typhimurium - genetics Salmonella typhimurium - metabolism Salmonella typhimurium - virology Sequence Analysis, DNA Site-Specific DNA-Methyltransferase (Adenine-Specific) - metabolism |
| title | Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism |
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