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Pasteurella multocida Heddleston Serovar 3 and 4 Strains Share a Common Lipopolysaccharide Biosynthesis Locus but Display both Inter- and Intrastrain Lipopolysaccharide Heterogeneity
Pasteurella multocida is a Gram-negative multispecies pathogen and the causative agent of fowl cholera, a serious disease of poultry which can present in both acute and chronic forms. The major outer membrane component lipopolysaccharide (LPS) is both an important virulence factor and a major immuno...
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Published in: | Journal of Bacteriology 2013-11, Vol.195 (21), p.4854-4864 |
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description | Pasteurella multocida is a Gram-negative multispecies pathogen and the causative agent of fowl cholera, a serious disease of poultry which can present in both acute and chronic forms. The major outer membrane component lipopolysaccharide (LPS) is both an important virulence factor and a major immunogen. Our previous studies determined the LPS structures expressed by different P. multocida strains and revealed that a number of strains belonging to different serovars contain the same LPS biosynthesis locus but express different LPS structures due to mutations within glycosyltransferase genes. In this study, we report the full LPS structure of the serovar 4 type strain, P1662, and reveal that it shares the same LPS outer core biosynthesis locus, L3, with the serovar 3 strains P1059 and Pm70. Using directed mutagenesis, the role of each glycosyltransferase gene in LPS outer core assembly was determined. LPS structural analysis of 23 Australian field isolates that contain the L3 locus revealed that at least six different LPS outer core structures can be produced as a result of mutations within the LPS glycosyltransferase genes. Moreover, some field isolates produce multiple but related LPS glycoforms simultaneously, and three LPS outer core structures are remarkably similar to the globo series of vertebrate glycosphingolipids. Our in-depth analysis showing the genetics and full range of P. multocida lipopolysaccharide structures will facilitate the improvement of typing systems and the prediction of the protective efficacy of vaccines. |
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The major outer membrane component lipopolysaccharide (LPS) is both an important virulence factor and a major immunogen. Our previous studies determined the LPS structures expressed by different P. multocida strains and revealed that a number of strains belonging to different serovars contain the same LPS biosynthesis locus but express different LPS structures due to mutations within glycosyltransferase genes. In this study, we report the full LPS structure of the serovar 4 type strain, P1662, and reveal that it shares the same LPS outer core biosynthesis locus, L3, with the serovar 3 strains P1059 and Pm70. Using directed mutagenesis, the role of each glycosyltransferase gene in LPS outer core assembly was determined. LPS structural analysis of 23 Australian field isolates that contain the L3 locus revealed that at least six different LPS outer core structures can be produced as a result of mutations within the LPS glycosyltransferase genes. Moreover, some field isolates produce multiple but related LPS glycoforms simultaneously, and three LPS outer core structures are remarkably similar to the globo series of vertebrate glycosphingolipids. Our in-depth analysis showing the genetics and full range of P. multocida lipopolysaccharide structures will facilitate the improvement of typing systems and the prediction of the protective efficacy of vaccines.</description><identifier>ISSN: 0021-9193</identifier><identifier>EISSN: 1067-8832</identifier><identifier>EISSN: 1098-5530</identifier><identifier>DOI: 10.1128/JB.00779-13</identifier><identifier>PMID: 23974032</identifier><identifier>CODEN: JOBAAY</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Amino Acid Sequence ; antigens ; Bacteriology ; Biosynthesis ; Cholera ; fowl cholera ; Gene expression ; Gene Expression Regulation, Bacterial - physiology ; genes ; Genetic Variation ; glycosphingolipids ; Gram-negative bacteria ; lipopolysaccharides ; Lipopolysaccharides - biosynthesis ; Lipopolysaccharides - genetics ; loci ; Membranes ; Molecular Sequence Data ; mutagenesis ; Mutation ; Pasteurella multocida ; Pasteurella multocida - classification ; Pasteurella multocida - genetics ; Pasteurella multocida - metabolism ; pathogens ; prediction ; serotypes ; Vaccines ; vertebrates ; virulence</subject><ispartof>Journal of Bacteriology, 2013-11, Vol.195 (21), p.4854-4864</ispartof><rights>Copyright American Society for Microbiology Nov 2013</rights><rights>Copyright © 2013, American Society for Microbiology. All Rights Reserved. 2013 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c493t-99676caeb9ba6e94c7da96006731bbee9d6e396c5c188d98bbea6cdeb7806cac3</citedby><cites>FETCH-LOGICAL-c493t-99676caeb9ba6e94c7da96006731bbee9d6e396c5c188d98bbea6cdeb7806cac3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3807493/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3807493/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,3189,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23974032$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Harper, Marina</creatorcontrib><creatorcontrib>St. Michael, Frank</creatorcontrib><creatorcontrib>John, Marietta</creatorcontrib><creatorcontrib>Vinogradov, Evgeny</creatorcontrib><creatorcontrib>Steen, Jennifer A</creatorcontrib><creatorcontrib>van Dorsten, Lieke</creatorcontrib><creatorcontrib>Steen, Jason A</creatorcontrib><creatorcontrib>Turni, Conny</creatorcontrib><creatorcontrib>Blackall, Patrick J</creatorcontrib><creatorcontrib>Adler, Ben</creatorcontrib><creatorcontrib>Cox, Andrew D</creatorcontrib><creatorcontrib>Boyce, John D</creatorcontrib><title>Pasteurella multocida Heddleston Serovar 3 and 4 Strains Share a Common Lipopolysaccharide Biosynthesis Locus but Display both Inter- and Intrastrain Lipopolysaccharide Heterogeneity</title><title>Journal of Bacteriology</title><addtitle>J Bacteriol</addtitle><description>Pasteurella multocida is a Gram-negative multispecies pathogen and the causative agent of fowl cholera, a serious disease of poultry which can present in both acute and chronic forms. The major outer membrane component lipopolysaccharide (LPS) is both an important virulence factor and a major immunogen. Our previous studies determined the LPS structures expressed by different P. multocida strains and revealed that a number of strains belonging to different serovars contain the same LPS biosynthesis locus but express different LPS structures due to mutations within glycosyltransferase genes. In this study, we report the full LPS structure of the serovar 4 type strain, P1662, and reveal that it shares the same LPS outer core biosynthesis locus, L3, with the serovar 3 strains P1059 and Pm70. Using directed mutagenesis, the role of each glycosyltransferase gene in LPS outer core assembly was determined. LPS structural analysis of 23 Australian field isolates that contain the L3 locus revealed that at least six different LPS outer core structures can be produced as a result of mutations within the LPS glycosyltransferase genes. Moreover, some field isolates produce multiple but related LPS glycoforms simultaneously, and three LPS outer core structures are remarkably similar to the globo series of vertebrate glycosphingolipids. Our in-depth analysis showing the genetics and full range of P. multocida lipopolysaccharide structures will facilitate the improvement of typing systems and the prediction of the protective efficacy of vaccines.</description><subject>Amino Acid Sequence</subject><subject>antigens</subject><subject>Bacteriology</subject><subject>Biosynthesis</subject><subject>Cholera</subject><subject>fowl cholera</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Bacterial - physiology</subject><subject>genes</subject><subject>Genetic Variation</subject><subject>glycosphingolipids</subject><subject>Gram-negative bacteria</subject><subject>lipopolysaccharides</subject><subject>Lipopolysaccharides - biosynthesis</subject><subject>Lipopolysaccharides - genetics</subject><subject>loci</subject><subject>Membranes</subject><subject>Molecular Sequence Data</subject><subject>mutagenesis</subject><subject>Mutation</subject><subject>Pasteurella multocida</subject><subject>Pasteurella multocida - classification</subject><subject>Pasteurella multocida - genetics</subject><subject>Pasteurella multocida - metabolism</subject><subject>pathogens</subject><subject>prediction</subject><subject>serotypes</subject><subject>Vaccines</subject><subject>vertebrates</subject><subject>virulence</subject><issn>0021-9193</issn><issn>1067-8832</issn><issn>1098-5530</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNptkstu1DAYhSMEotPCij1YsEFCKb4lsTdIzHCZViOBNHRtOc4_E4-SOLWTVnkxng-nUypArGzZn4-Pj0-SvCD4nBAq3l8uzzEuCpkS9ihZEJwXqRCMPk4WGFOSSiLZSXIawgFjwnlGnyYnlMmCY0YXyc_vOgwwemgajdqxGZyxlUZrqKoGwuA6tAXvbrRHDOmuQhxtB69tF9C21h6QRivXthHb2N71rpmCNibu2ArQ0rowdUMNwQa0cWYMqBwH9MmGvtETKt1Qo4tuAJ_eScepj2Zm9f-prSGSbg8d2GF6ljzZ6SbA8_vxLLn68vnHap1uvn29WH3cpIZLNqRS5kVuNJSy1DlIbopKyxzHiBgpSwBZ5cBkbjJDhKikiGs6NxWUhcDxnGFnyYejbj-WLVQGZo-N6r1ttZ-U01b9vdPZWu3djWICF9FCFHh7L-Dd9RgTVa0NZk67AzcGFX9EUJrxDEf0zT_owY2-i8-bKSqI4JxE6t2RMt6F4GH3YIZgNfdBXS7VXR8Uma9_-af_B_Z3ASLw-gjUdl_fWg9Kh1YdSkVkpihRXGQ8Qq-O0E47pffeBnW1pZhkc6PymCf7BXQjygg</recordid><startdate>20131101</startdate><enddate>20131101</enddate><creator>Harper, Marina</creator><creator>St. Michael, Frank</creator><creator>John, Marietta</creator><creator>Vinogradov, Evgeny</creator><creator>Steen, Jennifer A</creator><creator>van Dorsten, Lieke</creator><creator>Steen, Jason A</creator><creator>Turni, Conny</creator><creator>Blackall, Patrick J</creator><creator>Adler, Ben</creator><creator>Cox, Andrew D</creator><creator>Boyce, John D</creator><general>American Society for Microbiology</general><scope>FBQ</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>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>F1W</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20131101</creationdate><title>Pasteurella multocida Heddleston Serovar 3 and 4 Strains Share a Common Lipopolysaccharide Biosynthesis Locus but Display both Inter- and Intrastrain Lipopolysaccharide Heterogeneity</title><author>Harper, Marina ; St. Michael, Frank ; John, Marietta ; Vinogradov, Evgeny ; Steen, Jennifer A ; van Dorsten, Lieke ; Steen, Jason A ; Turni, Conny ; Blackall, Patrick J ; Adler, Ben ; Cox, Andrew D ; Boyce, John D</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c493t-99676caeb9ba6e94c7da96006731bbee9d6e396c5c188d98bbea6cdeb7806cac3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amino Acid Sequence</topic><topic>antigens</topic><topic>Bacteriology</topic><topic>Biosynthesis</topic><topic>Cholera</topic><topic>fowl cholera</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Bacterial - physiology</topic><topic>genes</topic><topic>Genetic Variation</topic><topic>glycosphingolipids</topic><topic>Gram-negative bacteria</topic><topic>lipopolysaccharides</topic><topic>Lipopolysaccharides - biosynthesis</topic><topic>Lipopolysaccharides - genetics</topic><topic>loci</topic><topic>Membranes</topic><topic>Molecular Sequence Data</topic><topic>mutagenesis</topic><topic>Mutation</topic><topic>Pasteurella multocida</topic><topic>Pasteurella multocida - classification</topic><topic>Pasteurella multocida - genetics</topic><topic>Pasteurella multocida - metabolism</topic><topic>pathogens</topic><topic>prediction</topic><topic>serotypes</topic><topic>Vaccines</topic><topic>vertebrates</topic><topic>virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Harper, Marina</creatorcontrib><creatorcontrib>St. Michael, Frank</creatorcontrib><creatorcontrib>John, Marietta</creatorcontrib><creatorcontrib>Vinogradov, Evgeny</creatorcontrib><creatorcontrib>Steen, Jennifer A</creatorcontrib><creatorcontrib>van Dorsten, Lieke</creatorcontrib><creatorcontrib>Steen, Jason A</creatorcontrib><creatorcontrib>Turni, Conny</creatorcontrib><creatorcontrib>Blackall, Patrick J</creatorcontrib><creatorcontrib>Adler, Ben</creatorcontrib><creatorcontrib>Cox, Andrew D</creatorcontrib><creatorcontrib>Boyce, John D</creatorcontrib><collection>AGRIS</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>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>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of Bacteriology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Harper, Marina</au><au>St. Michael, Frank</au><au>John, Marietta</au><au>Vinogradov, Evgeny</au><au>Steen, Jennifer A</au><au>van Dorsten, Lieke</au><au>Steen, Jason A</au><au>Turni, Conny</au><au>Blackall, Patrick J</au><au>Adler, Ben</au><au>Cox, Andrew D</au><au>Boyce, John D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pasteurella multocida Heddleston Serovar 3 and 4 Strains Share a Common Lipopolysaccharide Biosynthesis Locus but Display both Inter- and Intrastrain Lipopolysaccharide Heterogeneity</atitle><jtitle>Journal of Bacteriology</jtitle><addtitle>J Bacteriol</addtitle><date>2013-11-01</date><risdate>2013</risdate><volume>195</volume><issue>21</issue><spage>4854</spage><epage>4864</epage><pages>4854-4864</pages><issn>0021-9193</issn><eissn>1067-8832</eissn><eissn>1098-5530</eissn><coden>JOBAAY</coden><abstract>Pasteurella multocida is a Gram-negative multispecies pathogen and the causative agent of fowl cholera, a serious disease of poultry which can present in both acute and chronic forms. The major outer membrane component lipopolysaccharide (LPS) is both an important virulence factor and a major immunogen. Our previous studies determined the LPS structures expressed by different P. multocida strains and revealed that a number of strains belonging to different serovars contain the same LPS biosynthesis locus but express different LPS structures due to mutations within glycosyltransferase genes. In this study, we report the full LPS structure of the serovar 4 type strain, P1662, and reveal that it shares the same LPS outer core biosynthesis locus, L3, with the serovar 3 strains P1059 and Pm70. Using directed mutagenesis, the role of each glycosyltransferase gene in LPS outer core assembly was determined. LPS structural analysis of 23 Australian field isolates that contain the L3 locus revealed that at least six different LPS outer core structures can be produced as a result of mutations within the LPS glycosyltransferase genes. Moreover, some field isolates produce multiple but related LPS glycoforms simultaneously, and three LPS outer core structures are remarkably similar to the globo series of vertebrate glycosphingolipids. Our in-depth analysis showing the genetics and full range of P. multocida lipopolysaccharide structures will facilitate the improvement of typing systems and the prediction of the protective efficacy of vaccines.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>23974032</pmid><doi>10.1128/JB.00779-13</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence antigens Bacteriology Biosynthesis Cholera fowl cholera Gene expression Gene Expression Regulation, Bacterial - physiology genes Genetic Variation glycosphingolipids Gram-negative bacteria lipopolysaccharides Lipopolysaccharides - biosynthesis Lipopolysaccharides - genetics loci Membranes Molecular Sequence Data mutagenesis Mutation Pasteurella multocida Pasteurella multocida - classification Pasteurella multocida - genetics Pasteurella multocida - metabolism pathogens prediction serotypes Vaccines vertebrates virulence |
title | Pasteurella multocida Heddleston Serovar 3 and 4 Strains Share a Common Lipopolysaccharide Biosynthesis Locus but Display both Inter- and Intrastrain Lipopolysaccharide Heterogeneity |
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