Horizontal transfer of Yersinia high‐pathogenicity island by the conjugative RP4 attB target‐presenting shuttle plasmid
Summary The high‐pathogenicity island (HPI) encodes a highly efficient yersiniabactin system of iron acquisition responsible for mouse lethality in Yersinia. Although the HPI is widely disseminated among Enterobacteriaceae it lacks functions necessary for its replication and transmission. Therefore,...
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Veröffentlicht in: | Molecular microbiology 2005-08, Vol.57 (3), p.727-734 |
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description | Summary
The high‐pathogenicity island (HPI) encodes a highly efficient yersiniabactin system of iron acquisition responsible for mouse lethality in Yersinia. Although the HPI is widely disseminated among Enterobacteriaceae it lacks functions necessary for its replication and transmission. Therefore, the mechanism of its horizontal transfer and circulation is completely obscure. On the other hand, the HPI is a genetically active island in the bacterial cell. It encodes a functional recombinase and is able to transpose to new targets on the chromosome. Here we report on a possible mechanism of the HPI dissemination based on site‐specific recombination of the excised HPI with the attB‐presenting (asn tRNA gene) RP4 promiscuous conjugative shuttle plasmid. The resulting cointegrate can be transferred by conjugation to a new host, where it dissociates, and the released HPI integrates into any unoccupied asn tRNA gene target in the genome. This mechanism has been proven both with the ‘mini’ island carrying only the attP recognition site and genes coding for recombination enzymes and with the complete HPI labelled with an antibiotic resistance marker. After acquisition of the mobilized complete form of the HPI, the ability of the HPI‐cured Yersinia enterocolitica WA‐TH– strain to produce yersiniabactin has been restored. Such ‘trapping’ of pathogenicity islands and subsequent shuffling to new hosts by a conjugative replicon carrying a suitable attB site could be applied to other functional integrative elements and explain wide dissemination of PAIs. |
doi_str_mv | 10.1111/j.1365-2958.2005.04722.x |
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The high‐pathogenicity island (HPI) encodes a highly efficient yersiniabactin system of iron acquisition responsible for mouse lethality in Yersinia. Although the HPI is widely disseminated among Enterobacteriaceae it lacks functions necessary for its replication and transmission. Therefore, the mechanism of its horizontal transfer and circulation is completely obscure. On the other hand, the HPI is a genetically active island in the bacterial cell. It encodes a functional recombinase and is able to transpose to new targets on the chromosome. Here we report on a possible mechanism of the HPI dissemination based on site‐specific recombination of the excised HPI with the attB‐presenting (asn tRNA gene) RP4 promiscuous conjugative shuttle plasmid. The resulting cointegrate can be transferred by conjugation to a new host, where it dissociates, and the released HPI integrates into any unoccupied asn tRNA gene target in the genome. This mechanism has been proven both with the ‘mini’ island carrying only the attP recognition site and genes coding for recombination enzymes and with the complete HPI labelled with an antibiotic resistance marker. After acquisition of the mobilized complete form of the HPI, the ability of the HPI‐cured Yersinia enterocolitica WA‐TH– strain to produce yersiniabactin has been restored. Such ‘trapping’ of pathogenicity islands and subsequent shuffling to new hosts by a conjugative replicon carrying a suitable attB site could be applied to other functional integrative elements and explain wide dissemination of PAIs.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2005.04722.x</identifier><identifier>PMID: 16045617</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Science Ltd</publisher><subject>Bacteriology ; Biological and medical sciences ; Conjugation, Genetic ; Enzymes ; Fundamental and applied biological sciences. Psychology ; Gene Transfer, Horizontal ; Genetic recombination ; Genetic Vectors ; Genomic Islands - genetics ; Genomics ; Microbiology ; Miscellaneous ; Pathogens ; Phenols - metabolism ; Plasmids - genetics ; Recombination, Genetic ; Thiazoles - metabolism ; Yersinia enterocolitica - genetics ; Yersinia enterocolitica - growth & development ; Yersinia enterocolitica - metabolism ; Yersinia pseudotuberculosis - genetics ; Yersinia pseudotuberculosis - growth & development ; Yersinia pseudotuberculosis - metabolism</subject><ispartof>Molecular microbiology, 2005-08, Vol.57 (3), p.727-734</ispartof><rights>2005 INIST-CNRS</rights><rights>Copyright Blackwell Publishing Aug 2005</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5052-754188501327c686e3e2896b321422f4d6c29103dfe0ab579ea5038be8ce4e033</citedby><cites>FETCH-LOGICAL-c5052-754188501327c686e3e2896b321422f4d6c29103dfe0ab579ea5038be8ce4e033</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1365-2958.2005.04722.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-2958.2005.04722.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=16935675$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16045617$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Antonenka, Uladzimir</creatorcontrib><creatorcontrib>Nölting, Christina</creatorcontrib><creatorcontrib>Heesemann, Jürgen</creatorcontrib><creatorcontrib>Rakin, Alexander</creatorcontrib><title>Horizontal transfer of Yersinia high‐pathogenicity island by the conjugative RP4 attB target‐presenting shuttle plasmid</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
The high‐pathogenicity island (HPI) encodes a highly efficient yersiniabactin system of iron acquisition responsible for mouse lethality in Yersinia. Although the HPI is widely disseminated among Enterobacteriaceae it lacks functions necessary for its replication and transmission. Therefore, the mechanism of its horizontal transfer and circulation is completely obscure. On the other hand, the HPI is a genetically active island in the bacterial cell. It encodes a functional recombinase and is able to transpose to new targets on the chromosome. Here we report on a possible mechanism of the HPI dissemination based on site‐specific recombination of the excised HPI with the attB‐presenting (asn tRNA gene) RP4 promiscuous conjugative shuttle plasmid. The resulting cointegrate can be transferred by conjugation to a new host, where it dissociates, and the released HPI integrates into any unoccupied asn tRNA gene target in the genome. This mechanism has been proven both with the ‘mini’ island carrying only the attP recognition site and genes coding for recombination enzymes and with the complete HPI labelled with an antibiotic resistance marker. After acquisition of the mobilized complete form of the HPI, the ability of the HPI‐cured Yersinia enterocolitica WA‐TH– strain to produce yersiniabactin has been restored. Such ‘trapping’ of pathogenicity islands and subsequent shuffling to new hosts by a conjugative replicon carrying a suitable attB site could be applied to other functional integrative elements and explain wide dissemination of PAIs.</description><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>Conjugation, Genetic</subject><subject>Enzymes</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Transfer, Horizontal</subject><subject>Genetic recombination</subject><subject>Genetic Vectors</subject><subject>Genomic Islands - genetics</subject><subject>Genomics</subject><subject>Microbiology</subject><subject>Miscellaneous</subject><subject>Pathogens</subject><subject>Phenols - metabolism</subject><subject>Plasmids - genetics</subject><subject>Recombination, Genetic</subject><subject>Thiazoles - metabolism</subject><subject>Yersinia enterocolitica - genetics</subject><subject>Yersinia enterocolitica - growth & development</subject><subject>Yersinia enterocolitica - metabolism</subject><subject>Yersinia pseudotuberculosis - genetics</subject><subject>Yersinia pseudotuberculosis - growth & development</subject><subject>Yersinia pseudotuberculosis - metabolism</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkd2K1DAYhoMo7jh6CxIEPWvNT5OmBx7oou7CLooo6FFI069thk47m6S6oydegtfolZg6g4onmpME8rwf78eDEKYkp-k83uSUS5GxSqicESJyUpSM5dc30OrXx020IpUgGVfs_Qm6E8KGEMqJ5LfRCZWkEJKWK_TlbPLu8zRGM-DozRha8Hhq8QfwwY3O4N51_fev33Ym9lMHo7Mu7rELgxkbXO9x7AHbadzMnYnuI-A3rwtsYnyGo_EdxCXpIcAY3djh0M8xDoB3gwlb19xFt1ozBLh3vNfo3Yvnb0_PsotXL89Pn15kVhDBslIUVCmRyrPSSiWBA1OVrDmjBWNt0UjLKkp40wIxtSgrMIJwVYOyUADhfI0eHebu_HQ1Q4h664KFIe0A0xy0VKSspJT_BGkpOU09EvjgL3AzzX5MS2haSUHLIlFrpA6Q9VMIHlq9825r_F5ToheNeqMXW3qxpReN-qdGfZ2i94_z53oLze_g0VsCHh4BE6wZ2mTOuvAHV3EhS5G4Jwfukxtg_98F9OXl-fLiPwCtoLrB</recordid><startdate>200508</startdate><enddate>200508</enddate><creator>Antonenka, Uladzimir</creator><creator>Nölting, Christina</creator><creator>Heesemann, Jürgen</creator><creator>Rakin, Alexander</creator><general>Blackwell Science Ltd</general><general>Blackwell Science</general><general>Blackwell Publishing Ltd</general><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>7X8</scope></search><sort><creationdate>200508</creationdate><title>Horizontal transfer of Yersinia high‐pathogenicity island by the conjugative RP4 attB target‐presenting shuttle plasmid</title><author>Antonenka, Uladzimir ; Nölting, Christina ; Heesemann, Jürgen ; Rakin, Alexander</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5052-754188501327c686e3e2896b321422f4d6c29103dfe0ab579ea5038be8ce4e033</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>Conjugation, Genetic</topic><topic>Enzymes</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Transfer, Horizontal</topic><topic>Genetic recombination</topic><topic>Genetic Vectors</topic><topic>Genomic Islands - genetics</topic><topic>Genomics</topic><topic>Microbiology</topic><topic>Miscellaneous</topic><topic>Pathogens</topic><topic>Phenols - metabolism</topic><topic>Plasmids - genetics</topic><topic>Recombination, Genetic</topic><topic>Thiazoles - metabolism</topic><topic>Yersinia enterocolitica - genetics</topic><topic>Yersinia enterocolitica - growth & development</topic><topic>Yersinia enterocolitica - metabolism</topic><topic>Yersinia pseudotuberculosis - genetics</topic><topic>Yersinia pseudotuberculosis - growth & development</topic><topic>Yersinia pseudotuberculosis - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Antonenka, Uladzimir</creatorcontrib><creatorcontrib>Nölting, Christina</creatorcontrib><creatorcontrib>Heesemann, Jürgen</creatorcontrib><creatorcontrib>Rakin, Alexander</creatorcontrib><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>MEDLINE - Academic</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Antonenka, Uladzimir</au><au>Nölting, Christina</au><au>Heesemann, Jürgen</au><au>Rakin, Alexander</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Horizontal transfer of Yersinia high‐pathogenicity island by the conjugative RP4 attB target‐presenting shuttle plasmid</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2005-08</date><risdate>2005</risdate><volume>57</volume><issue>3</issue><spage>727</spage><epage>734</epage><pages>727-734</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
The high‐pathogenicity island (HPI) encodes a highly efficient yersiniabactin system of iron acquisition responsible for mouse lethality in Yersinia. Although the HPI is widely disseminated among Enterobacteriaceae it lacks functions necessary for its replication and transmission. Therefore, the mechanism of its horizontal transfer and circulation is completely obscure. On the other hand, the HPI is a genetically active island in the bacterial cell. It encodes a functional recombinase and is able to transpose to new targets on the chromosome. Here we report on a possible mechanism of the HPI dissemination based on site‐specific recombination of the excised HPI with the attB‐presenting (asn tRNA gene) RP4 promiscuous conjugative shuttle plasmid. The resulting cointegrate can be transferred by conjugation to a new host, where it dissociates, and the released HPI integrates into any unoccupied asn tRNA gene target in the genome. This mechanism has been proven both with the ‘mini’ island carrying only the attP recognition site and genes coding for recombination enzymes and with the complete HPI labelled with an antibiotic resistance marker. After acquisition of the mobilized complete form of the HPI, the ability of the HPI‐cured Yersinia enterocolitica WA‐TH– strain to produce yersiniabactin has been restored. Such ‘trapping’ of pathogenicity islands and subsequent shuffling to new hosts by a conjugative replicon carrying a suitable attB site could be applied to other functional integrative elements and explain wide dissemination of PAIs.</abstract><cop>Oxford, UK</cop><pub>Blackwell Science Ltd</pub><pmid>16045617</pmid><doi>10.1111/j.1365-2958.2005.04722.x</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Bacteriology Biological and medical sciences Conjugation, Genetic Enzymes Fundamental and applied biological sciences. Psychology Gene Transfer, Horizontal Genetic recombination Genetic Vectors Genomic Islands - genetics Genomics Microbiology Miscellaneous Pathogens Phenols - metabolism Plasmids - genetics Recombination, Genetic Thiazoles - metabolism Yersinia enterocolitica - genetics Yersinia enterocolitica - growth & development Yersinia enterocolitica - metabolism Yersinia pseudotuberculosis - genetics Yersinia pseudotuberculosis - growth & development Yersinia pseudotuberculosis - metabolism |
title | Horizontal transfer of Yersinia high‐pathogenicity island by the conjugative RP4 attB target‐presenting shuttle plasmid |
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