Integrating conjugative elements of the SXT/R391 family from fish-isolated Vibrios encode restriction–modification systems that confer resistance to bacteriophages
Abstract Integrating conjugative elements (ICEs) of the SXT/R391 family have been described in Vibrios, mainly Vibrio cholerae, and other bacteria as carriers of variable gene content conferring adaptive advantages upon their hosts, including antimicrobial resistance and motility regulation. However...
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| Veröffentlicht in: | FEMS microbiology ecology 2013-02, Vol.83 (2), p.457-467 |
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| creator | Miguel, Balado Manuel L., Lemos Carlos R., Osorio |
| description | Abstract
Integrating conjugative elements (ICEs) of the SXT/R391 family have been described in Vibrios, mainly Vibrio cholerae, and other bacteria as carriers of variable gene content conferring adaptive advantages upon their hosts, including antimicrobial resistance and motility regulation. However, our knowledge on their host range and ecological significance is still limited. Here, we report the identification and characterization of ICEVspPor3 and ICEValSpa1, two novel ICEs of the SXT/R391 family from fish-isolated Vibrio splendidus and Vibrio alginolyticus, respectively. We found that ICEVspPor3 carries tetracycline and HgCl2 resistance determinants and can be transferred by conjugation to Escherichia coli and to several species of marine bacteria including some of the major bacterial fish pathogens in marine aquaculture, whereas ICEValSpa1 lacks resistance genes. Interestingly, both ICEs harbor genes encoding distinct restriction–modification (RM) systems. We demonstrate here that these RM systems, when expressed in E. coli, confer protection to infection by T1 bacteriophage and by environmental water bacteriophages. Our results provide evidences that the variable gene content of ICEs of the SXT/R391 family encodes fitness functions beyond those related to antimicrobial resistance and motility regulation and suggest that the host range of these elements in the marine environment might be broader than expected. |
| doi_str_mv | 10.1111/1574-6941.12007 |
| format | Article |
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Integrating conjugative elements (ICEs) of the SXT/R391 family have been described in Vibrios, mainly Vibrio cholerae, and other bacteria as carriers of variable gene content conferring adaptive advantages upon their hosts, including antimicrobial resistance and motility regulation. However, our knowledge on their host range and ecological significance is still limited. Here, we report the identification and characterization of ICEVspPor3 and ICEValSpa1, two novel ICEs of the SXT/R391 family from fish-isolated Vibrio splendidus and Vibrio alginolyticus, respectively. We found that ICEVspPor3 carries tetracycline and HgCl2 resistance determinants and can be transferred by conjugation to Escherichia coli and to several species of marine bacteria including some of the major bacterial fish pathogens in marine aquaculture, whereas ICEValSpa1 lacks resistance genes. Interestingly, both ICEs harbor genes encoding distinct restriction–modification (RM) systems. We demonstrate here that these RM systems, when expressed in E. coli, confer protection to infection by T1 bacteriophage and by environmental water bacteriophages. Our results provide evidences that the variable gene content of ICEs of the SXT/R391 family encodes fitness functions beyond those related to antimicrobial resistance and motility regulation and suggest that the host range of these elements in the marine environment might be broader than expected.</description><identifier>ISSN: 0168-6496</identifier><identifier>EISSN: 1574-6941</identifier><identifier>DOI: 10.1111/1574-6941.12007</identifier><identifier>PMID: 22974320</identifier><identifier>CODEN: FMECEZ</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Animals ; bacteriophage ; Bacteriophages - physiology ; conjugation ; Conjugation, Genetic ; DNA Restriction-Modification Enzymes - genetics ; Drug Resistance, Bacterial ; E coli ; Ecology ; Escherichia coli ; Escherichia coli - genetics ; Escherichia coli - virology ; Fishes - microbiology ; Gammaproteobacteria - drug effects ; Gammaproteobacteria - genetics ; Genes, Bacterial ; Harbors ; integrative conjugative element ; Interspersed Repetitive Sequences ; Marine aquaculture ; Marine environment ; Marine fish ; Microbiology ; Molecular Sequence Data ; restriction–modification ; Vibrio ; Vibrio - genetics ; Vibrio - isolation & purification ; Vibrio alginolyticus ; Vibrio cholerae ; Vibrio cholerae - genetics ; Vibrio splendidus</subject><ispartof>FEMS microbiology ecology, 2013-02, Vol.83 (2), p.457-467</ispartof><rights>2012 Federation of European Microbiological Societies 2012</rights><rights>2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved</rights><rights>2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.</rights><rights>Copyright © 2013 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4397-4b0421a4d93e08f87b420098017cc7013b6e21f79287f941b8f540efbfa37ac33</citedby><cites>FETCH-LOGICAL-c4397-4b0421a4d93e08f87b420098017cc7013b6e21f79287f941b8f540efbfa37ac33</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%2F1574-6941.12007$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1574-6941.12007$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,778,782,1414,27907,27908,45557,45558</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22974320$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Miguel, Balado</creatorcontrib><creatorcontrib>Manuel L., Lemos</creatorcontrib><creatorcontrib>Carlos R., Osorio</creatorcontrib><title>Integrating conjugative elements of the SXT/R391 family from fish-isolated Vibrios encode restriction–modification systems that confer resistance to bacteriophages</title><title>FEMS microbiology ecology</title><addtitle>FEMS Microbiol Ecol</addtitle><description>Abstract
Integrating conjugative elements (ICEs) of the SXT/R391 family have been described in Vibrios, mainly Vibrio cholerae, and other bacteria as carriers of variable gene content conferring adaptive advantages upon their hosts, including antimicrobial resistance and motility regulation. However, our knowledge on their host range and ecological significance is still limited. Here, we report the identification and characterization of ICEVspPor3 and ICEValSpa1, two novel ICEs of the SXT/R391 family from fish-isolated Vibrio splendidus and Vibrio alginolyticus, respectively. We found that ICEVspPor3 carries tetracycline and HgCl2 resistance determinants and can be transferred by conjugation to Escherichia coli and to several species of marine bacteria including some of the major bacterial fish pathogens in marine aquaculture, whereas ICEValSpa1 lacks resistance genes. Interestingly, both ICEs harbor genes encoding distinct restriction–modification (RM) systems. We demonstrate here that these RM systems, when expressed in E. coli, confer protection to infection by T1 bacteriophage and by environmental water bacteriophages. Our results provide evidences that the variable gene content of ICEs of the SXT/R391 family encodes fitness functions beyond those related to antimicrobial resistance and motility regulation and suggest that the host range of these elements in the marine environment might be broader than expected.</description><subject>Animals</subject><subject>bacteriophage</subject><subject>Bacteriophages - physiology</subject><subject>conjugation</subject><subject>Conjugation, Genetic</subject><subject>DNA Restriction-Modification Enzymes - genetics</subject><subject>Drug Resistance, Bacterial</subject><subject>E coli</subject><subject>Ecology</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - virology</subject><subject>Fishes - microbiology</subject><subject>Gammaproteobacteria - drug effects</subject><subject>Gammaproteobacteria - genetics</subject><subject>Genes, Bacterial</subject><subject>Harbors</subject><subject>integrative conjugative element</subject><subject>Interspersed Repetitive Sequences</subject><subject>Marine aquaculture</subject><subject>Marine environment</subject><subject>Marine fish</subject><subject>Microbiology</subject><subject>Molecular Sequence Data</subject><subject>restriction–modification</subject><subject>Vibrio</subject><subject>Vibrio - genetics</subject><subject>Vibrio - isolation & purification</subject><subject>Vibrio alginolyticus</subject><subject>Vibrio cholerae</subject><subject>Vibrio cholerae - genetics</subject><subject>Vibrio splendidus</subject><issn>0168-6496</issn><issn>1574-6941</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkd9qFDEUxoModq1eeycBb0SYbv7NZOZSSquFilCreBcymZPdLDOTNckoe-c7-Ay-WJ-kGbctRQTNTf7w-75zcj6EnlNyRPNa0lKKomoEPaKMEPkALe5eHqIFoVVdVKKpDtCTGDeE0JIL8hgdMNZIwRlZoF9nY4JV0MmNK2z8uJlW-fwNMPQwwJgi9hanNeCPXy6XF7yh2OrB9Ttsgx-wdXFduOh7naDDn10bnI8YRuM7wAFiCs4k58erHz8H3znrjJ6vOO5igiFmY53mqhbCjLuY9GgAJ49bbRJkt-1aryA-RY-s7iM8u9kP0afTk8vjd8X5h7dnx2_OCyN4IwvREsGoFl3DgdS2lq3IU2lqQqUxklDeVsColQ2rpc0jamtbCgK2tZpLbTg_RK_2vtvgv065fzW4aKDv9Qh-iooyyTnhtJL_g2a44oxm9OUf6MZPYcwfyVRV1bwUZZ2p5Z4ywccYwKptcIMOO0WJmsNWc7Rqjlb9DjsrXtz4Tu0A3R1_m24Gyj3w3fWw-5efOj15f2v8eq_z0_avquJeF9feHsJm</recordid><startdate>20130201</startdate><enddate>20130201</enddate><creator>Miguel, Balado</creator><creator>Manuel L., Lemos</creator><creator>Carlos R., Osorio</creator><general>Blackwell Publishing Ltd</general><general>Oxford University Press</general><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>7SN</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7TN</scope><scope>7U9</scope><scope>F1W</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>H98</scope><scope>L.G</scope><scope>7X8</scope></search><sort><creationdate>20130201</creationdate><title>Integrating conjugative elements of the SXT/R391 family from fish-isolated Vibrios encode restriction–modification systems that confer resistance to bacteriophages</title><author>Miguel, Balado ; Manuel L., Lemos ; Carlos R., Osorio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4397-4b0421a4d93e08f87b420098017cc7013b6e21f79287f941b8f540efbfa37ac33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>bacteriophage</topic><topic>Bacteriophages - physiology</topic><topic>conjugation</topic><topic>Conjugation, Genetic</topic><topic>DNA Restriction-Modification Enzymes - genetics</topic><topic>Drug Resistance, Bacterial</topic><topic>E coli</topic><topic>Ecology</topic><topic>Escherichia coli</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - virology</topic><topic>Fishes - microbiology</topic><topic>Gammaproteobacteria - drug effects</topic><topic>Gammaproteobacteria - genetics</topic><topic>Genes, Bacterial</topic><topic>Harbors</topic><topic>integrative conjugative element</topic><topic>Interspersed Repetitive Sequences</topic><topic>Marine aquaculture</topic><topic>Marine environment</topic><topic>Marine fish</topic><topic>Microbiology</topic><topic>Molecular Sequence Data</topic><topic>restriction–modification</topic><topic>Vibrio</topic><topic>Vibrio - genetics</topic><topic>Vibrio - isolation & purification</topic><topic>Vibrio alginolyticus</topic><topic>Vibrio cholerae</topic><topic>Vibrio cholerae - genetics</topic><topic>Vibrio splendidus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Miguel, Balado</creatorcontrib><creatorcontrib>Manuel L., Lemos</creatorcontrib><creatorcontrib>Carlos R., Osorio</creatorcontrib><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>Ecology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>AIDS and Cancer Research 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) Aquaculture Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>MEDLINE - Academic</collection><jtitle>FEMS microbiology ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Miguel, Balado</au><au>Manuel L., Lemos</au><au>Carlos R., Osorio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Integrating conjugative elements of the SXT/R391 family from fish-isolated Vibrios encode restriction–modification systems that confer resistance to bacteriophages</atitle><jtitle>FEMS microbiology ecology</jtitle><addtitle>FEMS Microbiol Ecol</addtitle><date>2013-02-01</date><risdate>2013</risdate><volume>83</volume><issue>2</issue><spage>457</spage><epage>467</epage><pages>457-467</pages><issn>0168-6496</issn><eissn>1574-6941</eissn><coden>FMECEZ</coden><abstract>Abstract
Integrating conjugative elements (ICEs) of the SXT/R391 family have been described in Vibrios, mainly Vibrio cholerae, and other bacteria as carriers of variable gene content conferring adaptive advantages upon their hosts, including antimicrobial resistance and motility regulation. However, our knowledge on their host range and ecological significance is still limited. Here, we report the identification and characterization of ICEVspPor3 and ICEValSpa1, two novel ICEs of the SXT/R391 family from fish-isolated Vibrio splendidus and Vibrio alginolyticus, respectively. We found that ICEVspPor3 carries tetracycline and HgCl2 resistance determinants and can be transferred by conjugation to Escherichia coli and to several species of marine bacteria including some of the major bacterial fish pathogens in marine aquaculture, whereas ICEValSpa1 lacks resistance genes. Interestingly, both ICEs harbor genes encoding distinct restriction–modification (RM) systems. We demonstrate here that these RM systems, when expressed in E. coli, confer protection to infection by T1 bacteriophage and by environmental water bacteriophages. Our results provide evidences that the variable gene content of ICEs of the SXT/R391 family encodes fitness functions beyond those related to antimicrobial resistance and motility regulation and suggest that the host range of these elements in the marine environment might be broader than expected.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>22974320</pmid><doi>10.1111/1574-6941.12007</doi><tpages>11</tpages></addata></record> |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Oxford Journals Open Access Collection |
| subjects | Animals bacteriophage Bacteriophages - physiology conjugation Conjugation, Genetic DNA Restriction-Modification Enzymes - genetics Drug Resistance, Bacterial E coli Ecology Escherichia coli Escherichia coli - genetics Escherichia coli - virology Fishes - microbiology Gammaproteobacteria - drug effects Gammaproteobacteria - genetics Genes, Bacterial Harbors integrative conjugative element Interspersed Repetitive Sequences Marine aquaculture Marine environment Marine fish Microbiology Molecular Sequence Data restriction–modification Vibrio Vibrio - genetics Vibrio - isolation & purification Vibrio alginolyticus Vibrio cholerae Vibrio cholerae - genetics Vibrio splendidus |
| title | Integrating conjugative elements of the SXT/R391 family from fish-isolated Vibrios encode restriction–modification systems that confer resistance to bacteriophages |
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