Prevention of biofilm formation and removal of existing biofilms by extracellular DNases of Campylobacter jejuni
The fastidious nature of the foodborne bacterial pathogen Campylobacter jejuni contrasts with its ability to survive in the food chain. The formation of biofilms, or the integration into existing biofilms by C. jejuni, is thought to contribute to food chain survival. As extracellular DNA (eDNA) has...
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| description | The fastidious nature of the foodborne bacterial pathogen Campylobacter jejuni contrasts with its ability to survive in the food chain. The formation of biofilms, or the integration into existing biofilms by C. jejuni, is thought to contribute to food chain survival. As extracellular DNA (eDNA) has previously been proposed to play a role in C. jejuni biofilms, we have investigated the role of extracellular DNases (eDNases) produced by C. jejuni in biofilm formation. A search of 2791 C. jejuni genomes highlighted that almost half of C. jejuni genomes contains at least one eDNase gene, but only a minority of isolates contains two or three of these eDNase genes, such as C. jejuni strain RM1221 which contains the cje0256, cje0566 and cje1441 eDNase genes. Strain RM1221 did not form biofilms, whereas the eDNase-negative strains NCTC 11168 and 81116 did. Incubation of pre-formed biofilms of NCTC 11168 with live C. jejuni RM1221 or with spent medium from a RM1221 culture resulted in removal of the biofilm. Inactivation of the cje1441 eDNase gene in strain RM1221 restored biofilm formation, and made the mutant unable to degrade biofilms of strain NCTC 11168. Finally, C. jejuni strain RM1221 was able to degrade genomic DNA from C. jejuni NCTC 11168, 81116 and RM1221, whereas strain NCTC 11168 and the RM1221 cje1441 mutant were unable to do so. This was mirrored by an absence of eDNA in overnight cultures of C. jejuni RM1221. This suggests that the activity of eDNases in C. jejuni affects biofilm formation and is not conducive to a biofilm lifestyle. These eDNases do however have a potential role in controlling biofilm formation by C. jejuni strains in food chain relevant environments. |
| doi_str_mv | 10.1371/journal.pone.0121680 |
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The formation of biofilms, or the integration into existing biofilms by C. jejuni, is thought to contribute to food chain survival. As extracellular DNA (eDNA) has previously been proposed to play a role in C. jejuni biofilms, we have investigated the role of extracellular DNases (eDNases) produced by C. jejuni in biofilm formation. A search of 2791 C. jejuni genomes highlighted that almost half of C. jejuni genomes contains at least one eDNase gene, but only a minority of isolates contains two or three of these eDNase genes, such as C. jejuni strain RM1221 which contains the cje0256, cje0566 and cje1441 eDNase genes. Strain RM1221 did not form biofilms, whereas the eDNase-negative strains NCTC 11168 and 81116 did. Incubation of pre-formed biofilms of NCTC 11168 with live C. jejuni RM1221 or with spent medium from a RM1221 culture resulted in removal of the biofilm. Inactivation of the cje1441 eDNase gene in strain RM1221 restored biofilm formation, and made the mutant unable to degrade biofilms of strain NCTC 11168. Finally, C. jejuni strain RM1221 was able to degrade genomic DNA from C. jejuni NCTC 11168, 81116 and RM1221, whereas strain NCTC 11168 and the RM1221 cje1441 mutant were unable to do so. This was mirrored by an absence of eDNA in overnight cultures of C. jejuni RM1221. This suggests that the activity of eDNases in C. jejuni affects biofilm formation and is not conducive to a biofilm lifestyle. These eDNases do however have a potential role in controlling biofilm formation by C. jejuni strains in food chain relevant environments.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0121680</identifier><identifier>PMID: 25803828</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biofilms ; Biofilms - drug effects ; Biofilms - growth & development ; Brucella ; Campylobacter ; Campylobacter jejuni ; Campylobacter jejuni - enzymology ; Campylobacter jejuni - genetics ; Deactivation ; Deoxyribonucleases - pharmacology ; Deoxyribonucleic acid ; DNA ; DNA Primers - genetics ; Environmental DNA ; Enzymes ; Extracellular Space - genetics ; Food ; Food chains ; Food Microbiology ; Genes ; Genomes ; Genomics ; Gentian Violet ; Green Fluorescent Proteins ; Inactivation ; Indoles ; Neutrophils ; Pathogens ; Proteins ; Species Specificity ; Staphylococcus infections ; Strains (organisms)</subject><ispartof>PloS one, 2015-03, Vol.10 (3), p.e0121680-e0121680</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Brown 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>2015 Brown et al 2015 Brown et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-302d86bd619492a041c4746a3dab3f66d70e2ad5952b2e0ba43738be5f972c4c3</citedby><cites>FETCH-LOGICAL-c692t-302d86bd619492a041c4746a3dab3f66d70e2ad5952b2e0ba43738be5f972c4c3</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/PMC4372405/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4372405/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25803828$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gerlach, Roman G.</contributor><creatorcontrib>Brown, Helen L</creatorcontrib><creatorcontrib>Reuter, Mark</creatorcontrib><creatorcontrib>Hanman, Kate</creatorcontrib><creatorcontrib>Betts, Roy P</creatorcontrib><creatorcontrib>van Vliet, Arnoud H M</creatorcontrib><title>Prevention of biofilm formation and removal of existing biofilms by extracellular DNases of Campylobacter jejuni</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The fastidious nature of the foodborne bacterial pathogen Campylobacter jejuni contrasts with its ability to survive in the food chain. The formation of biofilms, or the integration into existing biofilms by C. jejuni, is thought to contribute to food chain survival. As extracellular DNA (eDNA) has previously been proposed to play a role in C. jejuni biofilms, we have investigated the role of extracellular DNases (eDNases) produced by C. jejuni in biofilm formation. A search of 2791 C. jejuni genomes highlighted that almost half of C. jejuni genomes contains at least one eDNase gene, but only a minority of isolates contains two or three of these eDNase genes, such as C. jejuni strain RM1221 which contains the cje0256, cje0566 and cje1441 eDNase genes. Strain RM1221 did not form biofilms, whereas the eDNase-negative strains NCTC 11168 and 81116 did. Incubation of pre-formed biofilms of NCTC 11168 with live C. jejuni RM1221 or with spent medium from a RM1221 culture resulted in removal of the biofilm. Inactivation of the cje1441 eDNase gene in strain RM1221 restored biofilm formation, and made the mutant unable to degrade biofilms of strain NCTC 11168. Finally, C. jejuni strain RM1221 was able to degrade genomic DNA from C. jejuni NCTC 11168, 81116 and RM1221, whereas strain NCTC 11168 and the RM1221 cje1441 mutant were unable to do so. This was mirrored by an absence of eDNA in overnight cultures of C. jejuni RM1221. This suggests that the activity of eDNases in C. jejuni affects biofilm formation and is not conducive to a biofilm lifestyle. These eDNases do however have a potential role in controlling biofilm formation by C. jejuni strains in food chain relevant environments.</description><subject>Biofilms</subject><subject>Biofilms - drug effects</subject><subject>Biofilms - growth & development</subject><subject>Brucella</subject><subject>Campylobacter</subject><subject>Campylobacter jejuni</subject><subject>Campylobacter jejuni - enzymology</subject><subject>Campylobacter jejuni - genetics</subject><subject>Deactivation</subject><subject>Deoxyribonucleases - pharmacology</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Primers - genetics</subject><subject>Environmental DNA</subject><subject>Enzymes</subject><subject>Extracellular Space - genetics</subject><subject>Food</subject><subject>Food chains</subject><subject>Food Microbiology</subject><subject>Genes</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Gentian Violet</subject><subject>Green Fluorescent Proteins</subject><subject>Inactivation</subject><subject>Indoles</subject><subject>Neutrophils</subject><subject>Pathogens</subject><subject>Proteins</subject><subject>Species Specificity</subject><subject>Staphylococcus infections</subject><subject>Strains (organisms)</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk0uP0zAUhSMEYobCP0AQCQnBosWvOM4GaVRelUYM4rW1bhyn48qJO3ZS0X-PM01HDZoFyiLRzXeP7XN8k-Q5RgtMc_xu43rfgl1sXasXCBPMBXqQnOOCkjkniD48-T5LnoSwQSijgvPHyRnJBKKCiPNk-83rnW4749rU1WlpXG1sk9bON3BbhLZKvW7cDuwA6D8mdKZdH8mQlvtY7DwobW1vwacfvkLQYYCX0Gz31pWgOu3Tjd70rXmaPKrBBv1sfM-SX58-_lx-mV9efV4tLy7nihekm1NEKsHLiuOCFQQQw4rljAOtoKQ151WONIEqKzJSEo1KYDSnotRZXeREMUVnycuD7ta6IEezgsScc4oxzkQkVgeicrCRW28a8HvpwMjbgvNrCb4zympZEJFnjAqtdMkyTAE4Zljnea4EBVFErffjan3Z6EpFRz3Yiej0T2uu5drtZNw2YTGXWfJmFPDuptehk40Jg6XQatcf9l0InjEc0Vf_oPefbqTWEA9g2toNGQ2i8oIRQnPE8bDs4h4qPpVujIo3K2aspw1vJw2R6WL8a-hDkKsf3_-fvfo9ZV-fsNcabHcdnO2HOximIDuAyrsQvK7vTMZIDoNxdEMOgyHHwYhtL04Dums6TgL9C9kLCIg</recordid><startdate>20150324</startdate><enddate>20150324</enddate><creator>Brown, Helen L</creator><creator>Reuter, Mark</creator><creator>Hanman, Kate</creator><creator>Betts, Roy P</creator><creator>van Vliet, Arnoud H M</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150324</creationdate><title>Prevention of biofilm formation and removal of existing biofilms by extracellular DNases of Campylobacter jejuni</title><author>Brown, Helen L ; Reuter, Mark ; Hanman, Kate ; Betts, Roy P ; van Vliet, Arnoud H M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-302d86bd619492a041c4746a3dab3f66d70e2ad5952b2e0ba43738be5f972c4c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Biofilms</topic><topic>Biofilms - drug effects</topic><topic>Biofilms - growth & development</topic><topic>Brucella</topic><topic>Campylobacter</topic><topic>Campylobacter jejuni</topic><topic>Campylobacter jejuni - enzymology</topic><topic>Campylobacter jejuni - genetics</topic><topic>Deactivation</topic><topic>Deoxyribonucleases - pharmacology</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA Primers - genetics</topic><topic>Environmental DNA</topic><topic>Enzymes</topic><topic>Extracellular Space - genetics</topic><topic>Food</topic><topic>Food chains</topic><topic>Food Microbiology</topic><topic>Genes</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Gentian Violet</topic><topic>Green Fluorescent Proteins</topic><topic>Inactivation</topic><topic>Indoles</topic><topic>Neutrophils</topic><topic>Pathogens</topic><topic>Proteins</topic><topic>Species Specificity</topic><topic>Staphylococcus infections</topic><topic>Strains (organisms)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brown, Helen L</creatorcontrib><creatorcontrib>Reuter, Mark</creatorcontrib><creatorcontrib>Hanman, Kate</creatorcontrib><creatorcontrib>Betts, Roy P</creatorcontrib><creatorcontrib>van Vliet, Arnoud H M</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</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>Brown, Helen L</au><au>Reuter, Mark</au><au>Hanman, Kate</au><au>Betts, Roy P</au><au>van Vliet, Arnoud H M</au><au>Gerlach, Roman G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prevention of biofilm formation and removal of existing biofilms by extracellular DNases of Campylobacter jejuni</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-03-24</date><risdate>2015</risdate><volume>10</volume><issue>3</issue><spage>e0121680</spage><epage>e0121680</epage><pages>e0121680-e0121680</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The fastidious nature of the foodborne bacterial pathogen Campylobacter jejuni contrasts with its ability to survive in the food chain. The formation of biofilms, or the integration into existing biofilms by C. jejuni, is thought to contribute to food chain survival. As extracellular DNA (eDNA) has previously been proposed to play a role in C. jejuni biofilms, we have investigated the role of extracellular DNases (eDNases) produced by C. jejuni in biofilm formation. A search of 2791 C. jejuni genomes highlighted that almost half of C. jejuni genomes contains at least one eDNase gene, but only a minority of isolates contains two or three of these eDNase genes, such as C. jejuni strain RM1221 which contains the cje0256, cje0566 and cje1441 eDNase genes. Strain RM1221 did not form biofilms, whereas the eDNase-negative strains NCTC 11168 and 81116 did. Incubation of pre-formed biofilms of NCTC 11168 with live C. jejuni RM1221 or with spent medium from a RM1221 culture resulted in removal of the biofilm. Inactivation of the cje1441 eDNase gene in strain RM1221 restored biofilm formation, and made the mutant unable to degrade biofilms of strain NCTC 11168. Finally, C. jejuni strain RM1221 was able to degrade genomic DNA from C. jejuni NCTC 11168, 81116 and RM1221, whereas strain NCTC 11168 and the RM1221 cje1441 mutant were unable to do so. This was mirrored by an absence of eDNA in overnight cultures of C. jejuni RM1221. This suggests that the activity of eDNases in C. jejuni affects biofilm formation and is not conducive to a biofilm lifestyle. These eDNases do however have a potential role in controlling biofilm formation by C. jejuni strains in food chain relevant environments.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25803828</pmid><doi>10.1371/journal.pone.0121680</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Biofilms Biofilms - drug effects Biofilms - growth & development Brucella Campylobacter Campylobacter jejuni Campylobacter jejuni - enzymology Campylobacter jejuni - genetics Deactivation Deoxyribonucleases - pharmacology Deoxyribonucleic acid DNA DNA Primers - genetics Environmental DNA Enzymes Extracellular Space - genetics Food Food chains Food Microbiology Genes Genomes Genomics Gentian Violet Green Fluorescent Proteins Inactivation Indoles Neutrophils Pathogens Proteins Species Specificity Staphylococcus infections Strains (organisms) |
| title | Prevention of biofilm formation and removal of existing biofilms by extracellular DNases of Campylobacter jejuni |
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