{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T15:42:07Z","timestamp":1791214927826,"version":"4.1.0"},"reference-count":47,"publisher":"Oxford University Press (OUP)","issue":"8","license":[{"start":{"date-parts":[[2024,1,24]],"date-time":"2024-01-24T00:00:00Z","timestamp":1706054400000},"content-version":"vor","delay-in-days":3288,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/3.0\/"},{"start":{"date-parts":[[2015,1,23]],"date-time":"2015-01-23T00:00:00Z","timestamp":1421971200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/3.0\/"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2015,8,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Association of Vibrio cholerae with chitinous surfaces of zooplankton is important for its persistence in marine environments, as it provides accessibility to nutrients and resistance to stresses. Predation by heterotrophic protists has a major impact on the survival of V. cholerae. V. cholerae forms biofilms as its main defensive strategy, and quorum sensing (QS) additionally regulates the production of antiprotozoal factors. The role of chitin and QS regulation in V. cholerae grazing resistance was investigated by exposing V. cholerae wild-type (WT) and QS mutant biofilms grown on chitin flakes to the bacteriotrophic, surface-feeding flagellate Rhynchomonas nasuta. V. cholerae formed more biofilm biomass on chitin flakes compared with nonchitinous surfaces. The growth of R. nasuta was inhibited by WT biofilms grown on chitin flakes, whereas the inhibition was attenuated in QS mutant biofilms. The chitin-dependent toxicity was also observed when the V. cholerae biofilms were developed under continuous flow or grown on a natural chitin source, the exoskeleton of Artemia. In addition, the antiprotozoal activity and ammonium concentration of V. cholerae biofilm supernatants were quantified. The ammonium levels (3.5\u2009mm) detected in the supernatants of V. cholerae WT biofilms grown on chitin flakes were estimated to reduce the number of R. nasuta by &amp;gt;80% in add-back experiments, and the supernatant of QS mutant biofilms was less toxic owing to a decrease in ammonium production. Transcriptomic analysis revealed that the majority of genes involved in chitin metabolism and chemotaxis were significantly downregulated in QS mutant biofilms when grown on chitin compared with the WT biofilms.<\/jats:p>","DOI":"10.1038\/ismej.2014.265","type":"journal-article","created":{"date-parts":[[2015,1,23]],"date-time":"2015-01-23T16:36:52Z","timestamp":1422031012000},"page":"1812-1820","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":77,"title":["Quorum sensing-regulated chitin metabolism provides grazing resistance to <i>Vibrio cholerae<\/i> biofilms"],"prefix":"10.1093","volume":"9","author":[{"given":"Shuyang","family":"Sun","sequence":"first","affiliation":[{"name":"Centre for Marine Biofouling and Bio-Innovation, School of Biotechnology and Biomolecular Science, University of New South Wales , Sydney, New South Wales, Australia"},{"name":"Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qi Xiang Martin","family":"Tay","sequence":"additional","affiliation":[{"name":"Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Staffan","family":"Kjelleberg","sequence":"additional","affiliation":[{"name":"Centre for Marine Biofouling and Bio-Innovation, School of Biotechnology and Biomolecular Science, University of New South Wales , Sydney, New South Wales, Australia"},{"name":"Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , Singapore"},{"name":"School of Biological Sciences, Nanyang Technological University , Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott A","family":"Rice","sequence":"additional","affiliation":[{"name":"Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , Singapore"},{"name":"School of Biological Sciences, Nanyang Technological University , Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diane","family":"McDougald","sequence":"additional","affiliation":[{"name":"Centre for Marine Biofouling and Bio-Innovation, School of Biotechnology and Biomolecular Science, University of New South Wales , Sydney, New South Wales, Australia"},{"name":"Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , Singapore"},{"name":"School of Biological Sciences, Nanyang Technological University , Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2015,1,23]]},"reference":[{"key":"2024012421165827300_CR1","doi-asserted-by":"publisher","first-page":"2849","DOI":"10.1128\/AEM.72.4.2849-2855.2006","article-title":"Toxigenic Vibrio cholerae in the aquatic environment of Mathbaria, Bangladesh","volume":"72","author":"Alam","year":"2006","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR2","doi-asserted-by":"publisher","first-page":"1775","DOI":"10.1126\/science.1122396","article-title":"Microbiology. Chitin, cholera, and competence","volume":"310","author":"Bartlett","year":"2005","journal-title":"Science"},{"key":"2024012421165827300_CR3","doi-asserted-by":"publisher","first-page":"3478","DOI":"10.1016\/S0043-1354(01)00055-0","article-title":"Effects of chronic ammonium and nitrite contamination on the macroinvertebrate community in running water microcosms","volume":"35","author":"Berenzen","year":"2001","journal-title":"Water Res"},{"key":"2024012421165827300_CR4","doi-asserted-by":"publisher","first-page":"3220","DOI":"10.1128\/AEM.67.7.3220-3225.2001","article-title":"The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton","volume":"67","author":"Chiavelli","year":"2001","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR5","doi-asserted-by":"crossref","first-page":"3323","DOI":"10.1128\/aem.63.8.3323-3326.1997","article-title":"Effect of alum on free-living and copepod-associated Vibrio cholerae O1 and O139","volume":"63","author":"Chowdhury","year":"1997","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR6","doi-asserted-by":"publisher","first-page":"1051","DOI":"10.1073\/pnas.0237386100","article-title":"Reduction of cholera in Bangladeshi villages by simple filtration","volume":"100","author":"Colwell","year":"2003","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024012421165827300_CR7","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1111\/j.1758-2229.2009.00043.x","article-title":"Quorum sensing negatively regulates chitinase in Vibrio harveyi","volume":"2","author":"Defoirdt","year":"2010","journal-title":"Environ Microbiol Rep"},{"key":"2024012421165827300_CR8","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1111\/j.1574-6941.2011.01067.x","article-title":"In situ grazing resistance of Vibrio cholerae in the marine environment","volume":"76","author":"Erken","year":"2011","journal-title":"FEMS Microbiol Ecol"},{"key":"2024012421165827300_CR9","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1128\/MMBR.62.4.1301-1314.1998","article-title":"Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae","volume":"62","author":"Faruque","year":"1998","journal-title":"Microbiol Mol Biol Rev"},{"key":"2024012421165827300_CR10","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1007\/s00248-009-9578-9","article-title":"What genomic sequence information has revealed about Vibrio ecology in the ocean\u2014a review","volume":"58","author":"Grimes","year":"2009","journal-title":"Microb Ecol"},{"key":"2024012421165827300_CR11","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1128\/AEM.01412-07","article-title":"Conservation of the chitin utilization pathway in the Vibrionaceae","volume":"74","author":"Hunt","year":"2008","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR12","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1128\/aem.45.1.275-283.1983","article-title":"Ecological relationships between Vibrio cholerae and planktonic crustacean copepods","volume":"45","author":"Huq","year":"1983","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR13","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1128\/aem.48.2.420-424.1984","article-title":"Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms","volume":"48","author":"Huq","year":"1984","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR14","doi-asserted-by":"publisher","first-page":"1249","DOI":"10.1016\/S0140-6736(95)92038-2","article-title":"Coexistence of Vibrio cholerae O1 and O139 Bengal in plankton in Bangladesh","volume":"345","author":"Huq","year":"1995","journal-title":"Lancet"},{"key":"2024012421165827300_CR15","doi-asserted-by":"crossref","first-page":"2508","DOI":"10.1128\/aem.62.7.2508-2512.1996","article-title":"A simple filtration method to remove plankton-associated Vibrio cholerae in raw water supplies in developing countries","volume":"62","author":"Huq","year":"1996","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR16","doi-asserted-by":"publisher","first-page":"e6734","DOI":"10.1371\/journal.pone.0006734","article-title":"Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains","volume":"4","author":"Ishikawa","year":"2009","journal-title":"PLoS One"},{"key":"2024012421165827300_CR17","doi-asserted-by":"publisher","first-page":"7083","DOI":"10.1128\/AEM.00557-06","article-title":"Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing","volume":"72","author":"Jousset","year":"2006","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR18","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1038\/nature04249","article-title":"A colonization factor links Vibrio cholerae environmental survival and human infection","volume":"438","author":"Kirn","year":"2005","journal-title":"Nature"},{"key":"2024012421165827300_CR19","doi-asserted-by":"publisher","first-page":"3211","DOI":"10.1093\/bioinformatics\/bts611","article-title":"SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data","volume":"28","author":"Kopylova","year":"2012","journal-title":"Bioinformatics"},{"key":"2024012421165827300_CR20","doi-asserted-by":"publisher","first-page":"R25","DOI":"10.1186\/gb-2009-10-3-r25","article-title":"Ultrafast and memory-efficient alignment of short DNA sequences to the human genome","volume":"10","author":"Langmead","year":"2009","journal-title":"Genome Biology"},{"key":"2024012421165827300_CR21","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/S0070-2153(05)73004-0","article-title":"Signal relay during the life cycle of Dictyostelium","volume":"73","author":"Mahadeo","year":"2006","journal-title":"Curr Top Dev Biol"},{"key":"2024012421165827300_CR22","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/j.chom.2011.07.007","article-title":"RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression","volume":"10","author":"Mandlik","year":"2011","journal-title":"Cell Host Microbe"},{"key":"2024012421165827300_CR23","doi-asserted-by":"publisher","first-page":"10","DOI":"10.14806\/ej.17.1.200","article-title":"Cutadapt removes adapter sequences from high-throughput sequencing reads","volume":"17","author":"Martin","year":"2011","journal-title":"EMBnet.journal"},{"key":"2024012421165827300_CR24","doi-asserted-by":"publisher","first-page":"16819","DOI":"10.1073\/pnas.0505350102","article-title":"Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae","volume":"102","author":"Matz","year":"2005","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024012421165827300_CR25","doi-asserted-by":"publisher","first-page":"2524","DOI":"10.1073\/pnas.0308707101","article-title":"The Vibrio cholerae chitin utilization program","volume":"101","author":"Meibom","year":"2004","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024012421165827300_CR26","doi-asserted-by":"publisher","first-page":"1824","DOI":"10.1126\/science.1120096","article-title":"Chitin induces natural competence in Vibrio cholerae","volume":"310","author":"Meibom","year":"2005","journal-title":"Science"},{"key":"2024012421165827300_CR27","doi-asserted-by":"publisher","first-page":"2941","DOI":"10.1128\/IAI.01266-10","article-title":"Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum","volume":"79","author":"Miyata","year":"2011","journal-title":"Infect Immun"},{"key":"2024012421165827300_CR28","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1128\/AEM.64.2.721-732.1998","article-title":"In situ gene expression in mixed-culture biofilms: evidence of metabolic interactions between community members","volume":"64","author":"Moller","year":"1998","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR29","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1098\/rstb.2006.1957","article-title":"Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web","volume":"362","author":"Murphy","year":"2007","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"2024012421165827300_CR30","first-page":"260","article-title":"Role of shrimp chitin in the ecology of toxigenic Vibrio cholerae and cholera transmission","volume":"2","author":"Nahar","year":"2011","journal-title":"Front Microbiol"},{"key":"2024012421165827300_CR31","doi-asserted-by":"crossref","first-page":"768","DOI":"10.1128\/iai.25.2.768-770.1979","article-title":"Adsorption and growth of Vibrio cholerae on chitin","volume":"25","author":"Nalin","year":"1979","journal-title":"Infect Immun"},{"key":"2024012421165827300_CR32","doi-asserted-by":"publisher","first-page":"2847","DOI":"10.1016\/j.watres.2004.03.042","article-title":"Lethal and sublethal toxicity of ammonia to native, invasive, and parasitised freshwater amphipods","volume":"38","author":"Prenter","year":"2004","journal-title":"Water Res"},{"key":"2024012421165827300_CR33","doi-asserted-by":"publisher","first-page":"1400","DOI":"10.1111\/j.1462-2920.2007.01559.x","article-title":"Global impact of Vibrio cholerae interactions with chitin","volume":"10","author":"Pruzzo","year":"2008","journal-title":"Environ Microbiol"},{"key":"2024012421165827300_CR34","doi-asserted-by":"publisher","first-page":"3551","DOI":"10.1128\/JB.187.10.3551-3555.2005","article-title":"Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin","volume":"187","author":"Reguera","year":"2005","journal-title":"J Bacteriol"},{"key":"2024012421165827300_CR35","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1136\/gut.28.8.1043","article-title":"Chronic portal systemic encephalopathy: update 1987","volume":"28","author":"Sherlock","year":"1987","journal-title":"Gut"},{"key":"2024012421165827300_CR36","doi-asserted-by":"publisher","first-page":"e56338","DOI":"10.1371\/journal.pone.0056338","article-title":"Relative contributions of Vibrio polysaccharide and quorum sensing to the resistance of Vibrio cholerae to predation by heterotrophic protists","volume":"8","author":"Sun","year":"2013","journal-title":"PLoS One"},{"key":"2024012421165827300_CR37","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1007\/s12192-008-0011-y","article-title":"Exposure of gnotobiotic Artemia franciscana larvae to abiotic stress promotes heat shock protein 70 synthesis and enhances resistance to pathogenic Vibrio campbellii","volume":"13","author":"Sung","year":"2008","journal-title":"Cell Stress Chaperones"},{"key":"2024012421165827300_CR38","doi-asserted-by":"crossref","first-page":"1348","DOI":"10.1128\/AEM.65.3.1348-1351.1999","article-title":"Role of surface proteins in Vibrio cholerae attachment to chitin","volume":"65","author":"Tarsi","year":"1999","journal-title":"Appl Environ Microbiol"},{"key":"2024012421165827300_CR39","first-page":"1","article-title":"Microbiological studies on coastal waters of the Northern Baltic sea, I. Distribution and abundance of bacteria and yeasts in the Tvarminne area","volume":"1","author":"Vaatanen","year":"1976","journal-title":"Walter Andre Nottback Found Sci Rep"},{"key":"2024012421165827300_CR40","doi-asserted-by":"publisher","first-page":"9280","DOI":"10.1073\/pnas.0601754103","article-title":"A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing","volume":"103","author":"Vaitkevicius","year":"2006","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024012421165827300_CR41","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1016\/j.copbio.2008.04.002","article-title":"Dual role colonization factors connecting Vibrio cholerae\u2019s lifestyles in human and aquatic environments open new perspectives for combating infectious diseases","volume":"19","author":"Vezzulli","year":"2008","journal-title":"Curr Opin Biotechnol"},{"key":"2024012421165827300_CR42","doi-asserted-by":"crossref","first-page":"3606","DOI":"10.1128\/JB.181.11.3606-3609.1999","article-title":"A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor","volume":"181","author":"Watnick","year":"1999","journal-title":"J Bacteriol"},{"key":"2024012421165827300_CR43","doi-asserted-by":"publisher","first-page":"1593","DOI":"10.1111\/j.1462-2920.2005.00851.x","article-title":"Grazing resistance of Pseudomonas aeruginosa biofilms depends on type of protective mechanism, developmental stage and protozoan feeding mode","volume":"7","author":"Weitere","year":"2005","journal-title":"Environ Microbiol"},{"key":"2024012421165827300_CR44","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1111\/j.1462-2920.2005.00863.x","article-title":"Trophic regulation of Vibrio cholerae in coastal marine waters","volume":"8","author":"Worden","year":"2006","journal-title":"Environ Microbiol"},{"key":"2024012421165827300_CR45","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1111\/j.1365-2958.2004.04154.x","article-title":"Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant","volume":"53","author":"Yildiz","year":"2004","journal-title":"Mol Microbiol"},{"key":"2024012421165827300_CR46","doi-asserted-by":"crossref","first-page":"24260","DOI":"10.1016\/S0021-9258(18)54223-X","article-title":"Chitin utilization by marine bacteria. A physiological function for bacterial adhesion to immobilized carbohydrates","volume":"266","author":"Yu","year":"1991","journal-title":"J Biol Chem"},{"key":"2024012421165827300_CR47","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.femsle.2005.01.052","article-title":"Vibrio cholerae persistence in aquatic environments and colonization of intestinal cells: involvement of a common adhesion mechanism","volume":"244","author":"Zampini","year":"2005","journal-title":"FEMS Microbiol Lett"}],"container-title":["The ISME Journal"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/ismej2014265.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/ismej2014265","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/ismej\/article-pdf\/9\/8\/1812\/56370697\/41396_2015_article_bfismej2014265.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/www.nature.com\/articles\/ismej2014265.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"},{"URL":"https:\/\/academic.oup.com\/ismej\/article-pdf\/9\/8\/1812\/56370697\/41396_2015_article_bfismej2014265.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,14]],"date-time":"2024-02-14T17:57:03Z","timestamp":1707933423000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ismej\/article\/9\/8\/1812-1820\/7558203"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,1,23]]},"references-count":47,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2015,8,1]]}},"URL":"https:\/\/doi.org\/10.1038\/ismej.2014.265","relation":{},"ISSN":["1751-7362","1751-7370"],"issn-type":[{"value":"1751-7362","type":"print"},{"value":"1751-7370","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2015,8]]},"published":{"date-parts":[[2015,1,23]]},"assertion":[{"value":"29 September 2014","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 December 2014","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 January 2015","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no conflict of interest.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}