{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T16:18:12Z","timestamp":1791389892497,"version":"4.3.3"},"reference-count":40,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,2,20]],"date-time":"2023-02-20T00:00:00Z","timestamp":1676851200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Science and Technology Major Project","award":["2018ZX10714002"],"award-info":[{"award-number":["2018ZX10714002"]}]},{"name":"National Science and Technology Major Project","award":["2020YFE0205700"],"award-info":[{"award-number":["2020YFE0205700"]}]},{"name":"National Science and Technology Major Project","award":["2016\u20134-1101"],"award-info":[{"award-number":["2016\u20134-1101"]}]},{"name":"National Key Research and Development Program of China","award":["2018ZX10714002"],"award-info":[{"award-number":["2018ZX10714002"]}]},{"name":"National Key Research and Development Program of China","award":["2020YFE0205700"],"award-info":[{"award-number":["2020YFE0205700"]}]},{"name":"National Key Research and Development Program of China","award":["2016\u20134-1101"],"award-info":[{"award-number":["2016\u20134-1101"]}]},{"name":"Capital\u2019s Funds for Health Improvement and Research","award":["2018ZX10714002"],"award-info":[{"award-number":["2018ZX10714002"]}]},{"name":"Capital\u2019s Funds for Health Improvement and Research","award":["2020YFE0205700"],"award-info":[{"award-number":["2020YFE0205700"]}]},{"name":"Capital\u2019s Funds for Health Improvement and Research","award":["2016\u20134-1101"],"award-info":[{"award-number":["2016\u20134-1101"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Background. Quinolones are commonly used for reducing the duration of diarrhea, infection severity, and limiting further transmission of disease related to Vibrio cholerae, but V. cholerae susceptibility to quinolone decreases over time. In addition to mutations in the quinolone-resistance determining regions (QRDRs), the presence of qnr and other acquired genes also contributes to quinolone resistance. Results. We determined the prevalence of quinolone resistance related genes among V. cholerae O139 strains isolated in China. We determined that eight strains carried qnrVC, which encodes a pentapeptide repeat protein of the Qnr subfamily, the members of which protect topoisomerases from quinolone action. Four qnrVC alleles were detected: qnrVC1, qnrVC5, qnrVC12, and qnrVC9. However, the strains carrying qnrVC1, qnrVC5, and qnrVC12 were ciprofloxacin (CIP)-sensitive. Contrastingly, the strain carrying qnrVC9 demonstrated high CIP resistance. qnrVC9 was carried by a small plasmid, which was conjugative and contributed to the high CIP resistance to the receptor V. cholerae strain. The same plasmid was also detected in V. vulnificus. The qnrVC1, qnrVC5, and qnrVC12 were cloned into expression plasmids and conferred CIP resistance on the host V. cholerae O139 strain. Conclusions. Our results revealed the contribution of quinolone resistance mediated by the qnrVC9 carried on the small plasmid and its active horizontal transfer among Vibrio species. The results also suggested the different effects of qnrVC alleles in different V. cholerae strains, which is possibly due to differences in sequences of qnrVC alleles and even the genetic characteristics of the host strains.<\/jats:p>","DOI":"10.3390\/antibiotics12020416","type":"journal-article","created":{"date-parts":[[2023,2,20]],"date-time":"2023-02-20T04:28:57Z","timestamp":1676867337000},"page":"416","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Quinolone Resistance Genes and Their Contribution to Resistance in Vibrio cholerae Serogroup O139"],"prefix":"10.3390","volume":"12","author":[{"given":"Yan-Yan","family":"Zhou","sequence":"first","affiliation":[{"name":"Department of Clinical Laboratory Medicine, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li-Yan","family":"Ma","sequence":"additional","affiliation":[{"name":"Department of Clinical Laboratory Medicine, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Yu","sequence":"additional","affiliation":[{"name":"Beijing Municipal Center for Disease Prevention and Control, Beijing 100013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xin","family":"Lu","sequence":"additional","affiliation":[{"name":"Chinese Center for Disease Control and Prevention, State Key Laboratory for Infectious Disease Prevention and Control, Department of Diarrheal Diseases, National Institute for Communicable Disease Control and Prevention, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei-Li","family":"Liang","sequence":"additional","affiliation":[{"name":"Chinese Center for Disease Control and Prevention, State Key Laboratory for Infectious Disease Prevention and Control, Department of Diarrheal Diseases, National Institute for Communicable Disease Control and Prevention, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Biao","family":"Kan","sequence":"additional","affiliation":[{"name":"Chinese Center for Disease Control and Prevention, State Key Laboratory for Infectious Disease Prevention and Control, Department of Diarrheal Diseases, National Institute for Communicable Disease Control and Prevention, Beijing 102206, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian-Rong","family":"Su","sequence":"additional","affiliation":[{"name":"Department of Clinical Laboratory Medicine, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/microbiolspec.PoH-0012-2015","article-title":"Cholera","volume":"4","author":"Lippi","year":"2016","journal-title":"Microbiol. Spectr."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"209","DOI":"10.2471\/BLT.11.093427","article-title":"The global burden of cholera","volume":"90","author":"Ali","year":"2012","journal-title":"Bull. World Health Organ."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2306","DOI":"10.1128\/JCM.41.6.2306-2310.2003","article-title":"Molecular epidemiology of Vibrio cholerae O139 in China: Polymorphism of ribotypes and CTX elements","volume":"41","author":"Qu","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Yu, L., Zhou, Y., Wang, R., Lou, J., Zhang, L., Li, J., Bi, Z., and Kan, B. (2012). Multiple antibiotic resistance of Vibrio cholerae serogroup O139 in China from 1993 to 2009. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0038633"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"638331","DOI":"10.3389\/fmicb.2021.638331","article-title":"Foodborne Pathogenic Vibrios: Antimicrobial Resistance","volume":"12","author":"Dutta","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_6","first-page":"1117","article-title":"Cholera","volume":"67","author":"Piarroux","year":"2017","journal-title":"Rev. Prat."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.1039\/C9MD00120D","article-title":"Quinolone antibiotics","volume":"10","author":"Pham","year":"2019","journal-title":"Med. Chem. Comm."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1111\/j.1462-2920.2006.01054.x","article-title":"Heavy use of prophylactic antibiotics in aquaculture: A growing problem for human and animal health and for the environment","volume":"8","author":"Cabello","year":"2006","journal-title":"Environ. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1111\/nyas.12830","article-title":"Mechanisms of drug resistance: Quinolone resistance","volume":"1354","author":"Hooper","year":"2015","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1038\/nm1347","article-title":"Fluoroquinolone-modifying enzyme: A new adaptation of a common aminoglycoside acetyltransferase","volume":"12","author":"Robicsek","year":"2006","journal-title":"Nat. Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.ijantimicag.2013.03.004","article-title":"Accumulation of mutations in DNA gyrase and topoisomerase IV genes contributes to fluoroquinolone resistance in Vibrio cholerae O139 strains","volume":"42","author":"Zhou","year":"2013","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"146","DOI":"10.3389\/fmicb.2016.00146","article-title":"Characterization of Vibrio fluvialis qnrVC5 Gene in Native and Heterologous Hosts: Synergy of qnrVC5 with other Determinants in Conferring Quinolone Resistance","volume":"7","author":"Vinothkumar","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1016\/S0140-6736(97)07322-4","article-title":"Quinolone resistance from a transferable plasmid","volume":"351","author":"Pascual","year":"1998","journal-title":"Lancet"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Miranda, C.D., Concha, C., Godoy, F.A., and Lee, M.R. (2022). Aquatic Environments as Hotspots of Transferable Low-Level Quinolone Resistance and Their Potential Contribution to High-Level Quinolone Resistance. Antibiotics, 11.","DOI":"10.3390\/antibiotics11111487"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.3201\/eid1407.080132","article-title":"New qnr gene cassettes associated with superintegron repeats in Vibrio cholerae O1","volume":"14","author":"Fonseca","year":"2008","journal-title":"Emerg. Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1128\/AAC.01051-08","article-title":"Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period","volume":"53","author":"Kim","year":"2009","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1128\/AAC.00997-08","article-title":"qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin","volume":"53","author":"Cavaco","year":"2009","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Albornoz, E., Tijet, N., De Belder, D., Gomez, S., Martino, F., Corso, A., Melano, R.G., and Petroni, A. (2017). qnrE1, a Member of a New Family of Plasmid-Located Quinolone Resistance Genes, Originated from the Chromosome of Enterobacter Species. Antimicrob. Agents Chemother., 61.","DOI":"10.1128\/AAC.02555-16"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Zhang, Y., Zheng, Z., Chan, E.W., Dong, N., Xia, X., and Chen, S. (2018). Molecular Characterization of qnrVCGenes Their Novel Alleles in Vibrio spp Isolated from Food Products in China. Antimicrob. Agents Chemother., 62.","DOI":"10.1128\/AAC.00529-18"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/j.ijantimicag.2013.08.014","article-title":"Molecular characterisation of a multidrug resistance conjugative plasmid from Vibrio parahaemolyticus","volume":"42","author":"Liu","year":"2013","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.ijantimicag.2009.03.020","article-title":"Mechanism of drug resistance in a clinical isolate of Vibrio fluvialis: Involvement of multiple plasmids and integrons","volume":"34","author":"Rajpara","year":"2009","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.eimc.2012.09.008","article-title":"QnrVC, a new transferable Qnr-like family","volume":"31","author":"Pons","year":"2013","journal-title":"Enferm. Infecc. Y Microbiol. Clin."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1628","DOI":"10.1099\/jmm.0.062661-0","article-title":"Epidemiology of qnrVC alleles and emergence out of the Vibrionaceae family","volume":"62","author":"Fonseca","year":"2013","journal-title":"J. Med. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.jgar.2022.08.004","article-title":"qnrVC occurs in different genetic contexts in Klebsiella and Enterobacter strains isolated from Brazilian coastal waters","volume":"31","author":"Kraychete","year":"2022","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_25","first-page":"405","article-title":"Fluoroquinolone resistance contributing mechanisms and genotypes of ciprofloxacin- unsusceptible Pseudomonas aeruginosa strains in Iran: Emergence of isolates carrying qnr\/aac(6)-Ib genes. International microbiology","volume":"25","author":"Nabilou","year":"2022","journal-title":"Off. J. Span. Soc. Microbiol."},{"key":"ref_26","first-page":"93","article-title":"Burden of Fluoroquinolone Resistance in Clinical Isolates of Escherichia coli at the Ho Teaching Hospital, Ghana","volume":"32","author":"Deku","year":"2022","journal-title":"Ethiop. J. Health Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1016\/j.tim.2014.04.007","article-title":"Fluoroquinolone resistance: Mechanisms, impact on bacteria, and role in evolutionary success","volume":"22","author":"Redgrave","year":"2014","journal-title":"Trends Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3050","DOI":"10.1128\/AAC.49.7.3050-3052.2005","article-title":"Interaction of the plasmid-encoded quinolone resistance protein QnrA with Escherichia coli topoisomerase IV","volume":"49","author":"Tran","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1128\/AAC.01045-09","article-title":"Transferable quinolone resistance in Vibrio cholerae","volume":"54","author":"Kim","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Kotb, D.N., Mahdy, W.K., Mahmoud, M.S., and Khairy, R.M.M. (2019). Impact of co-existence of PMQR genes and QRDR mutations on fluoroquinolones resistance in Enterobacteriaceae strains isolated from community and hospital acquired UTIs. BMC Infect. Dis., 19.","DOI":"10.1186\/s12879-019-4606-y"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Nohejl, T., Valcek, A., Papousek, I., Palkovicova, J., Wailan, A.M., Pratova, H., Minoia, M., and Dolejska, M. (2022). Genomic analysis of qnr-harbouring IncX plasmids and their transferability within different hosts under induced stress. BMC Microbiol., 22.","DOI":"10.1186\/s12866-022-02546-6"},{"key":"ref_32","first-page":"250","article-title":"Fluoroquinolone antibiotics: An emerging class of environmental micropollutants","volume":"500\u2013501","author":"Dewulf","year":"2014","journal-title":"Sci. Total Environ."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"117402","DOI":"10.1016\/j.envpol.2021.117402","article-title":"Distribution of antibiotic resistance genes in the environment","volume":"285","author":"Zhuang","year":"2021","journal-title":"Environ. Pollut."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1016\/j.scitotenv.2019.06.134","article-title":"Identifying hotspots for antibiotic resistance emergence and selection, and elucidating pathways to human exposure: Application of a systems-thinking approach to aquaculture systems","volume":"687","author":"Brunton","year":"2019","journal-title":"Sci. Total Environ."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1093\/jac\/dkv103","article-title":"Description of an original integron encompassing blaVIM-2, qnrVC1 and genes encoding bacterial group II intron proteins in Pseudomonas aeruginosa","volume":"70","author":"Belotti","year":"2015","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1128\/AAC.01158-10","article-title":"Structural and biochemical analysis of the pentapeptide repeat protein EfsQnr, a potent DNA gyrase inhibitor","volume":"55","author":"Hegde","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"5733","DOI":"10.1128\/AAC.01533-13","article-title":"Mutational analysis of quinolone resistance protein QnrB1","volume":"57","author":"Jacoby","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1939","DOI":"10.1128\/AAC.01805-15","article-title":"Mutational Analysis of Quinolone Resistance Protein QnrVC7 Provides Novel Insights into the Structure-Activity Relationship of Qnr Proteins","volume":"60","author":"Po","year":"2016","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3354","DOI":"10.1128\/AAC.00339-07","article-title":"New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate","volume":"51","author":"Yamane","year":"2007","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/2\/416\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:36:59Z","timestamp":1760121419000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/2\/416"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,20]]},"references-count":40,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["antibiotics12020416"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12020416","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,20]]}}}