{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,3]],"date-time":"2026-03-03T01:15:33Z","timestamp":1772500533717,"version":"3.50.1"},"reference-count":45,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,4,20]],"date-time":"2021-04-20T00:00:00Z","timestamp":1618876800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Extended-spectrum \u03b2-lactamases (ESBLs) production and (fluoro)quinolone (FQ) resistance among <jats:italic>Salmonella<\/jats:italic> pose a public health threat. The objective of this study was the phenotypic and genotypic characterization of an ESBL-producing and nalidixic acid-resistant <jats:italic>Salmonella enterica<\/jats:italic> serovar Gloucester isolate (serotype 4:i:l,w) of sequence type 34 (ST34) from ready-to-eat (RTE) meat products in China. Whole-genome short and long read sequencing (HiSeq and MinION) results showed that it contained <jats:italic>bla<\/jats:italic><jats:sub>CTX\u2013M\u2013<\/jats:sub><jats:sub>55<\/jats:sub>, <jats:italic>qnrS1<\/jats:italic>, and <jats:italic>tetB<\/jats:italic> genes, with <jats:italic>bla<\/jats:italic><jats:sub>CTX\u2013M\u2013<\/jats:sub><jats:sub>55<\/jats:sub> and <jats:italic>qnrS1<\/jats:italic> located in chromosomal IS<jats:italic>26<\/jats:italic>-mediated composite transposon (IS<jats:italic>26<\/jats:italic>\u2013<jats:italic>qnrS1<\/jats:italic>\u2013IS<jats:italic>3<\/jats:italic>\u2013Tn<jats:italic>3<\/jats:italic>\u2013<jats:italic>orf<\/jats:italic>\u2013<jats:italic>bla<\/jats:italic><jats:sub>CTX\u2013M\u2013<\/jats:sub><jats:sub>55<\/jats:sub>\u2013IS<jats:italic>Ecp1<\/jats:italic>\u2013IS<jats:italic>26<\/jats:italic>). The same genetic structure was found in the chromosome of <jats:italic>S. enterica<\/jats:italic> subsp. <jats:italic>enterica<\/jats:italic> serovar Typhimurium strain and in several plasmids of <jats:italic>Escherichia coli<\/jats:italic>, indicating that the IS<jats:italic>26<\/jats:italic>-mediated composite transposon in the chromosome of <jats:italic>S.<\/jats:italic> Gloucester may originate from plasmids of <jats:italic>E. coli<\/jats:italic> and possess the ability to disseminate to <jats:italic>Salmonella<\/jats:italic> and other bacterial species. Besides, the structural unit <jats:italic>qnrS1<\/jats:italic>\u2013IS<jats:italic>3<\/jats:italic>\u2013Tn<jats:italic>3<\/jats:italic>\u2013<jats:italic>orf<\/jats:italic>\u2013<jats:italic>bla<\/jats:italic><jats:sub>CTX\u2013M\u2013<\/jats:sub><jats:sub>55<\/jats:sub> was also observed to be linked with IS<jats:italic>Kpn19<\/jats:italic> in both the chromosomes and plasmids of various bacteria species, highlighting the contribution of the insertion sequences (IS<jats:italic>26<\/jats:italic> and IS<jats:italic>Kpn19<\/jats:italic>) to the co-dissemination of <jats:italic>bla<\/jats:italic><jats:sub>CTX\u2013M\u2013<\/jats:sub><jats:sub>55<\/jats:sub> and <jats:italic>qnrS1<\/jats:italic>. To our knowledge, this is the first description of chromosomal <jats:italic>bla<\/jats:italic><jats:sub>CTX\u2013M\u2013<\/jats:sub><jats:sub>55<\/jats:sub> and <jats:italic>qnrS<\/jats:italic> in <jats:italic>S.<\/jats:italic> Gloucester from RTE meat products. Our work expands the host range and provides additional evidence of the co-transfer of <jats:italic>bla<\/jats:italic><jats:sub>CTX\u2013M\u2013<\/jats:sub><jats:sub>55<\/jats:sub> and <jats:italic>qnrS1<\/jats:italic> among different species of <jats:italic>Salmonella<\/jats:italic> through the food chain.<\/jats:p>","DOI":"10.3389\/fmicb.2021.646101","type":"journal-article","created":{"date-parts":[[2021,4,20]],"date-time":"2021-04-20T06:15:38Z","timestamp":1618899338000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":12,"title":["First Report of a Foodborne Salmonella enterica Serovar Gloucester (4:i:l,w) ST34 Strain Harboring blaCTX\u2013M\u201355 and qnrS Genes Located in IS26-Mediated Composite Transposon"],"prefix":"10.3389","volume":"12","author":[{"given":"Lili","family":"Li","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rikke Heidemann","family":"Olsen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anhua","family":"Song","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jian","family":"Xiao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chong","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hecheng","family":"Meng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lei","family":"Shi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2021,4,20]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1945","DOI":"10.1016\/j.micinf.2005.12.029","article-title":"Salmonella resistant to extended-spectrum cephalosporins: prevalence and epidemiology.","volume":"8","author":"Arlet","year":"2006","journal-title":"Microbes. Infect."},{"key":"B2","doi-asserted-by":"publisher","first-page":"17","DOI":"10.5455\/medarh.2013.67.17-21","article-title":"Causes of infectious acute diarrhea in infants treated at pediatric clinic.","volume":"67","author":"Azemi","year":"2013","journal-title":"Med. Arch."},{"key":"B3","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"2284","DOI":"10.3201\/eid2412.180500","article-title":"CTX-M-65 extended-spectrum \u03b2-lactamase-producing Salmonella enterica serotype Infantis, United States.","volume":"24","author":"Brown","year":"2018","journal-title":"Emerg. Infect. Dis."},{"key":"B5","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1007\/978-1-4939-9877-7_20","article-title":"PlasmidFinder and In Silico pMLST: identification and typing of plasmid replicons in whole-genome sequencing (WGS).","volume":"2075","author":"Carattoli","year":"2020","journal-title":"Methods Mol. Biol."},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2018.02431","article-title":"Genomic characterization of extended-spectrum cephalosporin-resistant Salmonella enterica in the Colombian poultry chain.","volume":"9","author":"Castellanos","year":"2018","journal-title":"Front. Microbiol."},{"key":"B7","article-title":"M100-S26 Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Sixth Informational Supplement","year":"2016"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1099\/mgen.0.000195","article-title":"Fluoroquinolone resistance in Salmonella: insights by whole-genome sequencing.","volume":"4","author":"Cuypers","year":"2018","journal-title":"Microb. Genom."},{"key":"B9","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1016\/j.vetmic.2014.01.030","article-title":"Antimicrobial susceptibility of Salmonella isolates from healthy pigs and chickens (2008-2011).","volume":"171","author":"de Jong","year":"2014","journal-title":"Vet. Microbiol."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1186\/s12879-020-05203-3","article-title":"The phenotypic and molecular characteristics of antimicrobial resistance of Salmonella enterica subsp. enterica serovar Typhimurium in Henan Province. China.","volume":"20","author":"Dong","year":"2020","journal-title":"BMC Infect. Dis."},{"key":"B11","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/j.ijfoodmicro.2011.02.004","article-title":"Salmonella in chicken meat, eggs and humans; Adelaide, South Australia, 2008.","volume":"146","author":"Fearnley","year":"2011","journal-title":"Int. J. Food Microbiol."},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01866-15","article-title":"IS26-mediated precise excision of the IS26-aphA1a translocatable unit.","volume":"6","author":"Harmer","year":"2015","journal-title":"MBio"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1128\/mSphere.00038-16","article-title":"IS26-mediated formation of transposons carrying antibiotic resistance genes.","volume":"1","author":"Harmer","year":"2016","journal-title":"mSphere"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01801-14","article-title":"Movement of IS26-associated antibiotic resistance genes occurs via a translocatable unit that includes a single IS26 and preferentially inserts adjacent to another IS26.","volume":"5","author":"Harmer","year":"2014","journal-title":"MBio"},{"key":"B15","doi-asserted-by":"publisher","first-page":"5976","DOI":"10.1128\/AAC.04920-14","article-title":"Residues distal to the active site contribute to enhanced catalytic activity of variant and hybrid \u03b2-Lactamases derived from CTX-M-14 and CTX-M-15.","volume":"59","author":"He","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"B16","doi-asserted-by":"publisher","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":"B17","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1016\/0732-8893(94)90005-1","article-title":"Multiple-drug-resistant Salmonella gloucester infections in Bangladesh.","volume":"20","author":"Hoque","year":"1994","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"B18","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1089\/fpd.2016.2180","article-title":"Ceftriaxone-resistant nontyphoidal Salmonella from humans, retail meats, and food animals in the United States, 1996\u20132013.","volume":"14","author":"Iwamoto","year":"2017","journal-title":"Foodborne Pathog. Dis."},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1128\/microbiolspec.PLAS-0006-2013","article-title":"Plasmid-mediated quinolone resistance.","volume":"2","author":"Jacoby","year":"2014","journal-title":"Microbiol. Spectr."},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.1001921","article-title":"World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis.","volume":"12","author":"Kirk","year":"2015","journal-title":"PLoS Med."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1089\/fpd.2020.2878","article-title":"Molecular characterization of cephalosporin-resistant Salmonella Enteritidis ST11 isolates carrying blaCTX-M from children with diarrhea.","author":"Li","year":"2021","journal-title":"Foodborne Pathog. Dis."},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1093\/femspd\/ftw103","article-title":"Disseminated infections with antibiotic-resistant non-typhoidal Salmonella strains: contributions of host and pathogen factors.","volume":"74","author":"Lokken","year":"2016","journal-title":"Pathog. Dis."},{"key":"B23","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.ebiom.2019.03.006","article-title":"Epidemiologic and genomic insights on mcr-1-harbouring Salmonella from diarrhoeal outpatients in Shanghai, China, 2006-2016.","volume":"42","author":"Lu","year":"2019","journal-title":"EBio Med."},{"key":"B24","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1016\/j.ijmm.2018.03.008","article-title":"High prevalence of ceftriaxone resistance among invasive Salmonella enterica serotype choleraesuis isolates in thailand: the emergence and increase of CTX-M-55 in ciprofloxacin-resistant S. choleraesuis isolates.","volume":"308","author":"Luk-In","year":"2018","journal-title":"Int. J. Med. Microbiol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1093\/jac\/dkx489","article-title":"Emergence of blaCTX-M-55 associated with fosA, rmtB and mcr gene variants in Escherichia coli from various animal species in France.","volume":"73","author":"Lupo","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"B26","doi-asserted-by":"publisher","first-page":"2824","DOI":"10.1128\/AAC.02155-12","article-title":"Genetic characterization of IncI2 plasmids carrying blaCTX-M-55 spreading in both pets and food animals in China.","volume":"57","author":"Lv","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"B27","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1093\/jac\/dky451","article-title":"CTX-M-55-type ESBL-producing Salmonella enterica are emerging among retail meats in Phnom Penh.","volume":"74","author":"Nadimpalli","year":"2019","journal-title":"Cambodia. J. Antimicrob. Chemother."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2012.00024","article-title":"Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies.","volume":"3","author":"Poirel","year":"2012","journal-title":"Front. Microbiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1016\/j.ijfoodmicro.2017.02.016","article-title":"Characterization of extended-spectrum \u03b2-lactamases (ESBLs)-producing Salmonella in retail raw chicken carcasses.","volume":"248","author":"Qiao","year":"2017","journal-title":"Int. J. Food Microbiol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.2217\/fmb.14.53","article-title":"Plasmid-encoding extended-spectrum \u03b2-lactamase CTX-M-55 in a clinical Shigella sonnei strain, China.","volume":"9","author":"Qu","year":"2014","journal-title":"Future microbiol."},{"key":"B31","first-page":"191","article-title":"Emergence of multidrug-resistant Salmonella gloucester and Salmonella typhimurium in Bangladesh.","volume":"19","author":"Rahman","year":"2001","journal-title":"J. Health Popul. Nutr."},{"key":"B32","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.drup.2016.09.001","article-title":"Plasmid-mediated quinolone resistance: two decades on.","volume":"29","author":"Rodr\u00edguez-Mart\u00ednez","year":"2016","journal-title":"Drug. Resist. Updat."},{"key":"B33","doi-asserted-by":"publisher","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: rapid prokaryotic genome annotation.","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1588","DOI":"10.1099\/jmm.0.2008\/000950-0","article-title":"A Klebsiella pneumoniae sputum culture isolate from China carrying blaOXA-1, blaCTX-M-55 and aac(6\u2019)-Ib-cr.","volume":"57","author":"Shi","year":"2008","journal-title":"J. Med. Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1019","DOI":"10.1128\/JCM.00219-10","article-title":"Extended-spectrum-beta-lactamase, AmpC, and carbapenemase issues.","volume":"48","author":"Thomson","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1089\/fpd.2019.2738","article-title":"Occurrence and antimicrobial susceptibility profile of Salmonella spp. in raw and ready-to-eat foods and campylobacter spp. in retail raw chicken meat in Transylvania, Romania.","volume":"17","author":"T\u00eerziu","year":"2020","journal-title":"Foodborne Pathog. Dis."},{"key":"B37","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.vetmic.2017.08.009","article-title":"High abundance and diversity of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli in faeces and tonsils of pigs at slaughter.","volume":"208","author":"Van Damme","year":"2017","journal-title":"Vet. Microbiol."},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1128\/mSphere.00137-18","article-title":"Evolution and comparative genomics of F33:A-:B- plasmids carrying blaCTX-M-55 or blaCTX-M-65 in Escherichia coli and Klebsiella pneumoniae isolated from animals, food products, and humans in China.","volume":"3","author":"Wang","year":"2018","journal-title":"mSphere"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1005595","article-title":"Unicycler: resolving bacterial genome assemblies from short and long sequencing reads.","volume":"13","author":"Wick","year":"2017","journal-title":"PLoS Comput. Biol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"5026","DOI":"10.1128\/AAC.00775-15","article-title":"Dissemination of IncI2 plasmids that harbor the blaCTX-M element among clinical Salmonella isolates.","volume":"59","author":"Wong","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"B41","doi-asserted-by":"publisher","first-page":"3752","DOI":"10.1128\/AAC.02770-13","article-title":"Emergence of clinical Salmonella enterica serovar Typhimurium isolates with concurrent resistance to ciprofloxacin, ceftriaxone, and azithromycin.","volume":"58","author":"Wong","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"B42","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1089\/fpd.2012.1266","article-title":"Characterization of Salmonella food isolates with concurrent resistance to ceftriaxone and ciprofloxacin.","volume":"10","author":"Wong","year":"2013","journal-title":"Foodborne Pathog. Dis."},{"key":"B43","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1089\/fpd.2014.1859","article-title":"Emergence of \u03b2-lactamases and extended-spectrum \u03b2-lactamases (ESBLs) producing Salmonella in retail raw chicken in China.","volume":"12","author":"Wu","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"B44","doi-asserted-by":"publisher","first-page":"2640","DOI":"10.1093\/jac\/dks261","article-title":"Identification of acquired antimicrobial resistance genes.","volume":"67","author":"Zankari","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.01268","article-title":"The emergence of chromosomally located blaCTX-M-55 in Salmonella from foodborne animals in China.","volume":"10","author":"Zhang","year":"2019","journal-title":"Front. Microbiol."}],"updated-by":[{"DOI":"10.3389\/fmicb.2021.792791","type":"corrigendum","label":"Corrigendum","source":"publisher","updated":{"date-parts":[[2021,11,2]],"date-time":"2021-11-02T00:00:00Z","timestamp":1635811200000}}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2021.646101\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,2]],"date-time":"2021-11-02T17:12:51Z","timestamp":1635873171000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2021.646101\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,20]]},"references-count":45,"alternative-id":["10.3389\/fmicb.2021.646101"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2021.646101","relation":{"corrigendum":[{"id-type":"doi","id":"10.3389\/fmicb.2021.792791","asserted-by":"object"}]},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,20]]},"article-number":"646101"}}