{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,12]],"date-time":"2026-03-12T06:12:19Z","timestamp":1773295939212,"version":"3.50.1"},"reference-count":29,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2019,8,9]],"date-time":"2019-08-09T00:00:00Z","timestamp":1565308800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>A series of human and animal diseases that are caused by Salmonella infections pose a serious threat to human health and huge economic losses to the livestock industry. We found antibiotic resistance (AR) genes in the genome of 133 strains of S. Indiana from a poultry production site in Shandong Province, China. Salmonella enterica subsp. enterica serovar Indiana strain MHYL had multidrug-resistance (MDR) genes on its genome. Southern blot analysis was used to locate genes on the genomic DNA. High-throughput sequencing technology was used to determine the gene sequence of the MHYL genome. Areas containing MDR genes were mapped based on the results of gene annotation. The AR genes blaTEM, strA, tetA, and aac(6\u2032)-Ib-cr were found on the MHYL genome. The resistance genes were located in two separate MDR regions, RR1 and RR2, containing type I integrons, and Tn7 transposons and multiple IS26 complex transposons with transposable functions. Portions of the MDR regions were determined to be highly homologous to the structure of plasmid pAKU_1 in S. enterica serovar Paratyphi A (accession number: AM412236), SGI11 in S. enterica serovar Typhimurium (accession number: KM023773), and plasmid pS414 in S. Indiana (accession No.: KC237285).<\/jats:p>","DOI":"10.3390\/microorganisms7080248","type":"journal-article","created":{"date-parts":[[2019,8,9]],"date-time":"2019-08-09T11:11:31Z","timestamp":1565349091000},"page":"248","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Genomic Sequence Analysis of the Multidrug-Resistance Region of Avian Salmonella enterica serovar Indiana Strain MHYL"],"prefix":"10.3390","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8941-3896","authenticated-orcid":false,"given":"Yan","family":"Lu","sequence":"first","affiliation":[{"name":"National Demonstration Center for Animal Experimental Education, Beijing University of Agriculture, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4427-8907","authenticated-orcid":false,"given":"Yanjia","family":"Wen","sequence":"additional","affiliation":[{"name":"National Demonstration Center for Animal Experimental Education, Beijing University of Agriculture, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ge","family":"Hu","sequence":"additional","affiliation":[{"name":"Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, Beijing University of Agriculture, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuqi","family":"Liu","sequence":"additional","affiliation":[{"name":"National Demonstration Center for Animal Experimental Education, Beijing University of Agriculture, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3445-1008","authenticated-orcid":false,"given":"Ross C.","family":"Beier","sequence":"additional","affiliation":[{"name":"United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, College Station, TX 77845\u20134988, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4423-635X","authenticated-orcid":false,"given":"Xiaolin","family":"Hou","sequence":"additional","affiliation":[{"name":"National Demonstration Center for Animal Experimental Education, Beijing University of Agriculture, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,8,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1086\/650733","article-title":"The global burden of nontyphoidal Salmonella gastroenteritis","volume":"50","author":"Majowicz","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/j.cmi.2015.12.004","article-title":"Salmonellosis: The role of poultry meat","volume":"22","author":"Antunes","year":"2016","journal-title":"Clin. Microbial. Infect."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"7","DOI":"10.3201\/eid1701.P11101","article-title":"Foodborne illness acquired in the United States\u2014Major pathogens","volume":"17","author":"Scallan","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_4","unstructured":"Centers for Disease Control and Prevention (CDC) (2018, October 11). Foodborne Diseases Active Surveillance Network (FoodNet): FoodNet Surveillance Report for 2012 (Final Report), Available online: https:\/\/www.cdc.gov\/foodnet\/PDFs\/2012_annual_report_508c.pdf."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1111\/zph.12328","article-title":"Prevalence and antimicrobial resistance of Salmonella enterica serovar Indiana in China (1984\u20132016)","volume":"64","author":"Gong","year":"2017","journal-title":"Zoonoses Public Health"},{"key":"ref_6","first-page":"1051","article-title":"Identification and drug resistance of the first Salmonella Indiana in Yunnan military garrison","volume":"13","author":"Li","year":"2013","journal-title":"Chin. Trop. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"607","DOI":"10.3201\/eid0505.990502","article-title":"Food-related illness and death in the United States","volume":"5","author":"Mead","year":"1999","journal-title":"Emerg. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4114","DOI":"10.1128\/AAC.00560-11","article-title":"Characterization of Salmonella enterica serovar Typhimurium isolates harboring a chromosomally encoded CMY-2 \u03b2-lactamase gene located on a multidrug resistance genomic island","volume":"55","author":"Shahada","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1111\/j.1574-6968.2000.tb09245.x","article-title":"Partial characterization of a genomic island associated with the multidrug resistance region of Salmonella enterica Typhymurium DT104","volume":"189","author":"Boyd","year":"2000","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e01503-17","DOI":"10.1128\/AEM.01503-17","article-title":"Horizontal dissemination of antimicrobial resistance determinants in multiple Salmonella serotypes following isolation from the commercial swine operation environment after manure application","volume":"83","author":"Pornsukarom","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1915","DOI":"10.1016\/j.micinf.2005.12.028","article-title":"The genetics of Salmonella genomic island 1","volume":"8","author":"Mulvey","year":"2006","journal-title":"Microb. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"585","DOI":"10.3201\/eid0905.020609","article-title":"Variant Salmonella genomic island 1 antibiotic resistance gene cluster in Salmonella enterica serovar Albany","volume":"9","author":"Doublet","year":"2003","journal-title":"Emerg. Infect. Dis."},{"key":"ref_13","unstructured":"Clinical and Laboratory Standards Institute (CLSI) (2012). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals, Clinical and Laboratory Standards Institute. Approved Standard Third Edition. Informational Supplement; CLSI document M31-A3."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Lu, Y., Zhao, H., Sun, J., Liu, Y., Zhou, X., Beier, R.C., Wu, G., and Hou, X. (2014). Characterization of multidrug-resistant Salmonella enterica serovars Indiana and Enteritidis from chickens in Eastern China. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0096050"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1089\/fpd.2010.0605","article-title":"Prevalence of antimicrobial resistance among Salmonella isolates from chicken in China","volume":"8","author":"Lu","year":"2011","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1007\/s00438-013-0762-8","article-title":"Genomic comparison of Salmonella typhimurium DT104 with non-DT104 strains","volume":"288","author":"Zhao","year":"2013","journal-title":"Mol. Genet. Genom."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1089\/fpd.2012.1455","article-title":"Unique class 1 integron and multiple resistance genes co-located on IncHI2 plasmid is associated with the emerging multidrug resistance of Salmonella Indiana isolated from chicken in China","volume":"10","author":"Lai","year":"2013","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1128\/AAC.04081-14","article-title":"Chromosome-mediated multidrug resistance in Salmonella enterica serovar Typhi","volume":"59","author":"Chiou","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"4257","DOI":"10.1128\/JB.00232-07","article-title":"Multidrug-resistant Salmonella enterica serovar Paratyphi A harbors IncHI1 plasmids similar to those found in serovar Typhi","volume":"189","author":"Holt","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/PL00008668","article-title":"The 51,409-bp R-plasmid pTP10 from the multiresistant clinical isolate Corynebacterium striatum M82B is composed of DNA segments initially identified in soil bacteria and in plant, animal, and human pathogens","volume":"263","author":"Tauch","year":"2000","journal-title":"Mol. Gen. Genet."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.jbiotec.2008.02.009","article-title":"The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing","volume":"136","author":"Tauch","year":"2008","journal-title":"J. Biotechnol."},{"key":"ref_22","unstructured":"Berg, D.E., and Howe, M.M. (1989). Mobile DNA, ASM Press."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3745","DOI":"10.1128\/AAC.00525-08","article-title":"Novel insertion sequence- and transposon-mediated genetic rearrangements in genomic island SGI1 of Salmonella enterica serovar Kentucky","volume":"52","author":"Doublet","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_24","first-page":"73","article-title":"Mechanisms of copper homeostasis in bacteria","volume":"3","author":"Raimunda","year":"2013","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1099\/jmm.0.023036-0","article-title":"Bacterial antimicrobial metal ion resistance","volume":"64","author":"Hobman","year":"2014","journal-title":"J. Med. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1371\/journal.pgen.0020007","article-title":"Comparative genomics of multidrug resistance in Acinetobacter baumannii","volume":"2","author":"Fournier","year":"2006","journal-title":"PloS Genet."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/S0168-6445(03)00046-9","article-title":"Bacterial mercury resistance from atoms to ecosystems","volume":"27","author":"Barkay","year":"2003","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"6377","DOI":"10.1128\/jb.174.20.6377-6385.1992","article-title":"Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding","volume":"174","author":"Hamlett","year":"1992","journal-title":"J. Bacteriol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1111\/1574-6968.12005","article-title":"A novel gene, ardD, determines antirestriction activity of the non-conjugative transposon Tn5053 and is located antisense within the tniA gene","volume":"337","author":"Balabanov","year":"2012","journal-title":"FEMS Microbiol. Lett."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/7\/8\/248\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:09:54Z","timestamp":1760188194000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/7\/8\/248"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8,9]]},"references-count":29,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2019,8]]}},"alternative-id":["microorganisms7080248"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms7080248","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,8,9]]}}}