{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T03:20:30Z","timestamp":1789874430674,"version":"4.0.1"},"reference-count":41,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2020,9,1]],"date-time":"2020-09-01T00:00:00Z","timestamp":1598918400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Salmonella is a leading cause of bacterial infections in animals and humans. We sequenced a collection of 450 Salmonella strains from diseased animals to better understand the genetic makeup of their virulence and resistance features. The presence of Salmonella pathogenicity islands (SPIs) varied by serotype. S. Enteritidis carried the most SPIs (n = 15), while S. Mbandaka, S. Cerro, S. Meleagridis, and S. Havana carried the least (n = 10). S. Typhimurium, S. Choleraesuis, S. I 4,5,12:i:-, and S. Enteritidis each contained the spv operon on IncFII or IncFII-IncFIB hybrid plasmids. Two S. IIIa carried a spv operon with spvD deletion on the chromosome. Twelve plasmid types including 24 hybrid plasmids were identified. IncA\/C was frequently associated with S. Newport (83%) and S. Agona (100%) from bovine, whereas IncFII (100%), IncFIB (100%), and IncQ1 (94%) were seen in S. Choleraesuis from swine. IncX (100%) was detected in all S. Kentucky from chicken. A total of 60 antimicrobial resistance genes (ARGs), four disinfectant resistances genes (DRGs) and 33 heavy metal resistance genes (HMRGs) were identified. The Salmonella strains from sick animals contained various SPIs, resistance genes and plasmid types based on the serotype and source of the isolates. Such complicated genomic structures shed light on the strain characteristics contributing to the severity of disease and treatment failures in Salmonella infections, including those causing illnesses in animals.<\/jats:p>","DOI":"10.3390\/genes11091025","type":"journal-article","created":{"date-parts":[[2020,9,1]],"date-time":"2020-09-01T14:21:10Z","timestamp":1598970070000},"page":"1025","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":51,"title":["Comparative Genomic Analysis of 450 Strains of Salmonella enterica Isolated from Diseased Animals"],"prefix":"10.3390","volume":"11","author":[{"given":"Shaohua","family":"Zhao","sequence":"first","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cong","family":"Li","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chih-Hao","family":"Hsu","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gregory H.","family":"Tyson","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Errol","family":"Strain","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heather","family":"Tate","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thu-Thuy","family":"Tran","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason","family":"Abbott","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick F.","family":"McDermott","sequence":"additional","affiliation":[{"name":"Center for Veterinary Medicine, U.S. Food and Drug Administration, Laurel, MD 20708, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,9,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1128\/JB.185.2.553-563.2003","article-title":"Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar typhimurium DNA microarray","volume":"185","author":"Chan","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2279","DOI":"10.1101\/gr.091017.109","article-title":"Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype","volume":"19","author":"Kingsley","year":"2009","journal-title":"Genome Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1786","DOI":"10.1128\/iai.65.5.1786-1792.1997","article-title":"The spv genes on the Salmonella dublin virulence plasmid are required for severe enteritis and systemic infection in the natural host","volume":"65","author":"Libby","year":"1997","journal-title":"Infect. Immun."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1574-6968.2010.01904.x","article-title":"So similar, yet so different: Uncovering distinctive features in the genomes of Salmonella enterica serovars Typhimurium and Typhi","volume":"305","author":"Sabbagh","year":"2010","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2709","DOI":"10.1098\/rstb.2009.0094","article-title":"Molecular insights into farm animal and zoonotic Salmonella infections","volume":"364","author":"Stevens","year":"2009","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_6","first-page":"317","article-title":"Salmonella pathogenicity islands in host specificity, host pathogen-interactions and antibiotics resistance of Salmonella enterica","volume":"120","author":"Gerlach","year":"2007","journal-title":"Berl. Munch. Tierarztl. Wochenschr."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.ijmm.2004.06.025","article-title":"Evolution of pathogenicity islands of Salmonella enterica","volume":"294","author":"Hensel","year":"2004","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Rychlik, I., Karasova, D., Sebkova, A., Volf, J., Sisak, F., Havlickova, H., Kummer, V., Imre, A., Szmolka, A., and Nagy, B. (2009). Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens. BMC Microbiol., 9.","DOI":"10.1186\/1471-2180-9-268"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Suez, J., Porwollik, S., Dagan, A., Marzel, A., Schorr, Y.I., Desai, P.T., Agmon, V., McClelland, M., Rahav, G., and Gal-Mor, O. (2013). Virulence gene profiling and pathogenicity characterization of non-typhoidal Salmonella accounted for invasive disease in humans. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0058449"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3624","DOI":"10.1128\/JB.185.12.3624-3635.2003","article-title":"Variation between pathogenic serovars within Salmonella pathogenicity islands","volume":"185","author":"Amavisit","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/0966-842X(96)30013-9","article-title":"Bacterial responses to host-defense peptides","volume":"4","author":"Groisman","year":"1996","journal-title":"Trends Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/S1286-4579(00)00273-2","article-title":"Salmonella pathogenicity islands: Big virulence in small packages","volume":"2","author":"Marcus","year":"2000","journal-title":"Microbes Infect."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Blondel, C.J., Jimenez, J.C., Contreras, I., and Santiviago, C.A. (2009). Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genom., 10.","DOI":"10.1186\/1471-2164-10-354"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Hayward, M.R., AbuOun, M., La Ragione, R.M., Tchorzewska, M.A., Cooley, W.A., Everest, D.J., Petrovska, L., Jansen, V.A., and Woodward, M.J. (2014). SPI-23 of S. Derby: Role in adherence and invasion of porcine tissues. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0107857"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Fookes, M., Schroeder, G.N., Langridge, G.C., Blondel, C.J., Mammina, C., Connor, T.R., Seth-Smith, H., Vernikos, G.S., Robinson, K.S., and Sanders, M. (2011). Salmonella bongori provides insights into the evolution of the Salmonellae. PLoS Pathog., 7.","DOI":"10.1371\/journal.ppat.1002191"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1089\/mdr.2019.0045","article-title":"Comparative Genomic Analysis of Virulence, Antimicrobial Resistance, and Plasmid Profiles of Salmonella Dublin Isolated from Sick Cattle, Retail Beef, and Humans in the United States","volume":"25","author":"Hsu","year":"2019","journal-title":"Microb. Drug Resist."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1574-6968.1994.tb07253.x","article-title":"Plasmid-mediated virulence genes in non-typhoid Salmonella serovars","volume":"124","author":"Guiney","year":"1994","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"S146","DOI":"10.1093\/clinids\/21.Supplement_2.S146","article-title":"Biology and clinical significance of virulence plasmids in Salmonella serovars","volume":"21","author":"Guiney","year":"1995","journal-title":"Clin. Infect Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1128\/iai.61.2.504-511.1993","article-title":"The Salmonella typhimurium virulence plasmid increases the growth rate of salmonellae in mice","volume":"61","author":"Gulig","year":"1993","journal-title":"Infect. Immun."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2612","DOI":"10.1128\/IAI.69.4.2612-2620.2001","article-title":"Complete DNA sequence and comparative analysis of the 50-kilobase virulence plasmid of Salmonella enterica serovar Choleraesuis","volume":"69","author":"Haneda","year":"2001","journal-title":"Infect. Immun."},{"key":"ref_21","first-page":"177","article-title":"The virulence plasmids of Salmonella","volume":"2","author":"Rotger","year":"1999","journal-title":"Int. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.vetmic.2007.03.001","article-title":"Characterization of multidrug resistant Salmonella recovered from diseased animals","volume":"123","author":"Zhao","year":"2007","journal-title":"Vet. Microbiol."},{"key":"ref_23","unstructured":"FDA (2017). National Antimicrobial Resistance Monitoring System (NARMS): 2017 Report."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1080\/10495390600957092","article-title":"Genetics of antimicrobial resistance","volume":"17","author":"Harbottle","year":"2006","journal-title":"Anim. Biotechnol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"832","DOI":"10.3389\/fmicb.2019.00832","article-title":"Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals","volume":"10","author":"McMillan","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_26","unstructured":"Aarestrup, F.M., Schwarz, S., Shen, J., and Cavaco, L. (2018). Antimicrobial Resistance in nontyphoidal Salmonella. Antimicrobial Resistance in Bacteria from Livestock and Companion Animals, ASM Press."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1951","DOI":"10.3201\/eid2011.140889","article-title":"Multidrug-resistant IncA\/C plasmid in Vibrio cholerae from Haiti","volume":"20","author":"Folster","year":"2014","journal-title":"Emerg Infect. Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"6614","DOI":"10.1093\/nar\/gkw569","article-title":"NCBI prokaryotic genome annotation pipeline","volume":"44","author":"Tatusova","year":"2016","journal-title":"Nucleic. Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1186\/s13059-015-0849-0","article-title":"Circlator: Automated circularization of genome assemblies using long sequencing reads","volume":"16","author":"Hunt","year":"2015","journal-title":"Genome Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1525","DOI":"10.2217\/fmb.10.122","article-title":"Salmonella genomic islands and antibiotic resistance in Salmonella enterica","volume":"5","author":"Hall","year":"2010","journal-title":"Future Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3216","DOI":"10.1093\/jac\/dku314","article-title":"Proteus genomic island 1 (PGI1), a new resistance genomic island from two Proteus mirabilis French clinical isolates","volume":"69","author":"Siebor","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"11058","DOI":"10.1038\/s41598-019-45838-0","article-title":"Genomic Features of High-Priority Salmonella enterica Serovars Circulating in the Food Production Chain, Brazil, 2000-2016","volume":"9","author":"Monte","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Silva, C., Puente, J.L., and Calva, E. (2017). Salmonella virulence plasmid: Pathogenesis and ecology. Pathog. Dis.","DOI":"10.1093\/femspd\/ftx070"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"3290","DOI":"10.1128\/IAI.70.6.3290-3294.2002","article-title":"Characterization of the spv locus in Salmonella enterica serovar Arizona","volume":"70","author":"Libby","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Mohammed, M., Le Hello, S., Leekitcharoenphon, P., and Hendriksen, R. (2017). The invasome of Salmonella Dublin as revealed by whole genome sequencing. BMC Infect. Dis., 17.","DOI":"10.1186\/s12879-017-2628-x"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Mangat, C.S., Bekal, S., Irwin, R.J., and Mulvey, M.R. (2017). A Novel Hybrid Plasmid Carrying Multiple Antimicrobial Resistance and Virulence Genes in Salmonella enterica Serovar Dublin. Antimicrob. Agents Chemother., 61.","DOI":"10.1128\/AAC.02601-16"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1058","DOI":"10.1016\/j.meegid.2012.03.004","article-title":"Inheritance of the Salmonella virulence plasmids: Mostly vertical and rarely horizontal","volume":"12","author":"Feng","year":"2012","journal-title":"Infect. Genet Evol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5366","DOI":"10.1128\/JCM.41.12.5366-5371.2003","article-title":"Characterization of Salmonella enterica serotype newport isolated from humans and food animals","volume":"41","author":"Zhao","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_39","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_40","doi-asserted-by":"crossref","unstructured":"de Curraize, C., Amoureux, L., Bador, J., Chapuis, A., Siebor, E., Clement, C., Sauge, J., Aho-Glele, L.S., and Neuwirth, C. (2017). \u201cDoes the Salmonella Genomic Island 1 (SGI1) confer invasiveness properties to human isolates?\u201d. BMC Infect. Dis., 17.","DOI":"10.1186\/s12879-017-2847-1"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Yang, S., Deng, W., Liu, S., Yu, X., Mustafa, G.R., Chen, S., He, L., Ao, X., Yang, Y., and Zhou, K. (2020). Presence of Heavy Metal Resistance Genes in Escherichia coli and Salmonella, and Analysis of Resistance Gene Structure in E. coli E308. J. Glob. Antimicrob. Resist.","DOI":"10.1016\/j.jgar.2020.01.009"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/9\/1025\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:05:40Z","timestamp":1760177140000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/9\/1025"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,9,1]]},"references-count":41,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2020,9]]}},"alternative-id":["genes11091025"],"URL":"https:\/\/doi.org\/10.3390\/genes11091025","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,9,1]]}}}