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http://dx.doi.org/10.4014/jmb.1904.04028

Comparative Genomics Approaches to Understanding Virulence and Antimicrobial Resistance of Salmonella Typhimurium ST1539 Isolated from a Poultry Slaughterhouse in Korea  

Kim, Eunsuk (Department of Molecular Science and Technology, Ajou University)
Park, Soyeon (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Cho, Seongbeom (Department of Veterinary Pathobiology and Preventive Medicine, Research Institute for Veterinary Science and College of Veterinary Medicine, Seoul National University)
Hahn, Tae-Wook (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Yoon, Hyunjin (Department of Molecular Science and Technology, Ajou University)
Publication Information
Journal of Microbiology and Biotechnology / v.29, no.6, 2019 , pp. 962-972 More about this Journal
Abstract
Non-typhoidal Salmonella (NTS) is one of the most frequent causes of bacterial foodborne illnesses. Considering that the main reservoir of NTS is the intestinal tract of livestock, foods of animal origin are regarded as the main vehicles of Salmonella infection. In particular, poultry colonized with Salmonella Typhimurium (S. Typhimurium), a dominant serotype responsible for human infections, do not exhibit overt signs and symptoms, thereby posing a potential health risk to humans. In this study, comparative genomics approaches were applied to two S. Typhimurium strains, ST1539 and ST1120, isolated from a duck slaughterhouse and a pig farm, respectively, to characterize their virulence and antimicrobial resistance-associated genomic determinants. ST1539 containing a chromosome (4,905,039 bp; 4,403 CDSs) and a plasmid (93,876 bp; 96 CDSs) was phylogenetically distinct from other S. Typhimurium strains such as ST1120 and LT2. Compared to the ST1120 genome (previously deposited in GenBank; CP021909.1 and CP021910.1), ST1539 possesses more virulence determinants, including ST64B prophage, plasmid spv operon encoding virulence factors, genes encoding SseJ effector, Rck invasin, and biofilm-forming factors (bcf operon and pefAB). In accordance with the in silico prediction, ST1539 exhibited higher cytotoxicity against epithelial cells, better survival inside macrophage cells, and faster mice-killing activity than ST1120. However, ST1539 showed less resistance against antibiotics than ST1120, which may be attributed to the multiple resistanceassociated genes in the ST1120 chromosome. The accumulation of comparative genomics data on S. Typhimurium isolates from livestock would enrich our understanding of strategies Salmonella employs to adapt to diverse host animals.
Keywords
Salmonella Typhimurium; comparative genomics; virulence; antibiotic resistance;
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1 Popoff MY, Bockemühl J, Gheesling LL. 2004. Supplement 2002 (no. 46) to the Kauffmann-White scheme. Res. Microbiol. 155: 568-570.   DOI
2 LIm S-K, Nam H-M, Lee H-S, Kim A-R, Jang G-C, Jung S-C, Kim T-S. 2013. Prevalence and characterization of apramycinresistant Salmonella enterica serotype Typhimurium isolated from healthy and diseased pigs in Korea during 1998 through 2009. J. Food Prot. 76: 1443-1446.   DOI
3 Cho S-H, Lim Y-S, Kang Y-H. 2012. Comparison of antimicrobial resistance in Escherichia coli strains isolated from healthy poultry and swine farm workers using antibiotics in Korea. Osong Public Health Res. Perspect. 3: 151-155.   DOI
4 APQA. 2017. Antimicrobial consumption in livestock and Monitoring of antimicrobial resistance in animals and carcasses, 2017. pp75-76. Animal and Plant Quarantine Agency, Gimcheon-si, Gyeongsangbuk-do.
5 Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, Banks G, et al. 1998. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30: 163-174.   DOI
6 Lostroh CP, Lee CA. 2001. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 3: 1281-1291.   DOI
7 Casjens S. 2003. Prophages and bacterial genomics: what have we learned so far? Mol. Microbiol. 49: 277-300.   DOI
8 Hopkins S, Muller-Pebody B. 2015. UK one health report: joint report on human and animal antibiotic use, sales and resistance, 2013.
9 Yoon R-H, Cha S-Y, Wei B, Roh J-H, Seo H-S, Oh J-Y, et al. 2014. Prevalence of Salmonella isolates and antimicrobial resistance in poultry meat from South Korea. J. Food Prt. 77: 1579-1582.   DOI
10 Yang B, Cui Y , Shi C, Wang J, Xia X , Xi M, et al. 2014. Counts, serotypes, and antimicrobial resistance of Salmonella isolates on retail raw poultry in the People's Republic of China. J. Food Prot. 77: 894-902.   DOI
11 Antunes P, Mourao J, Campos J, Peixe L. 2016. Salmonellosis: the role of poultry meat. Clin. Microbiol. Infect. 22: 110-121.   DOI
12 Kim S, Kim E, Park S, Hahn TW, Yoon H. 2017. Genomic approaches for understanding the characteristics of Salmonella enterica subsp. enterica Serovar Typhimurium ST1120, Isolated from Swine Feces in Korea. J. Microbiol. Biotechnol. 27: 1983-1993.   DOI
13 McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, et al. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852.   DOI
14 Jarvik T, Smillie C , Groisman EA, Ochman H. 2010. Shortterm signatures of evolutionary change in the Salmonella enterica serovar Typhimurium 14028 genome. J. Bacteriol. 192: 560-567.   DOI
15 Kroger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, et al. 2012. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc. Natl. Acad. Sci. USA 109: E1277-E1286.   DOI
16 Chin C-S, Alexander DH, Marks P , Klammer AA, Drake J , Heiner C, et al. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10: 563-569.   DOI
17 Swords WE, Cannon BM, Benjamin W. 1997. Avirulence of LT2 strains of Salmonella typhimurium results from a defective rpoS gene. Infect. Immun. 65: 2451-2453.   DOI
18 Mmolawa PT, Willmore R, Thomas CJ, Heuzenroeder MW. 2002. Temperate phages in Salmonella enterica serovar Typhimurium: implications for epidemiology. Int. J. Med. Microbiol. 291: 633-644.   DOI
19 Herrero-Fresno A, Leekitcharoenphon P, Hendriksen RS, Olsen JE, Aarestrup FM. 2014. Analysis of the contribution of bacteriophage ST64B to in vitro virulence traits of Salmonella enterica serovar Typhimurium. J. Med. Microbiol. 63: 331-342.   DOI
20 Brown NF, Coombes BK, Bishop JL, Wickham ME, Lowden MJ, Gal-Mor O, et al. 2011. Salmonella phage ST64B encodes a member of the SseK/NleB effector family. PLoS One 6: e17824.   DOI
21 Wilmes-Riesenberg MR, Foster JW, Curtiss R. 1997. An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect. Immun. 65: 203-210.   DOI
22 Chappell L, Kaiser P, Barrow P, Jones MA, Johnston C, Wigley P. 2009. The immunobiology of avian systemic salmonellosis. Vet. Immun. Immunopathol. 128: 53-59.   DOI
23 Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.   DOI
24 Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.   DOI
25 Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5: R12.   DOI
26 Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068-2069.   DOI
27 Lukashin AV, Borodovsky M. 1998. GeneMark. hmm: new solutions for gene finding. Nucleic Acids Res. 26: 1107-1115.   DOI
28 Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35: 3100-3108.   DOI
29 Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.   DOI
30 Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. 2008. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
31 Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart D S. 2011. PHAST: a fast phage search tool. Nucleic Acids Res. 39: W347-352.   DOI
32 Richter M, Rossello-Mora R, Oliver Glöckner F, Peplies J. 2015. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32: 929-931.   DOI
33 Chen L, Yang J, Yu J, Y ao Z , Sun L, Shen Y, Jin Q . 2005. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 33: D325-D328.   DOI
34 Yoshida CE, Kruczkiewicz P, Laing CR, Lingohr EJ, Gannon VP, Nash JH, et al 2016. The Salmonella in silico typing resource (SISTR): an open web-accessible tool for rapidly typing and subtyping draft Salmonella genome assemblies. PLoS One 11: e0147101.   DOI
35 Tatusova TA, Madden TL. 1999. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174: 247-250.   DOI
36 Sullivan MJ, Petty NK, Beatson SA. 2011. Easyfig: a genome comparison visualizer. Bioinformatics 27: 1009-1010.   DOI
37 Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. 2016. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 45: D566-D573.   DOI
38 Kozyreva VK, C randall J, Sabol A, Poe A , Zhang P , Concepcion-Acevedo J, et al. 2016. Laboratory investigation of Salmonella enterica serovar Poona outbreak in California: comparison of pulsed-field gel electrophoresis (PFGE) and whole genome sequencing (WGS) results. PLoS Curr. 8.
39 Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsedfield gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33: 2233-2239.   DOI
40 Wonderling L, Pearce R, Wallace FM, Call JE, Feder I, Tamplin M, et al. 2003. Use of pulsed-field gel electrophoresis to characterize the heterogeneity and clonality of Salmonella isolates obtained from the carcasses and feces of swine at slaughter. Appl. Environ. Microbiol. 69: 4177-4182.   DOI
41 Seo Y-S, Lee S-H, Shin E-K, Kim S-J, Jung R, Hahn T-W. 2006. Pulsed-field gel electrophoresis genotyping of Salmonella gallinarum and comparison with random amplified polymorphic DNA. Vet. Microbiol. 115: 349-357.   DOI
42 Hudzicki J. 2009. Kirby-Bauer disk diffusion susceptibility test protocol.
43 Reller LB, Weinstein M, Jorgensen JH, Ferraro MJ. 2009. Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin. Infect. Dis. 49: 1749-1755.   DOI
44 Jackson B R, Griffin PM, Cole D , Walsh KA, Chai SJ. 2013. Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998-2008. Emerg. Infect. Dis. 19: 1239-1244.   DOI
45 Chen H-M, Wang Y, Su L-H, Chiu C-H. 2013. N ontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatr. Neonatol. 54: 147-152.   DOI
46 Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM. 2015. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin. Microbiol. Rev. 28: 901-937.   DOI
47 Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D'Angelo M, Hurd S, et al. 2008. Salmonellosis outcomes differ substantially by serotype. J. Infect. Dis. 198: 109-114.   DOI
48 Barrow P, Huggins M, Lovell M, Simpson J. 1987. Observations on the pathogenesis of experimental Salmonella typhimurium infection in chickens. Res.Vet. Sci. 42: 194-199.   DOI
49 McEwen SA, Fedorka-Cray PJ. 2002. Antimicrobial use and resistance in animals. Clin. Infect. Dis. 34: S93-S106.   DOI
50 Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. 2015. Global trends in antimicrobial use in food animals. Proc. Natl. Acad. Sci. USA 112: 5649-5654.   DOI
51 Oladeinde A, Cook K, Orlek A, Zock G, Herrington K, Cox N, et al. 2018. Hotspot mutations and ColE1 plasmids contribute to the fitness of Salmonella Heidelberg in poultry litter. PLoS One 13: e0202286.   DOI
52 Mottawea W, Duceppe M-O, Dupras AA, Usongo V, Jeukens J, Freschi L, et al. 2018. Salmonella enterica prophage sequence profiles reflect genome diversity and can be used for high discrimination subtyping. Front. Microbiol. 9:836.   DOI