Genomic comparison of diverse Salmonella serovars isolated from swine
Autoři:
Sushim K. Gupta aff001; Poonam Sharma aff001; Elizabeth A. McMillan aff001; Charlene R. Jackson aff001; Lari M. Hiott aff001; Tiffanie Woodley aff001; Shaheen B. Humayoun aff001; John B. Barrett aff001; Jonathan G. Frye aff001; Michael McClelland aff003
Působiště autorů:
Bacterial Epidemiology and Antimicrobial Resistance Unit, USDA-ARS, Athens, GA, United States of America
aff001; Department of Microbiology, University of Georgia, Athens, GA, United States of America
aff002; Department of Microbiology and Molecular Genetics, University of California Irvine, Irvine, CA, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0224518
Souhrn
Food animals act as a reservoir for many foodborne pathogens. Salmonella enterica is one of the leading pathogens that cause food borne illness in a broad host range including animals and humans. They can also be associated with a single host species or a subset of hosts, due to genetic factors associated with colonization and infection. Adult swine are often asymptomatic carriers of a broad range of Salmonella servoars and can act as an important reservoir of infections for humans. In order to understand the genetic variations among different Salmonella serovars, Whole Genome Sequences (WGS) of fourteen Salmonella serovars from swine products were analyzed. More than 75% of the genes were part of the core genome in each isolate and the higher fraction of gene assign to different functional categories in dispensable genes indicated that these genes acquired for better adaptability and diversity. High concordance (97%) was detected between phenotypically confirmed antibiotic resistances and identified antibiotic resistance genes from WGS. The resistance determinants were mainly located on mobile genetic elements (MGE) on plasmids or integrated into the chromosome. Most of known and putative virulence genes were part of the core genome, but a small fraction were detected on MGE. Predicted integrated phage were highly diverse and many harbored virulence, metal resistance, or antibiotic resistance genes. CRISPR (Clustered regularly interspaced short palindromic repeats) patterns revealed the common ancestry or infection history among Salmonella serovars. Overall genomic analysis revealed a great deal of diversity among Salmonella serovars due to acquired genes that enable them to thrive and survive during infection.
Klíčová slova:
Antibiotic resistance – Antimicrobial resistance – Bacteriophages – CRISPR – Salmonella – Salmonella typhimurium – Swine – Salmonella enterica
Zdroje
1. Chan K, Baker S, Kim CC, Detweiler CS, Dougan G, Falkow S. Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar typhimurium DNA microarray. J Bacteriol. 2003;185(2):553–63. doi: 10.1128/JB.185.2.553-563.2003 12511502; PubMed Central PMCID: PMC145314.
2. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17(1):7–15. doi: 10.3201/eid1701.091101p1 21192848; PubMed Central PMCID: PMC3375761.
3. Minor T, Lasher A, Klontz K, Brown B, Nardinelli C, Zorn D. The Per Case and Total Annual Costs of Foodborne Illness in the United States. Risk Anal. 2015;35(6):1125–39. doi: 10.1111/risa.12316 25557397.
4. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemuhl J, Grimont PA, et al. Supplement 2003–2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol. 2010;161(1):26–9. doi: 10.1016/j.resmic.2009.10.002 19840847.
5. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 2010;74(3):417–33. doi: 10.1128/MMBR.00016-10 20805405; PubMed Central PMCID: PMC2937522.
6. Davies SC, Fowler T, Watson J, Livermore DM, Walker D. Annual Report of the Chief Medical Officer: infection and the rise of antimicrobial resistance. Lancet. 2013;381(9878):1606–9. doi: 10.1016/S0140-6736(13)60604-2 23489756.
7. Fricke WF, Mammel MK, McDermott PF, Tartera C, White DG, Leclerc JE, et al. Comparative genomics of 28 Salmonella enterica isolates: evidence for CRISPR-mediated adaptive sublineage evolution. J Bacteriol. 2011;193(14):3556–68. doi: 10.1128/JB.00297-11 21602358; PubMed Central PMCID: PMC3133335.
8. Carattoli A. Plasmids and the spread of resistance. Int J Med Microbiol. 2013;303(6–7):298–304. doi: 10.1016/j.ijmm.2013.02.001 23499304.
9. Chu C, Hong SF, Tsai C, Lin WS, Liu TP, Ou JT. Comparative physical and genetic maps of the virulence plasmids of Salmonella enterica serovars typhimurium, enteritidis, choleraesuis, and dublin. Infect Immun. 1999;67(5):2611–4. 10225928; PubMed Central PMCID: PMC116011.
10. Garcia P, Guerra B, Bances M, Mendoza MC, Rodicio MR. IncA/C plasmids mediate antimicrobial resistance linked to virulence genes in the Spanish clone of the emerging Salmonella enterica serotype 4,[5],12:i. J Antimicrob Chemother. 2011;66(3):543–9. doi: 10.1093/jac/dkq481 21177672.
11. Hoffmann M, Pettengill JB, Gonzalez-Escalona N, Miller J, Ayers SL, Zhao S, et al. Comparative Sequence Analysis of Multidrug-Resistant IncA/C Plasmids from Salmonella enterica. Front Microbiol. 2017;8:1459. doi: 10.3389/fmicb.2017.01459 28824587; PubMed Central PMCID: PMC5545573.
12. Suttle CA. Marine viruses—major players in the global ecosystem. Nat Rev Microbiol. 2007;5(10):801–12. Epub 2007/09/15. doi: 10.1038/nrmicro1750 17853907.
13. Boyd EF, Brussow H. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 2002;10(11):521–9. Epub 2002/11/07. doi: 10.1016/s0966-842x(02)02459-9 12419617.
14. Hooton SP, Timms AR, Rowsell J, Wilson R, Connerton IF. Salmonella Typhimurium-specific bacteriophage PhiSH19 and the origins of species specificity in the Vi01-like phage family. Virol J. 2011;8:498. Epub 2011/11/04. doi: 10.1186/1743-422X-8-498 22047448; PubMed Central PMCID: PMC3220722.
15. Kropinski AM, Sulakvelidze A, Konczy P, Poppe C. Salmonella phages and prophages—genomics and practical aspects. Methods Mol Biol. 2007;394:133–75. Epub 2008/03/28. doi: 10.1007/978-1-59745-512-1_9 18363236.
16. Price-Carter M, Roy-Chowdhury P, Pope CE, Paine S, de Lisle GW, Collins DM, et al. The evolution and distribution of phage ST160 within Salmonella enterica serotype Typhimurium. Epidemiol Infect. 2011;139(8):1262–71. Epub 2010/10/19. doi: 10.1017/S0950268810002335 20950514.
17. Barrangou R, Marraffini LA. CRISPR-Cas systems: Prokaryotes upgrade to adaptive immunity. Mol Cell. 2014;54(2):234–44. Epub 2014/04/29. doi: 10.1016/j.molcel.2014.03.011 24766887; PubMed Central PMCID: PMC4025954.
18. Horvath P, Romero DA, Coute-Monvoisin AC, Richards M, Deveau H, Moineau S, et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol. 2008;190(4):1401–12. Epub 2007/12/11. doi: 10.1128/JB.01415-07 18065539; PubMed Central PMCID: PMC2238196.
19. McDermott PF, Tyson GH, Kabera C, Chen Y, Li C, Folster JP, et al. Whole-Genome Sequencing for Detecting Antimicrobial Resistance in Nontyphoidal Salmonella. Antimicrob Agents Chemother. 2016;60(9):5515–20. doi: 10.1128/AAC.01030-16 27381390; PubMed Central PMCID: PMC4997858.
20. Pornsukarom S, van Vliet AHM, Thakur S. Whole genome sequencing analysis of multiple Salmonella serovars provides insights into phylogenetic relatedness, antimicrobial resistance, and virulence markers across humans, food animals and agriculture environmental sources. BMC Genomics. 2018;19(1):801. doi: 10.1186/s12864-018-5137-4 30400810; PubMed Central PMCID: PMC6218967.
21. CLSI. Performance standards for antimicrobial susceptibility testing: 25th informational supplement (m100-S25). Clinical and Laboratory Standards Institute. 2015.
22. McMillan EAG, S. K.; Williams L.; Jove T.; Hiott L. M.; Woodley T. A.; Barrett J. B.; Jackson C. R.; Wasilenko J. L.; Simmons M.; Tillman G. E.; McClelland M.; Frye J. G. Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals. Frontiers in Microbiology. 2019;10:832. doi: 10.3389/fmicb.2019.00832 31057528
23. Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics. 2015;31(4):587–9. doi: 10.1093/bioinformatics/btu661 25338718.
24. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–9. Epub 2014/03/20. doi: 10.1093/bioinformatics/btu153 24642063.
25. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31(22):3691–3. Epub 2015/07/23. doi: 10.1093/bioinformatics/btv421 26198102; PubMed Central PMCID: PMC4817141.
26. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003;4:41. doi: 10.1186/1471-2105-4-41 12969510; PubMed Central PMCID: PMC222959.
27. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother. 2014;58(1):212–20. Epub 2013/10/23. doi: 10.1128/AAC.01310-13 24145532; PubMed Central PMCID: PMC3910750.
28. Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DG. BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res. 2014;42(Database issue):D737–43. doi: 10.1093/nar/gkt1252 24304895; PubMed Central PMCID: PMC3965030.
29. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 2005;33(Database issue):D325–8. Epub 2004/12/21. doi: 10.1093/nar/gki008 15608208; PubMed Central PMCID: PMC539962.
30. Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016;44(W1):W16–21. doi: 10.1093/nar/gkw387 27141966; PubMed Central PMCID: PMC4987931.
31. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35(Web Server issue):W52–7. Epub 2007/06/01. doi: 10.1093/nar/gkm360 17537822; PubMed Central PMCID: PMC1933234.
32. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011;27(7):1009–10. doi: 10.1093/bioinformatics/btr039 21278367; PubMed Central PMCID: PMC3065679.
33. Moura A, Soares M, Pereira C, Leitao N, Henriques I, Correia A. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics. 2009;25(8):1096–8. doi: 10.1093/bioinformatics/btp105 19228805.
34. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895–903. doi: 10.1128/AAC.02412-14 24777092; PubMed Central PMCID: PMC4068535.
35. Kisand V, Lettieri T. Genome sequencing of bacteria: sequencing, de novo assembly and rapid analysis using open source tools. BMC Genomics. 2013;14:211. doi: 10.1186/1471-2164-14-211 23547799; PubMed Central PMCID: PMC3618134.
36. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature. 2001;413(6858):852–6. doi: 10.1038/35101614 11677609.
37. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A. 2005;102(7):2567–72. doi: 10.1073/pnas.0409727102 15701695; PubMed Central PMCID: PMC549018.
38. Tyson GH, McDermott PF, Li C, Chen Y, Tadesse DA, Mukherjee S, et al. WGS accurately predicts antimicrobial resistance in Escherichia coli. J Antimicrob Chemother. 2015;70(10):2763–9. doi: 10.1093/jac/dkv186 26142410.
39. Ramirez MS, Tolmasky ME. Aminoglycoside modifying enzymes. Drug Resist Updat. 2010;13(6):151–71. doi: 10.1016/j.drup.2010.08.003 20833577; PubMed Central PMCID: PMC2992599.
40. Magnet S, Courvalin P, Lambert T. Activation of the cryptic aac(6')-Iy aminoglycoside resistance gene of Salmonella by a chromosomal deletion generating a transcriptional fusion. J Bacteriol. 1999;181(21):6650–5. 10542165; PubMed Central PMCID: PMC94128.
41. Carattoli A. Animal reservoirs for extended spectrum beta-lactamase producers. Clin Microbiol Infect. 2008;14 Suppl 1:117–23. doi: 10.1111/j.1469-0691.2007.01851.x 18154535.
42. Frye JG, Jackson CR. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Front Microbiol. 2013;4:135. doi: 10.3389/fmicb.2013.00135 23734150; PubMed Central PMCID: PMC3661942.
43. Scholz P, Haring V, Wittmann-Liebold B, Ashman K, Bagdasarian M, Scherzinger E. Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene. 1989;75(2):271–88. doi: 10.1016/0378-1119(89)90273-4 2653965.
44. Cambray G, Guerout AM, Mazel D. Integrons. Annu Rev Genet. 2010;44:141–66. doi: 10.1146/annurev-genet-102209-163504 20707672.
45. Benacer D, Thong KL, Watanabe H, Puthucheary SD. Characterization of drug resistant Salmonella enterica serotype Typhimurium by antibiograms, plasmids, integrons, resistance genes and PFGE. J Microbiol Biotechnol. 2010;20(6):1042–52. doi: 10.4014/jmb.0910.10028 20622506.
46. Frye JG, Lindsey RL, Meinersmann RJ, Berrang ME, Jackson CR, Englen MD, et al. Related antimicrobial resistance genes detected in different bacterial species co-isolated from swine fecal samples. Foodborne Pathog Dis. 2011;8(6):663–79. doi: 10.1089/fpd.2010.0695 21385089.
47. Lopes GV, Michael GB, Cardoso M, Schwarz S. Antimicrobial resistance and class 1 integron-associated gene cassettes in Salmonella enterica serovar Typhimurium isolated from pigs at slaughter and abattoir environment. Vet Microbiol. 2016;194:84–92. doi: 10.1016/j.vetmic.2016.04.020 27142182.
48. Roberts MC. Update on acquired tetracycline resistance genes. FEMS Microbiol Lett. 2005;245(2):195–203. doi: 10.1016/j.femsle.2005.02.034 15837373.
49. Daly M, Villa L, Pezzella C, Fanning S, Carattoli A. Comparison of multidrug resistance gene regions between two geographically unrelated Salmonella serotypes. J Antimicrob Chemother. 2005;55(4):558–61. doi: 10.1093/jac/dki015 15722395.
50. Peters ED, Leverstein-van Hall MA, Box AT, Verhoef J, Fluit AC. Novel gene cassettes and integrons. Antimicrob Agents Chemother. 2001;45(10):2961–4. doi: 10.1128/AAC.45.10.2961-2964.2001 11557503; PubMed Central PMCID: PMC90765.
51. Abatcha MG, Effarizah ME, Rusul G. Antibiotic susceptibility and molecular characterization of Salmonella enterica serovar Paratyphi B isolated from vegetables and processing environment in Malaysia. Int J Food Microbiol. 2019;290:180–3. doi: 10.1016/j.ijfoodmicro.2018.09.021 30342248.
52. Hsu SC, Chiu TH, Pang JC, Hsuan-Yuan CH, Chang GN, Tsen HY. Characterisation of antimicrobial resistance patterns and class 1 integrons among Escherichia coli and Salmonella enterica serovar Choleraesuis strains isolated from humans and swine in Taiwan. Int J Antimicrob Agents. 2006;27(5):383–91. doi: 10.1016/j.ijantimicag.2005.11.020 16621462.
53. Khemtong S, Chuanchuen R. Class 1 integrons and Salmonella genomic island 1 among Salmonella enterica isolated from poultry and swine. Microb Drug Resist. 2008;14(1):65–70. doi: 10.1089/mdr.2008.0807 18328001.
54. Kwon HJ, Kim TE, Cho SH, Seol JG, Kim BJ, Hyun JW, et al. Distribution and characterization of class 1 integrons in Salmonella enterica serotype Gallinarum biotype Gallinarum. Vet Microbiol. 2002;89(4):303–9. doi: 10.1016/s0378-1135(02)00257-2 12383639.
55. Adesiji YO, Deekshit VK, Karunasagar I. Antimicrobial-resistant genes associated with Salmonella spp. isolated from human, poultry, and seafood sources. Food Sci Nutr. 2014;2(4):436–42. doi: 10.1002/fsn3.119 25473501; PubMed Central PMCID: PMC4221842.
56. Almeida F, Seribelli AA, Medeiros MIC, Rodrigues DDP, de MelloVarani A, Luo Y, et al. Phylogenetic and antimicrobial resistance gene analysis of Salmonella Typhimurium strains isolated in Brazil by whole genome sequencing. PLoS One. 2018;13(8):e0201882. doi: 10.1371/journal.pone.0201882 30102733; PubMed Central PMCID: PMC6089434.
57. El-Sharkawy H, Tahoun A, El-Gohary AEA, El-Abasy M, El-Khayat F, Gillespie T, et al. Epidemiological, molecular characterization and antibiotic resistance of Salmonella enterica serovars isolated from chicken farms in Egypt. Gut Pathog. 2017;9:8. doi: 10.1186/s13099-017-0157-1 28203289; PubMed Central PMCID: PMC5301364.
58. Guerra B, Junker E, Helmuth R. Incidence of the recently described sulfonamide resistance gene sul3 among German Salmonella enterica strains isolated from livestock and food. Antimicrob Agents Chemother. 2004;48(7):2712–5. doi: 10.1128/AAC.48.7.2712-2715.2004 15215132; PubMed Central PMCID: PMC434208.
59. Infante B, Grape M, Larsson M, Kristiansson C, Pallecchi L, Rossolini GM, et al. Acquired sulphonamide resistance genes in faecal Escherichia coli from healthy children in Bolivia and Peru. Int J Antimicrob Agents. 2005;25(4):308–12. doi: 10.1016/j.ijantimicag.2004.12.004 15784310.
60. Glenn LM, Lindsey RL, Folster JP, Pecic G, Boerlin P, Gilmour MW, et al. Antimicrobial resistance genes in multidrug-resistant Salmonella enterica isolated from animals, retail meats, and humans in the United States and Canada. Microb Drug Resist. 2013;19(3):175–84. doi: 10.1089/mdr.2012.0177 23350745; PubMed Central PMCID: PMC4665089.
61. Komp Lindgren P, Marcusson LL, Sandvang D, Frimodt-Moller N, Hughes D. Biological cost of single and multiple norfloxacin resistance mutations in Escherichia coli implicated in urinary tract infections. Antimicrob Agents Chemother. 2005;49(6):2343–51. doi: 10.1128/AAC.49.6.2343-2351.2005 15917531; PubMed Central PMCID: PMC1140522.
62. Morgan-Linnell SK, Zechiedrich L. Contributions of the combined effects of topoisomerase mutations toward fluoroquinolone resistance in Escherichia coli. Antimicrob Agents Chemother. 2007;51(11):4205–8. doi: 10.1128/AAC.00647-07 17682104; PubMed Central PMCID: PMC2151436.
63. Tamamura Y, Tanaka K, Akiba M, Kanno T, Hatama S, Ishihara R, et al. Complete nucleotide sequences of virulence-resistance plasmids carried by emerging multidrug-resistant Salmonella enterica Serovar Typhimurium isolated from cattle in Hokkaido, Japan. PLoS One. 2013;8(10):e77644. doi: 10.1371/journal.pone.0077644 24155970; PubMed Central PMCID: PMC3796477.
64. Sundin GW, Bender CL. Dissemination of the strA-strB streptomycin-resistance genes among commensal and pathogenic bacteria from humans, animals, and plants. Mol Ecol. 1996;5(1):133–43. doi: 10.1111/j.1365-294x.1996.tb00299.x 9147689.
65. Antunes P, Machado J, Sousa JC, Peixe L. Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrob Agents Chemother. 2005;49(2):836–9. doi: 10.1128/AAC.49.2.836-839.2005 15673783; PubMed Central PMCID: PMC547296.
66. Parsons Y, Hall RM, Stokes HW. A new trimethoprim resistance gene, dhfrX, in the In7 integron of plasmid pDGO100. Antimicrob Agents Chemother. 1991;35(11):2436–9. doi: 10.1128/aac.35.11.2436 1804022; PubMed Central PMCID: PMC245401.
67. Steiniger-White M, Rayment I, Reznikoff WS. Structure/function insights into Tn5 transposition. Curr Opin Struct Biol. 2004;14(1):50–7. doi: 10.1016/j.sbi.2004.01.008 15102449.
68. Wright GD, Thompson PR. Aminoglycoside phosphotransferases: proteins, structure, and mechanism. Front Biosci. 1999;4:D9–21. doi: 10.2741/wright 9872733.
69. Krauland MG, Marsh JW, Paterson DL, Harrison LH. Integron-mediated multidrug resistance in a global collection of nontyphoidal Salmonella enterica isolates. Emerg Infect Dis. 2009;15(3):388–96. doi: 10.3201/eid1503.081131 19239750; PubMed Central PMCID: PMC2666292.
70. Boyd D, Cloeckaert A, Chaslus-Dancla E, Mulvey MR. Characterization of variant Salmonella genomic island 1 multidrug resistance regions from serovars Typhimurium DT104 and Agona. Antimicrob Agents Chemother. 2002;46(6):1714–22. doi: 10.1128/AAC.46.6.1714-1722.2002 12019080; PubMed Central PMCID: PMC127246.
71. Doublet B, Lailler R, Meunier D, Brisabois A, Boyd D, Mulvey MR, et al. Variant Salmonella genomic island 1 antibiotic resistance gene cluster in Salmonella enterica serovar Albany. Emerg Infect Dis. 2003;9(5):585–91. doi: 10.3201/eid0905.020609 12737743; PubMed Central PMCID: PMC2972765.
72. Doublet B, Weill FX, Fabre L, Chaslus-Dancla E, Cloeckaert A. Variant Salmonella genomic island 1 antibiotic resistance gene cluster containing a novel 3'-N-aminoglycoside acetyltransferase gene cassette, aac(3)-Id, in Salmonella enterica serovar newport. Antimicrob Agents Chemother. 2004;48(10):3806–12. doi: 10.1128/AAC.48.10.3806-3812.2004 15388438; PubMed Central PMCID: PMC521890.
73. Ebner P, Garner K, Mathew A. Class 1 integrons in various Salmonella enterica serovars isolated from animals and identification of genomic island SGI1 in Salmonella enterica var. Meleagridis. J Antimicrob Chemother. 2004;53(6):1004–9. doi: 10.1093/jac/dkh192 15117931.
74. Meunier D, Boyd D, Mulvey MR, Baucheron S, Mammina C, Nastasi A, et al. Salmonella enterica serotype Typhimurium DT 104 antibiotic resistance genomic island I in serotype paratyphi B. Emerg Infect Dis. 2002;8(4):430–3. doi: 10.3201/eid0804.010375 11971780; PubMed Central PMCID: PMC2730239.
75. Doublet B, Boyd D, Mulvey MR, Cloeckaert A. The Salmonella genomic island 1 is an integrative mobilizable element. Mol Microbiol. 2005;55(6):1911–24. doi: 10.1111/j.1365-2958.2005.04520.x 15752209.
76. Jacobsen A, Hendriksen RS, Aaresturp FM, Ussery DW, Friis C. The Salmonella enterica pan-genome. Microb Ecol. 2011;62(3):487–504. doi: 10.1007/s00248-011-9880-1 21643699; PubMed Central PMCID: PMC3175032.
77. Fu S, Hiley L, Octavia S, Tanaka MM, Sintchenko V, Lan R. Comparative genomics of Australian and international isolates of Salmonella Typhimurium: correlation of core genome evolution with CRISPR and prophage profiles. Sci Rep. 2017;7(1):9733. doi: 10.1038/s41598-017-06079-1 28851865; PubMed Central PMCID: PMC5575072.
78. Dilucca M, Cimini G, Giansanti A. Essentiality, conservation, evolutionary pressure and codon bias in bacterial genomes. Gene. 2018;663:178–88. doi: 10.1016/j.gene.2018.04.017 29678658.
79. Yu H, Wang J, Ye J, Tang P, Chu C, Hu S, et al. Complete nucleotide sequence of pSCV50, the virulence plasmid of Salmonella enterica serovar Choleraesuis SC-B67. Plasmid. 2006;55(2):145–51. doi: 10.1016/j.plasmid.2005.09.001 16257053.
80. Kingsley RA, Humphries AD, Weening EH, De Zoete MR, Winter S, Papaconstantinopoulou A, et al. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun. 2003;71(2):629–40. doi: 10.1128/IAI.71.2.629-640.2003 12540539; PubMed Central PMCID: PMC145368.
81. Alsop J. An outbreak of salmonellosis in a swine finishing barn. J Swine Health Prod. 2005;13:4.
82. Pilar AV, Reid-Yu SA, Cooper CA, Mulder DT, Coombes BK. GogB is an anti-inflammatory effector that limits tissue damage during Salmonella infection through interaction with human FBXO22 and Skp1. PLoS Pathog. 2012;8(6):e1002773. doi: 10.1371/journal.ppat.1002773 22761574; PubMed Central PMCID: PMC3386239.
83. Holt KE, Thomson NR, Wain J, Langridge GC, Hasan R, Bhutta ZA, et al. Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. BMC Genomics. 2009;10:36. doi: 10.1186/1471-2164-10-36 19159446; PubMed Central PMCID: PMC2658671.
84. Ledeboer NA, Frye JG, McClelland M, Jones BD. Salmonella enterica serovar Typhimurium requires the Lpf, Pef, and Tafi fimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect Immun. 2006;74(6):3156–69. doi: 10.1128/IAI.01428-05 16714543; PubMed Central PMCID: PMC1479237.
85. Bender JK, Wille T, Blank K, Lange A, Gerlach RG. LPS structure and PhoQ activity are important for Salmonella Typhimurium virulence in the Galleria mellonella infection model [corrected]. PLoS One. 2013;8(8):e73287. doi: 10.1371/journal.pone.0073287 23951347; PubMed Central PMCID: PMC3738532.
86. Murata T, Tseng W, Guina T, Miller SI, Nikaido H. PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar typhimurium. J Bacteriol. 2007;189(20):7213–22. doi: 10.1128/JB.00973-07 17693506; PubMed Central PMCID: PMC2168427.
87. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics. 2009;10:104. doi: 10.1186/1471-2164-10-104 19284603; PubMed Central PMCID: PMC2660368.
88. Pukatzki S, McAuley SB, Miyata ST. The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol. 2009;12(1):11–7. doi: 10.1016/j.mib.2008.11.010 19162533.
89. Blondel CJ, Jimenez JC, Contreras I, Santiviago CA. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics. 2009;10:354. doi: 10.1186/1471-2164-10-354 19653904; PubMed Central PMCID: PMC2907695.
90. Zeng L, Zhang L, Wang P, Meng G. Structural basis of host recognition and biofilm formation by Salmonella Saf pili. Elife. 2017;6. doi: 10.7554/eLife.28619 29125121; PubMed Central PMCID: PMC5700814.
91. Li YF, Poole S, Rasulova F, McVeigh AL, Savarino SJ, Xia D. A receptor-binding site as revealed by the crystal structure of CfaE, the colonization factor antigen I fimbrial adhesin of enterotoxigenic Escherichia coli. J Biol Chem. 2007;282(33):23970–80. doi: 10.1074/jbc.M700921200 17569668.
92. Lang AS, Zhaxybayeva O, Beatty JT. Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol. 2012;10(7):472–82. doi: 10.1038/nrmicro2802 22683880; PubMed Central PMCID: PMC3626599.
93. Penades JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP. Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol. 2015;23:171–8. doi: 10.1016/j.mib.2014.11.019 25528295.
94. Ehrbar K, Hardt WD. Bacteriophage-encoded type III effectors in Salmonella enterica subspecies 1 serovar Typhimurium. Infect Genet Evol. 2005;5(1):1–9. doi: 10.1016/j.meegid.2004.07.004 15567133.
95. Schmieger H, Schicklmaier P. Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiol Lett. 1999;170(1):251–6. doi: 10.1111/j.1574-6968.1999.tb13381.x 9919675.
96. Figueroa-Bossi N, Bossi L. Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol. 1999;33(1):167–76. doi: 10.1046/j.1365-2958.1999.01461.x 10411733.
97. Stanley TL, Ellermeier CD, Slauch JM. Tissue-specific gene expression identifies a gene in the lysogenic phage Gifsy-1 that affects Salmonella enterica serovar typhimurium survival in Peyer's patches. J Bacteriol. 2000;182(16):4406–13. doi: 10.1128/jb.182.16.4406-4413.2000 10913072; PubMed Central PMCID: PMC94610.
98. Villafane R, Zayas M, Gilcrease EB, Kropinski AM, Casjens SR. Genomic analysis of bacteriophage epsilon 34 of Salmonella enterica serovar Anatum (15+). BMC Microbiol. 2008;8:227. doi: 10.1186/1471-2180-8-227 19091116; PubMed Central PMCID: PMC2629481.
99. Beloglazova N, Petit P, Flick R, Brown G, Savchenko A, Yakunin AF. Structure and activity of the Cas3 HD nuclease MJ0384, an effector enzyme of the CRISPR interference. EMBO J. 2011;30(22):4616–27. doi: 10.1038/emboj.2011.377 22009198; PubMed Central PMCID: PMC3243599.
100. Touchon M, Rocha EP. The small, slow and specialized CRISPR and anti-CRISPR of Escherichia and Salmonella. PLoS One. 2010;5(6):e11126. doi: 10.1371/journal.pone.0011126 20559554; PubMed Central PMCID: PMC2886076.
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