Genomic comparison of non-typhoidal Salmonella enterica Serovars Typhimurium, Enteritidis, Heidelberg, Hadar and Kentucky isolates from broiler chickens

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Dhanani, Akhilesh S ^a   Block, Glenn ^b   Dewar, Ken ^c   Forgetta, Vincenzo ^d   Topp, Edward ^e   Beiko, Robert G ^a   Diarra, Moussa S ^b,f  

^a DALHOUSIE UNIVERSITY   (Canada)

^b SUMMERLAND RESEARCH AND DEVELOPMENT CENTRE   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^f GUELPH RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BROILER; CLADISTICS; COMPARATIVE STUDY; CONTROLLED STUDY; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; INTEGRON; IRON METABOLISM; IRON TRANSPORT; MOLECULAR PHYLOGENY; NONHUMAN; PATHOGENICITY ISLAND; PLASMID; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SPECIES COMPARISON; TYPE III SECRETION SYSTEM; TYPE IV SECRETION SYSTEM; ANIMAL; ANIMAL SALMONELLOSIS; BACTERIAL SECRETION SYSTEM; BIRD DISEASE; CHEMISTRY; CHICKEN; CLASSIFICATION; DRUG EFFECTS; GENETICS; GENOMIC ISLAND; HIGH THROUGHPUT SEQUENCING; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; PATHOGENICITY; PHYLOGENY; SALMONELLA ENTERICA;

BACTERIA (MICROORGANISMS); GALLUS GALLUS; SALMONELLA; SALMONELLA ENTERICA;

ANTIINFECTIVE AGENT; BACTERIAL SECRETION SYSTEM;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL SECRETION SYSTEMS; CHICKENS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENOME, BACTERIAL; GENOMIC ISLANDS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICROBIAL SENSITIVITY TESTS; PHYLOGENY; PLASMIDS; POULTRY DISEASES; SALMONELLA ENTERICA; SALMONELLA INFECTIONS, ANIMAL;

EID: 84939150697     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128773     Document Type: Article

References (68)

1. Diarrassouba F, Diarra MS, Bach S, Delaquis P, Pritchard J, Topp E, et al. Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. J Food Prot. 2007; 70: 1316-27. PMID: 17612058
2. Corrier DE, Byrd JA, Hargis BM, Hume ME, Bailey RH, Stanker LH. Presence of Salmonella in the crop and ceca of broiler chickens before and after preslaughter feed withdrawal. Poult Sci. 1999; 78: 45-49. PMID: 10023745
3. Aslam M, Diarra MS, Masson L. Characterization of antimicrobial resistance and virulence genotypes of Enterococcus faecalis recovered from a pork processing plant. J Food Prot. 2012; 75: 1486-91. doi: 10.4315/0362-028X.JFP-11-524 PMID: 22856575
4. Olsen SJ, Bishop R, Brenner FW, Roels TH, Bean N, Tauxe R V, et al. The changing epidemiology of salmonella: trends in serotypes isolated from humans in the United States, 1987-1997. J Infect Dis. 2001; 183: 753-761. PMID: 11181152
5. Rabsch W, Tschäpe H, Bäumler AJ. Non-typhoidal salmonellosis: Emerging problems. Microbes Infect. 2001; 3: 237-247. PMID: 11358718
6. Altekruse SF, Cohen ML, Swerdlow DL. Emerging foodborne diseases. Emerg Infect Dis. 1997; 3: 285-93. PMID: 9284372
7. Alcaine SD, Warnick LD, Wiedmann M. Antimicrobial resistance in nontyphoidal Salmonella. J Food Prot. 2007; 70: 780-90. PMID: 17388077
8. Diarra MS, Delaquis P, Rempel H, Bach S, Harlton C, Aslam M, et al. Antibiotic resistance and diversity of Salmonella enterica serovars associated with broiler chickens. J Food Prot. 2014; 77: 40-9. doi: 10.4315/0362-028.JFP-13-251 PMID: 24405997
9. Zhang-Barber Z, Turner a. K, Barrow P A. Vaccination for control of Salmonella in poultry. Vaccine. 1999; 17: 2538-2545. doi: 10.1016/S0264-410X(99)00060-2 PMID: 10418900
10. World Health Organisation Salmonellosis control: the role of animal and product hygiene. Geneva; 1988. PMID: 3144809
11. C-EnterNet News. In: Public Health Agency of Canada [Internet]. 2012. Available: http://www.phac-aspc.gc.ca/foodnetcanada/news-actualites/volume10-12-eng.php.
12. Joerger RD, Sartori CA, Kniel KE. Comparison of genetic and physiological properties of Salmonella enterica isolates from chickens reveals one major difference between serovar Kentucky and other serovars: response to acid. Foodborne Pathog Dis. 2009; 6: 503-12. doi: 10.1089/fpd.2008.0144 PMID: 19415975
13. Forgetta V, Rempel H, Malouin F, Vaillancourt R, Topp E, Dewar K, et al. Pathogenic and multidrug-resistant Escherichia fergusonii from broiler chicken. Poult Sci. 2012; 91: 512-25. doi: 10.3382/ps.2011-01738 PMID: 22252367
14. Fricke WF, McDermott PF, Mammel MK, Zhao S, Johnson TJ, Rasko D A, et al. Antimicrobial resistance-conferring plasmids with similarity to virulence plasmids from avian pathogenic Escherichia coli strains in Salmonella enterica serovar Kentucky isolates from poultry. Appl Environ Microbiol. 2009; 75: 5963-71. doi: 10.1128/AEM.00786-09 PMID: 19648374
15. Butaye P, Devriese LA, Haesebrouck F. Antimicrobial growth promoters used in animal feed : effects of less well known antibiotics on Gram-positive bacteria. Clin Microbiol Rev. 2003; 16: 175-188. doi: 10.1128/CMR.16.2.175 PMID: 12692092
16. Silbergeld EK, Graham J, Price LB. Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health. 2008; 29: 151-69. doi: 10.1146/annurev.publhealth.29.020907.090904 PMID: 18348709
17. LeClerc JE, Li B, Payne WL, Cebula TA. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science (80-). 1996; 274: 1208-1211. PMID: 8895473
18. Le Gall S, Desbordes L, Gracieux P, Saffroy S, Bousarghin L, Bonnaure-Mallet M, et al. Distribution of mutation frequencies among Salmonella enterica isolates from animal and human sources and genetic characterization of a Salmonella Heidelberg hypermutator. Vet Microbiol. 2009; 137: 306-12. doi: 10.1016/j.vetmic.2009.01.023 PMID: 19201550
19. Herbelin CJ, Chirillo SC, Melnick KA, Whittam TS. Gene conservation and loss in the mutS-rpoS genomic region of pathogenic Escherichia coli. J Bacteriol. 2000; 182: 5381-90. PMID: 10986240
20. Malorny B, Junker E, Helmuth R. Multi-locus variable-number tandem repeat analysis for outbreak studies of Salmonella enterica serotype Enteritidis. BMC Microbiol. 2008; 8: 84. doi: 10.1186/1471-2180-8-84 PMID: 18513386
21. Swaminathan B, Barrett TJ, Hunter SB, Tauxe R V. PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis. 2001; 7: 382-9. doi: 10.3201/eid0703.010303 PMID: 11384513
22. Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S, Churcher C, et al. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 2008; 18: 1624-37. doi: 10.1101/gr.077404.108 PMID: 18583645
23. Smith SE, Showers-Corneli P, Dardenne CN, Harpending HH, Martin DP, Beiko RG. Comparative genomic and phylogenetic approaches to characterize the role of genetic recombination in mycobacterial evolution. PLoS One. 2012; 7: e50070. doi: 10.1371/journal.pone.0050070 PMID: 23189179
24. Joshi N, Fass J. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) [Software] [Internet]. 2011. Available: https://github.com/najoshi/sickle.
25. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010; 5: e11147. doi: 10.1371/journal.pone.0011147 PMID: 20593022
26. Zhang X, Kelly SM, Bollen WS, Curtiss R. Characterization and immunogenicity of Salmonella typhimurium SL1344 and UK-1 delta crp and delta cdt deletion mutants. Infect Immun. 1997; 65: 5381-7. PMID: 9393846
27. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards R A, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008; 9: 75. doi: 10.1186/1471-2164-9-75 PMID: 18261238
28. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26: 2460-1. doi: 10.1093/bioinformatics/btq461 PMID: 20709691
29. Ragan MA, Gaasterland T. Microbial genescapes: a prokaryotic view of the yeast genome. Microb Comp Genomics. 1998; 3: 219-35. PMID: 10027191
30. Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc Natl Acad Sci U S A. 1999; 96: 4285-4288. PMID: 10200254
31. Lopez P, Bapteste E. Molecular phylogeny: reconstructing the forest. Comptes Rendus - Biol. Elsevier Masson SAS; 2009; 332: 171-182. doi: 10.1016/j.crvi.2008.07.003 PMID: 24797922
32. Castresana J. Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. Mol Biol Evol. 2000; 17: 540-552. PMID: 10742046
33. Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One. 2010; 5: e9490. doi: 10.1371/journal.pone.0009490 PMID: 20224823
34. Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006; 22: 2688-2690. doi: 10.1093/bioinformatics/btl446 PMID: 16928733
35. R Development Core Team. R Foundation for Statistical Computing [Internet]. Vienna, Austria: R: A Language and Environment for Statistical Computing.; 2007. Available: http://www.r-project.org/.
36. 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: D325-D328. doi: 10.1093/nar/gki008 PMID: 15608208
37. Hunt S, Green J, Artymiuk PJ. Hemolysin E (HlyE, ClyA, SheA) and related toxins. Adv Exp Med Biol. 2010; 677: 116-126. doi: 10.1007/978-1-4419-6327-7-10 PMID: 20687485
38. Eswarappa SM, Panguluri KK, Hensel M, Chakravortty D. The yejABEF operon of Salmonella confers resistance to antimicrobial peptides and contributes to its virulence. Microbiology. 2008; 154: 666-78. doi: 10.1099/mic.0.2007/011114-0 PMID: 18227269
39. Severinov K, Nair SK. Microcin C: biosynthesis and mechanisms of bacterial resistance. Future Microbiol. 2012; 7: 281-289. doi: 10.2217/fmb.11.148.Microcin PMID: 22324995
40. Wang Y, Huang H, Sun M, Zhang Q, Guo D. T3DB: an integrated database for bacterial type III secretion system. BMC Bioinformatics. 2012; 13: 66. doi: 10.1186/1471-2105-13-66 PMID: 22545727
41. Bi D, Liu L, Tai C, Deng Z, Rajakumar K, Ou H. SecReT4 : a web-based bacterial type IV secretion system resource. Nucleic Acids Res. 2013; 41: 660-665. doi: 10.1093/nar/gks1248
42. Shakyawar SK, Goyal A, Dubey VK. Genome Analysis of Selected Foodborne Pathogens for Identification of Drug Targets. Curr Trends Biotechnol Pharm. 2011; 5: 1134-1148.
43. Zhou CE, Smith J, Lam M, Zemla A, Dyer MD, Slezak T. MvirDB - a microbial database of protein toxins, virulence factors and antibiotic resistance genes for bio-defence applications. Nucleic Acids Res. 2007; 35: D391-D394. doi: 10.1093/nar/gkl791 PMID: 17090593
44. Blázquez J. Hypermutation as a Factor Contributing to the Acquisition of Antimicrobial Resistance. Clin Infect Dis. 2003; 37: 1201-1209. PMID: 14557965
45. Altschul SF, Madden TL, Schäffer A A, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997; 25: 3389-3402. doi: 10.1093/nar/25.17.3389 PMID: 9254694
46. Beltran P, Musser JM, Helmuth R, Farmer JJ, Frerichs WM, Wachsmuth IK, et al. Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc Natl Acad Sci U S A. 1988; 85: 7753-7757. doi: 10.1073/pnas.85.20.7753 PMID: 3051004
47. Lee SH, Galán JE. InvB is a type III secretion-associated chaperone for the Salmonella enterica effector protein SopE. J Bacteriol. 2003; 185: 7279-84. PMID: 14645290
48. Ramos-morales F. Impact of Salmonella enterica Type III Secretion System Effectors on the Eukaryotic Host Cell. ISRN Cell Biol. 2012; 2012: 1-36. doi: 10.5402/2012/787934
49. Lamers MH, Perrakis A, Enzlin JH, Winterwerp HH, de Wind N, Sixma TK. The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature. 2000; 407: 711-7. doi: 10.1038/35037523 PMID: 11048711
50. 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: 852-856. doi: 10.1128/genomeA.00467-13 PMID: 11677609
51. Shippy DC, Eakley NM, Mikheil DM, Fadl AA. Role of StdA in adhesion of Salmonella enterica serovar Enteritidis phage type 8 to host intestinal epithelial cells. Gut Pathog. 2013; 5: 43. doi: 10.1186/1757-4749-5-43 PMID: 24367906
52. Kingsley RA, Santos RL, Keestra AM, Adams LG, Bäumler AJ. Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol. 2002; 43: 895-905. PMID: 11929540
53. Hueck CJ. Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants. Microbiol Mol Biol Rev. 1998; 62: 379-433. PMID: 9618447
54. Hansen-Wester I, Hensel M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 2001; 3: 549-59. PMID: 11418329
55. Raffatellu M, Wilson RP, Chessa D, Andrews-Polymenis H, Tran QT, Lawhon S, et al. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. Infect Immun. 2005; 73: 146-54. doi: 10.1128/IAI.73.1.146154.2005 PMID: 15618149
56. Zhang S, Santos RL, Tsolis RM, Stender S, Hardt W-D, Bäumler AJ, et al. The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun. 2002; 70: 3843-55. doi: 10.1128/IAI.70.7.3843 PMID: 12065528
57. Shea JE, Beuzon CR, Gleeson C, Mundy R, Holden DW. Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun. 1999; 67: 213-9. PMID: 9864218
58. Figueira R, Watson KG, Holden DW, Helaine S. Identification of salmonella pathogenicity island-2 type III secretion system effectors involved in intramacrophage replication of S. enterica serovar typhimurium: implications for rational vaccine design. MBio. 2013; 4: e00065. doi: 10.1128/mBio.00065-13 PMID: 23592259
59. Ratledge C, Dover LG. Iron metabolism in pathogenic bacteria. Annu Rev Microbiol. 2000; 54: 881-941. PMID: 11018148
60. Bjarnason J, Southward CM, Surette MG. Genomic profiling of iron-responsive genes in Salmonella enterica serovar typhimurium by high-throughput screening of a random promoter library. J Bacteriol. 2003; 185: 4973-82. doi: 10.1128/JB.185.16.4973 PMID: 12897017
61. De Lorenzo V, Martinez JL. Aerobactin production as a virulence factor: a reevaluation. Eur J Clin Microbiol Infect Dis. 1988; 7: 621-9. PMID: 2973985
62. Janakiraman A, Slauch JM. The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol Microbiol. 2000; 35: 1146-55. PMID: 10712695
63. Bonalli M, Stephan R, Käppeli U, Cernela N, Adank L, Hächler H. Salmonella enterica serotype Kentucky associated with human infections in Switzerland: Genotype and resistance trends 2004-2009. Food Res Int. Elsevier Ltd; 2012; 45: 953-957.
64. Stojiljkovic I, Srinivasan N. Neisseria meningitidis tonB, exbB, and exbD genes: Ton-dependent utilization of protein-bound iron in Neisseriae. J Bacteriol. 1997; 179: 805-812. PMID: 9006036
65. Kingsley RA, Reissbrodt R, Rabsch W, Ketley JM, Tsolis RM, Everest P, et al. Ferrioxamine-mediated Iron(III) utilization by Salmonella enterica. Appl Environ Microbiol. 1999; 65: 1610-8. PMID: 10103258
66. Mulvey MR, Boyd D A, Finley R, Fakharuddin K, Langner S, Allen V, et al. Ciprofloxacin-resistant Salmonella enterica serovar Kentucky in Canada. Emerg Infect Dis. 2013; 19: 999-1001. doi: 10.3201/eid1906.121351 PMID: 23735312
67. Hsieh P. Molecular mechanisms of DNA mismatch repair. Mutat Res. 2001; 486: 71-87. PMID: 11425513
68. Marinus MG, Poteete A, Arraj JA. Correlation of DNA adenine methylase activity with spontaneous mutability in Escherichia coli K-12. Gene. 1984; 28: 123-5. PMID: 6376282