Genomic and evolutionary analysis of two salmonella enterica serovar Kentucky sequence types isolated from bovine and poultry sources in North America

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Haley, Bradd J ^a   Kim, Seon Woo ^a   Pettengill, James ^b   Luo, Yan ^b   Karns, Jeffrey S ^a   Van Kessel, Jo Ann S ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL HUSBANDRY; ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BIOLOGICAL MONITORING; BOVINE; CONTROLLED STUDY; DAIRY CATTLE; EUROPE; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIATION; GENOMICS; KENTUCKY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; POULTRY; POULTRY PRODUCT; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR KENTUCKY; SINGLE NUCLEOTIDE POLYMORPHISM; SOUTHEAST ASIA; ANIMAL; ANIMAL SALMONELLOSIS; ANTIBIOTIC RESISTANCE; BIRD DISEASE; CATTLE DISEASE; CHICKEN; EVOLUTION; GENETICS; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; NORTH AMERICA; PLASMID;

ANIMALS; BIOLOGICAL EVOLUTION; CATTLE; CATTLE DISEASES; CHICKENS; DRUG RESISTANCE, BACTERIAL; GENOME, BACTERIAL; MICROBIAL SENSITIVITY TESTS; NORTH AMERICA; PHYLOGENY; PLASMIDS; POLYMORPHISM, SINGLE NUCLEOTIDE; POULTRY DISEASES; SALMONELLA ENTERICA; SALMONELLA INFECTIONS, ANIMAL;

EID: 84991203715     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0161225     Document Type: Article

References (69)

1. Centers for Disease Control and Prevention (2011) Salmonella annual summary tables 2009. Atlanta, GA: US Department of Health and Human Services.
2. Foley SL, Nayak R, Hanning IB, Johnson TJ, Han J, Ricke SC (2011) Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Appl Env. Micro 77: 4273-4279 doi: 10. 1128/AEM. 00598-11 PMID: 21571882
3. Van Kessel JS, Karns JS, Wolfgang DR, Hovingh E, Schukken YH (2012) Dynamics of Salmonella serotype shifts in an endemically infected dairy herd. Foodborne Pathog Dis. 9: 319-324. doi: 10. 1089/fpd. 2011. 1054 PMID: 22300223
4. Parveen S, Taabodi M, Schwarz JG, Oscar TP, Harter-Dennis J, White DG. (2007) Prevalence and antimicrobial resistance of Salmonella recovered from processed poultry. J Food Prot. 70(11):2466-72. PMID: 18044422
5. Van Kessel JS, Karns JS, Wolfgang DR, Hovingh E. (2013) Regional distribution of two dairy-associated Salmonella enterica serotypes. Foodborne Pathog Dis. 10(5):448-52 doi: 10. 1089/fpd. 2012. 1380 PMID: 23536986
6. University of Warwick MLST Database http://mlst. warwick. ac. uk/mlst/
7. Le Hello S, Hendriksen RS, Doublet B, Fisher I, Nielsen EM, Whichard JM, et al. (2011) International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J Infec Dis. 204: 675-684. doi: 10. 1093/infdis/jir409 PMID: 21813512
8. Le Hello S, Bekhit A, Granier S, Barua H, Beutlich J, Zaj?c M, et al. (2013) The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Frontiers in Microbiology 4 (2013). doi: 10. 3389/fmicb. 2013. 00395 PMID: 24385975
9. Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D, Guibert V, Et al. (2013). Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis. 13 (8):672-9. doi: 10. 1016/S1473-3099(13)70124-5 PMID: 23721756
10. Li X, Payne JB, Santos FB, Levine JF, Anderson KE, Sheldon BW. (2007) Salmonella populations and prevalence in layer feces from commercial high-rise houses and characterization of the Salmonella isolates by serotyping, antibiotic resistance analysis, and pulsed field gel electrophoresis. Poult Sci. 86(3):591-7. doi: 10. 1093/ps/86. 3. 591 PMID: 17297173
11. Santos FB, Dsouza DH, Jaykus L, Ferket PR, Sheldon BW. (2007) Genotypes, serotypes, and antibiotic resistance profiles of Salmonella isolated from commercial North Carolina turkey farms. J Food Prot. 70(6):1328-33. PMID: 17612059
12. Fricke WF, McDermott PF, Mammel MK, Zhao S, Johnson TJ, Rasko DA, et al. (2009) 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. 75 (18):5963-71. doi: 10. 1128/AEM. 00786-09 PMID: 19648374
13. Ladely SR, Meinersmann RJ, Ball TA, Fedorka-Cray PJ. (2016) Antimicrobial Susceptibility and Plasmid Replicon Typing of Salmonella enterica Serovar Kentucky Isolates Recovered from Broilers. Foodborne Pathog Dis. 13(6):309-15. doi: 10. 1089/fpd. 2015. 2102 PMID: 27028167
14. Edrington TS, Hume ME, Looper ML, Schultz CL, Fitzgerald AC, Callaway TR, et al. (2004) Variation in the faecal shedding of Salmonella and E. coli O157: H7 in lactating dairy cattle and examination of Salmonella genotypes using pulsed-field gel electrophoresis. Letters Appl. Micro 38: 366-372. doi: 10. 1111/j. 1472-765X. 2004. 01495. x PMID: 15059205
15. Van Kessel JS, Karns JS, Lombard JE, Kopral C (2011) Prevalence of Salmonella enterica, Listeria monocytogenes, and Escherichia coli virulence factors in bulk tank milk and in-line filters from U. S. dairies. J. Food Prot. 74: 759-68. doi: 10. 4315/0362-028X. JFP-10-423 PMID: 21549046
16. Timme RE, Pettengill JB, Allard MW, Strain E, Barrangou R, et al. (2013) Phylogenetic diversity of the enteric pathogen Salmonella enterica subsp. enterica inferred from genome-wide reference-free SNP characters. Genome Biol Evol 5: 2109-2123. doi: 10. 1093/gbe/evt159 PMID: 24158624
17. Deng X, Desai PT, den Bakker HC, Mikoleit M, Tolar B, Trees E, et al. (2014). Genomic epidemiology of Salmonella enterica serotype Enteritidis based on population structure of prevalent lineages. Emerging Infectious Diseases. 20(9): 1481. doi: 10. 3201/eid2009. 131095 PMID: 25147968
18. Chun J., Grim CJ, Hasan NA, Lee JH, Choi SY, Haley B, Taviani E. et al. (2009) Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proceedings of the National Academy of Sciences 106(36): 15442-15447. doi: 10. 1073/pnas. 0907787106 PMID: 19720995
19. Haley BJ, Allard M, Brown E, Hovingh E, Karns JS, Van Kessel JS. (2015) Molecular detection of the index case of a subclinical Salmonella Kentucky epidemic on a dairy farm. Epidemiology and Infection, 143:682-686. doi: 10. 1017/S0950268814001289 PMID: 25703396
20. Herrera-Leon S, Ramiro R, Arroyo M, Diez R, Usera MA, Echeita MA (2007) Blind comparison of traditional serotyping with three multiplex PCRs for the identification of Salmonella serotypes. Res Microbiol. 158:122-127. doi: 10. 1016/j. resmic. 2006. 09. 009 PMID: 17258433
21. Karns JS, Haley BJ, Van Kessel JA. (2015) Improvements to a PCR-Based Serogrouping Scheme for Salmonella enterica from Dairy Farm Samples. J Food Prot. 78(6):1182-5. doi: 10. 4315/0362-028X. JFP-14-475 PMID: 26038910
22. Schmieder R, and Edwards R. (2011) Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE 6:e17288. doi: 10. 1371/journal. pone. 0017288 PMID: 21408061
23. Bolger AM, Lohse M, Usadel B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30(15):2114-20. doi: 10. 1093/bioinformatics/btu170 PMID: 24695404
24. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PAet al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. (2012) J Comput Biol. 19(5):455-77. doi: 10. 1089/cmb. 2012. 0021 PMID: 22506599
25. Albert MJ, Obaid K, Alfouzan W, Sheikh AR, Udo E, Izumiya H, Bulach DM, Seemann T. et al. (2014). Isolation of Salmonella enterica Serovar Kentucky Strain ST 198 and Its H2S-Negative Variant from a Patient: Implications for Diagnosis. Journal of Clinical Microbiology. 52(11): 4090-4093. doi: 10. 1128/ JCM. 01775-14 PMID: 25143568
26. https://github. com/lskatz/lyve-SET
27. Katz LS, Petkau A, Beaulaurier J, Tyler S, Antonova ES, Turnsek MA, Guo Y, Wang S, Paxinos EE, Orata F, Gladney LM, Stroika S, Folster JP, Rowe L, Freeman MM, Knox N, Frace M, Boncy J, Graham M, Hammer BK, Boucher Y, Bashir A, Hanage WP, Van Domselaar G, Tarr CLet al. (2013) Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti. MBio 4(4): e00398-13. doi: 10. 1128/mBio. 00398-13 PMID: 23820394
28. https://github. com/CFSAN-Biostatistics/snp-pipeline
29. https://peerj. com/articles/cs-20/
30. https://github. com/marbl/harvest
31. Treangen TJ, Ondov BD, Koren S, Phillippy AM. (2014). The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 15(524): 2. doi: 10. 1186/PREACCEPT-2573980311437212 PMID: 25410596
32. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DMet al. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 6(2):80-92. doi: 10. 4161/fly. 19695 PMID: 22728672
33. Tamura K., Stecher G., Peterson D., Filipski A., & Kumar S. (2013). MEGA6: molecular evolutionary genetics analysis version 6. 0. Molecular biology and evolution, 30(12), 2725-2729. doi: 10. 1093/ molbev/mst197 PMID: 24132122
34. Stamatakis A (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 30(9):1312-3. doi: 10. 1093/bioinformatics/btu033 PMID: 24451623
35. Cummings MP, Neel MC, Shaw KL. (2008) A genealogical approach to quantifying lineage divergence. Evolution. 62(9):2411-22. doi: 10. 1111/j. 1558-5646. 2008. 00442. x PMID: 18564377
36. http://molevol. lysine. umiacs. umd. edu/software/phylogenetics/gsi
37. https://cge. cbs. dtu. dk/services/MLST/
38. Pritchard JK, Stephens M, Donnelly P. (2000) Inference of population structure using multilocus genotype data. Genetics. 155(2):945-59. PMID: 10835412
39. Rosenberg (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes. 4, 137-138.
40. Carattoli A, Zankari E, Garcõa-Fernandez A, Voldby Larsen M, Lund O, Villa L, Aarestrup F, Hasman Het al. (2014) In in silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrobial agents and chemotherapy 5(7): 3895-3903.
41. Dhillon BK, Laird MR, Shay JA, Winsor GL, Lo R, Nizam F, Pereira SK, Waglechner N, McArthur AG, Langille MG, Brinkman FSet al. (2015) IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic Acids Res. 43(W1):W104-8. doi: 10. 1093/nar/gkv401 PMID: 25916842
42. Wells SJ, Fedorka-Cray PJ, Dargatz DA, Ferris K, Green A. (2001) Fecal shedding of Salmonella spp. by dairy cows on farm and at cull cow markets. J Food Prot. 64(1):3-11. PMID: 11198437
43. Blau DM, McCluskey BJ, Ladely SR, Dargatz DA, Fedorka-Cray PJ, Ferris KE, Headrick ML. et al. (2005) Salmonella in dairy operations in the United States: prevalence and antimicrobial drug susceptibility. J Food Prot. 68(4):696-702. PMID: 15830658
44. Le Hello S, Weill FX, Guibert V, Praud K, Cloeckaert A, Doublet B. (2012) Early strains of multidrugresistant Salmonella enterica serovar Kentucky sequence type 198 from Southeast Asia harbor Salmonella genomic island 1-J variants with a novel insertion sequence. Antimicrob Agents Chemother. 56(10):5096-102. doi: 10. 1128/AAC. 00732-12 PMID: 22802251
45. Baucheron S, Le Hello S, Doublet B, Giraud E, Weill FX, Cloeckaert A. (2013) ramR mutations affecting fluoroquinolone susceptibility in epidemic multidrug-resistant Salmonella enterica serovar Kentucky ST198. Front Microbiol. 4:213. doi: 10. 3389/fmicb. 2013. 00213 PMID: 23914184
46. Achtman M, Wain J, Weill FX, Nair S, Zhou Z, Sangal V, Krauland MG, Hale JL, Harbottle H, Uebeck A, Dougan J, Harrison LH, Brisse S, S. enterica MLST Study Groupet al. (2012). Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathogens. 8, e1002776. doi: 10. 1371/journal. ppat. 1002776 PMID: 22737074
47. Daniels MJ, Hutchings MR, Greig A. (2003) The risk of disease transmission to livestock posed by contamination of farm stored feed by wildlife excreta. Epidemiol Infect. 130(3):561-8. PMID: 12825742
48. Callaway TR, Edrington TS, Nisbet DJ. (2014). Isolation of Escherichia coli O157:H7 and Salmonella from migratory brown-headed cowbirds (Molothrus ater), common grackles (Quiscalus quiscula), and cattle egrets (Bubulcus ibis). Foodborne Pathogens and Disease. 11:791-794. doi: 10. 1089/fpd. 2014. 1800 PMID: 25078494
49. Carlson JC, Hyatt DR, Bentler K, Mangan AM, Russell M, Piaggio AJ, Linz GMet al. (2015) Molecular characterization of Salmonella enterica isolates associated with starling-livestock interactions. Vet Microbiol. 179(1-2):109-18. doi: 10. 1016/j. vetmic. 2015. 03. 015 PMID: 25866128
50. Chen YC, Chang MC, Chuang YC, Jeang CL. (2004). Characterization and virulence of hemolysin III from Vibrio vulnificus. Curr Microbiol. 49(3):175-9. doi: 10. 1007/s00284-004-4288-5 PMID: 15386100
51. Baida GE, Kuzmin NP. (1996) Mechanism of action of hemolysin III from Bacillus cereus. Biochim Biophys Acta. 1284(2):122-4. doi: 10. 1016/s0005-2736(96)00168-x PMID: 8962879
52. Johnson TJ, Thorsness JL, Anderson C, Lynne A, Foley S, Han J, Fricke WF, et al. (2010) Horizontal gene transfer of a ColV plasmid has resulted in a dominant avian clonal type of Salmonella enterica serovar Kentucky. PLoS One 5(12): e15524. doi: 10. 1371/journal. pone. 0015524 PMID: 21203520
53. Levings RS, Lightfoot D, Partridge SR, Hall RM, Djordjevic SP. (2005) The genomic island SGI1, containing the multiple antibiotic resistance region of Salmonella enterica serovar Typhimurium DT104 or variants of it, is widely distributed in other S. enterica serovars. J Bacteriol. 187(13):4401-9. doi: 10. 1128/JB. 187. 13. 4401-4409. 2005 PMID: 15968049
54. Boyd DA, Shi X, Hu QH, Ng LK, Doublet B, Cloeckaert A, Mulvey MRet al. (2008) Salmonella genomic island 1 (SGI1), variant SGI1-I, and new variant SGI1-O in Proteus mirabilis clinical and food isolates from China. Antimicrob Agents Chemother. 52(1):340-4. doi: 10. 1128/AAC. 00902-07 PMID: 18025121
55. Hamidian M, Holt KE, Hall RM. (2015) The complete sequence of Salmonella genomic island SGI1-K. J Antimicrob Chemother. 70(1):305-6. doi: 10. 1093/jac/dku331 PMID: 25193084
56. Morgan E, Campbell JD, Rowe SC, Bispham J, Stevens MP, Bowen AJ, Barrow PA, Maskell DJ, Wallis TSet al. (2004) Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol. 54(4):994-1010. doi: 10. 1111/j. 1365-2958. 2004. 04323. x PMID: 15522082
57. Latasa C, Roux A, Toledo-Arana A, Ghigo JM, Gamazo C, Penades JR, Lasa Iet al. (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol. 58(5):1322-39. doi: 10. 1111/j. 1365-2958. 2005. 04907. x PMID: 16313619
58. Gal-Mor O, Gibson DL, Baluta D, Vallance BA, Finlay BB. (2008) A novel secretion pathway of Salmonella enterica acts as an antivirulence modulator during salmonellosis. PLoS Pathog. 4(4):e1000036. doi: 10. 1371/journal. ppat. 1000036 PMID: 18389060
59. Kingsley RA, van Amsterdam K, Kramer N, Bàumler AJ. (2000) The shdA gene is restricted to serotypes of Salmonella enterica subspecies I and contributes to efficient and prolonged fecal shedding. Infect Immun. 68(5):2720-7. doi: 10. 1128/iai. 68. 5. 2720-2727. 2000 PMID: 10768965
60. Kingsley RA, Santos RL, Keestra AM, Adams LG, Bàumler AJ. (2002) Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol. 43(4):895-905. doi: 10. 1046/j. 1365-2958. 2002. 02805. x PMID: 11929540
61. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, Banks G, Vazquez-Torres A, Gleeson C, Fang FC, Holden DWet 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(1):163-74. doi: 10. 1046/j. 1365-2958. 1998. 01047. x PMID: 9786193
62. Zhang S, Santos RL, Tsolis RM, Stender S, Hardt WD, Bàumler AJ, Adams LGet al. (2002) The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun. 70(7):3843-55. doi: 10. 1128/iai. 70. 7. 3843-3855. 2002 PMID: 12065528
63. McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V (2009) Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 12: 117-124 doi: 10. 1016/j. mib. 2008. 12. 001 PMID: 19157959
64. Severi E, Hood DW, Thomas GH. (2007) Sialic acid utilization by bacterial pathogens. Microbiology. 153(Pt 9):2817-22. doi: 10. 1099/mic. 0. 2007/009480-0 PMID: 17768226
65. Almagro-Moreno S, and Boyd EF. (2009). Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infection and immunity, 77(9), 3807-3816. doi: 10. 1128/IAI. 00279-09 PMID: 19564383
66. Almagro-Moreno S, and Boyd EF. (2010). Bacterial catabolism of nonulosonic (sialic) acid and fitness in the gut. Gut Microbes, 1(1), 45-50. doi: 10. 4161/gmic. 1. 1. 10386 PMID: 21327116
67. Kròger C, and Fuchs TM. (2009). Characterization of the myo-inositol utilization island of Salmonella enterica serovar Typhimurium. Journal of bacteriologyBacteriology, 191(2), 545-554. doi: 10. 1128/ JB. 01253-08 PMID: 19011032
68. Chaudhuri RR, Morgan E, Peters SE, Pleasance SJ, Hudson DL, Davies HM, Wang J, et al. (2013) Comprehensive assignment of roles for Salmonella Typhimurium genes in intestinal colonization of food-producing animals. PLoS 9(4): e1003456. doi: 10. 1371/journal. pgen. 1003456 PMID: 23637626
69. Dobrindt U, Hochhut B, Hentschel U, Hacker J. (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol. 2(5):414-24. doi: 10. 1038/nrmicro884 PMID: 15100694