Genotypic and phenotypic characterization of multidrug resistant Salmonella Typhimurium and Salmonella Kentucky strains recovered from chicken carcasses

PLoS ONE

Volumn 12, Issue 5, 2017, Pages

  Tasmin, Rizwana ^a   Hasan, Nur A ^a,b   Grim, Christopher J ^c   Grant, Ar'Quette ^a   Choi, Seon Young ^b   Alam, M Samiul ^c   Bell, Rebecca ^c   Cavanaugh, Christopher ^c   Balan, Kannan V ^c   Babu, Uma S ^c   Parveen, Salina ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b Research and Development Department   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ACETOACETIC ACID; ALPHA LACTOSE; AMOXICILLIN; AMPICILLIN; CARBON; CEFOXITIN; CEFTIOFUR; FORMIC ACID; INOSITOL; MEMBRANE PROTEIN; PROPYLENE GLYCOL; RIBITOL; SIDEROPHORE; SULFAFURAZOLE; TAGATOSE; TARTARIC ACID; TETRACYCLINE; THREONINE;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIOPHAGE; CARBON UTILIZATION; CARCASS; CELL ASSAY; CELL KILLING; CHICKEN; CLADISTICS; FIMBRIA; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC DIFFERENCE; GENOTYPE PHENOTYPE CORRELATION; GRANULOSA CELL; HOST RESISTANCE; MACROPHAGE; MICROARRAY ANALYSIS; MONOPHYLY; MULTIDRUG RESISTANCE; NONHUMAN; OPERON; PHYLOGENY; SALMONELLA ENTERICA SEROVAR KENTUCKY; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SEROTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; ANIMAL; DRUG EFFECTS; GENETICS; GENOTYPE; MICROBIOLOGY; PHENOTYPE; SALMONELLA;

ANIMALS; CHICKENS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENOTYPE; PHENOTYPE; PHYLOGENY; SALMONELLA;

EID: 85019026743     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0176938     Document Type: Article

References (53)

1. Majowicz SE, Musto J, Scalla E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clinic Infect Dis. 2010; 50: 882-889.
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: 7-15. https://doi.org/10.3201/eid1701.P11101 PMID: 21192848
3. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, et al. Food-related illness and death in the United States. Emerg Infect Dis. 1999; 5: 607-625. https://doi.org/10.3201/eid0505.990502 PMID: 10511517
4. Hoffmann S, Maculloch B, Batz M. Economic burden of major foodborne illnesses acquired in the United States. USDA Economic Research Service. 2015. Economic Information Bulletin Number 140:53.
5. Haley BJ, Kim SW, Liljebjelke K, Guard J, Van Kessel JAS. Genome sequences of two Salmonella enterica serovar Kentucky isolates recovered from poultry carcasses in the United States. Genome Announc. 2016; 4(6):e01289-16. https://doi.org/10.1128/genomeA.01289-16 PMID: 27856587
6. Parveen S, Taabodi M, Schwarz JG, Oscar TP, Harter-Dennis J, White DG. Prevalence and antimicrobial resistance of Salmonella recovered from processed poultry. J Food Prot. 2007; 70: 2466-2472. PMID: 18044422
7. CDC. Salmonella surveillance: annual summary, 2006. U.S. Department of Health and Human Services, CDC, Atlanta, GA. 2008.
8. USDA. Serotype profiles of Salmonella strains from meat and poultry products January 1998 through December 2011. 2013. Available: http://www.fsis.usda.gov/wps/portal/fsis/topics/data-collection-andreports/microbiolog-y/annual-serotyping-reports. Accessed 1 December 2014.
9. Le Hello S, Bekhit A, Granier S, Barua H, Beutlich J, Zając M, et al. The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front Microbiol 2013; 4: 395. https://doi.org/10.3389/fmicb.2013.00395 PMID: 24385975
10. Le Hello S, Hendriksen RS, Doublet B, Fisher I, Nielsen EM, Whichard JM, et al. International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. J Infec Dis. 2011; 204: 675-684.
11. Voetsch AC, Van Gilder TJ, Angulo FJ, Farley MM, Shallow S, Marcus R, et al. Food net estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis. 2004; 38: 127-134.
12. USDA. Use of chlorine to treat poultry chiller water. Food Safety and Inspection Service, FSIS Notice 45-03. 2003.
13. Russell SM. Controlling Salmonella in Poultry Production and Processing. CRC Press, Boca Raton; 2012.
14. Sneeringer S. Restrictions on antibiotic use for production purposes in U.S. livestock industries likely to have small effects on prices and quantities. United States Department of Agriculture, Economic Research Service. 2015; Available: http://www.ers.usda.gov/amber-waves.aspx. Accessed 24 May 2016.
15. Oscar TP, Rutto GK, Ludwig JB, Parveen S. Qualitative map of Salmonella contamination on young chicken carcasses. J Food Prot. 2010; 73: 1596-1603. PMID: 20828464
16. Mohamed T, Zhao S, White DG, Parveen S. Molecular characterization of antibiotic resistant Salmonella Typhimurium and Salmonella Kentucky isolated from pre- and post-chill whole broilers carcasses. Food Microbiol. 2014; 38: 6-15. https://doi.org/10.1016/j.fm.2013.08.002 PMID: 24290620
17. Zhao S, McDermott PF, Friedman S, Qaiyumi S, Abbott J, Kiessling C, et al. Characterization of antimicrobial-resistant Salmonella isolated from imported foods. J Food Prot. 2006; 69: 500-507. PMID: 16541678
18. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008; 8;9: 75.
19. Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4: 406-425. PMID: 3447015
20. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial dna in humans and chimpanzees. Mol Biol Evol. 1993; 10: 512-526. PMID: 8336541
21. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33:1870-1874. https://doi.org/10.1093/molbev/msw054 PMID: 27004904
22. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 2014; 15(11): 524. https://doi.org/10.1186/s13059-014-0524-x PMID: 25410596
23. Karlin S, Altschul SF. Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc Natl Acad Sci. 1990; 87: 2264-2268. PMID: 2315319
24. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014; 42: D206-D214. https://doi.org/10.1093/nar/gkt1226 PMID: 24293654
25. 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. https://doi.org/10.1128/AAC.02412-14 PMID: 24777092
26. Beug H, von Kirchbach A, Doderlain G, Conscience JF, Graf T. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell. 1979; 18: 375-390. PMID: 227607
27. Bowe F, Heffron F. Isolation of Salmonella mutants defective for intracellular survival. Methods Enzymol. 1994; 236: 509-26. PMID: 7968635
28. Alam MS, Zaki MH, Yoshitake J, Akuta T, Ezaki T, Akaike T. Involvement of Salmonella enterica serovar Typhi RpoS in resistance to NO-mediated host defense against serovar Typhi infection. Microb Pathog. 2006; 40: 116-125. https://doi.org/10.1016/j.micpath.2005.11.007 PMID: 16448800
29. Thiagarajan D, Saeed M, Turek J, Asem E. In vitro attachment and invasion of chicken ovarian granulosa cells by Salmonella enteritidis phage type 8. Infect Immun. 1996; 64(12): 5015-21. PMID: 8945540
30. Gilbert AB, Evans AJ, Perry MM, Davidson MH. A method for separating the granulosa cells, the basal lamina and the theca of the preovulatory ovarian follicle of the domestic fowl (Gallus domesticus). J Reprod Fertil. 1977; 50: 179-181. PMID: 864645
31. Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschape H, Adams LG, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun. 2002; 70: 2249-2255. https://doi.org/10.1128/IAI.70.5.2249-2255.2002 PMID: 11953356
32. Fricke WF, McDermott PF, Mammel MK, Zhao S, Johnson TJ, Rasko DA, 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: 5963-5971. https://doi.org/10.1128/AEM.00786-09 PMID: 19648374
33. Hoffmann M, Muruvanda T, Allard MW, Korlach J, Roberts RJ, Timme R, et al. Complete genome sequence of a multidrug-resistant Salmonella enterica serovar Typhimurium var. 5-strain isolated from chicken breast. Genome Announc. 2013; 1(6): e01068-13. https://doi.org/10.1128/genomeA.01068-13 PMID: 24356834
34. Ramos-Morales F. Impact of Salmonella enterica type III secretion system effectors on the eukaryotic host cell. ISRN Cell Biol. 2012;78934.
35. Sly LM, Guiney DG, Reiner NE. Salmonella enterica serovar Typhimurium periplasmic superoxide dismutases SodCI and SodCII are required for protection against the phagocyte oxidative burst. Infect Immun. 2002; 70: 5312-5315. https://doi.org/10.1128/IAI.70.9.5312-5315.2002 PMID: 12183590
36. 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: 3556-3568. https://doi.org/10.1128/JB.00297-11 PMID: 21602358
37. Montero I, Herrero-Fresno A, Rodicio R, Rodicio MR. Efficient mobilization of a resistance derivative of pSLT, the virulence plasmid specific of Salmonella enterica serovar Typhimurium, by an IncI1 plasmid. Plasmid. 2013; 70: 104-109. https://doi.org/10.1016/j.plasmid.2013.03.002 PMID: 23541844
38. KPC. Antimicrob Agents Chemother. 2016; 60: 3767-3778. https://doi.org/10.1128/AAC.00464-16 PMID: 27067320
39. Rotger R, Casadesús J. The virulence plasmids of Salmonella. Internatl Microbiol. 1999; 2: 177-184.
40. Chu C, Chiu C-H. Evolution of the virulence plasmids of non-typhoid Salmonella and its association with antimicrobial resistance. Microb Infect. 2006; 8: 1931-1936.
41. Rychlik I, Gregorova D, Hradecka H. Distribution and function of plasmids in Salmonella enterica. Vet Microbiol. 2006; 112: 1-12. https://doi.org/10.1016/j.vetmic.2005.10.030 PMID: 16303262
42. Obradors N, Badia J, Baldoma L, Aguilar J. Anaerobic metabolism of the L-rhamnose fermentation product 1,2-propanediol in Salmonella typhimurium. J Bacteriol. 1988; 170: 2159-2162. PMID: 3283105
43. Cheng S, Sinha S, Fan C, Liu Y, Bobik TA. Genetic analysis of thhe protein shell of the microcompartments involved in coenzyme B12-dependent 1,2-propanediol degradation by Salmonella. J Bacteriol. 2011; 193(6): 1385-1392. https://doi.org/10.1128/JB.01473-10 PMID: 21239588
44. Bobik TA, Havemann GD, Busch RJ, Williams DS, Aldrich HC. The propanediol utilization (pdu) operon of Salmonella enterica serovar Typhimurium LT2 includes genes necessary for formation of polyhedral organelles involved in coenzyme B12-dependent 1,2-propanediol degradation. J Bacteriol. 1999; 181 (19): 5967-5975. PMID: 10498708
45. Conner CP, Heithoff DM, Julio SM, Sinsheimer RL, Mahan MJ. Differential patterns of acquired virulence genes distinguish Salmonella strains. Proc Natl Acad Sci USA. 1998; 95: 4641-4645. PMID: 9539791
46. Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci USA. 2011; 108(42): 17480-17485. https://doi.org/10.1073/pnas.1107857108 PMID: 21969563
47. Winter SE, Baumler AJ. A breathtaking feat: to compete with the gut microbiota, Salmonella drives its host to provide a respiratory electron acceptor. Gut Microbes. 2011; 2: 58-60. https://doi.org/10.4161/gmic.2.1.14911 PMID: 21637020
48. Lindgren SW, Stojiljkovic I, Heffron F. Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc Natl Acad Sci USA. 1996; 93: 4197-4201. PMID: 8633040
49. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L. Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA. 2001; 98: 15264-15269. https://doi.org/10.1073/pnas.261348198 PMID: 11742086
50. Patel JC, Galan JE. Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr Opin Microbiol. 2005; 8: 10-15. https://doi.org/10.1016/j.mib.2004.09.001 PMID: 15694851
51. McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V. Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol. 2009; 12: 117-124. https://doi.org/10.1016/j.mib.2008. 12.001 PMID: 19157959
52. Zhou D, Chen L, Hernandez L, Shears SB, Galan JE. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol. 2001; 39(2): 248-259. PMID: 11136447
53. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L. Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA. 2001; 98: 15264-15269. https://doi.org/10.1073/pnas.261348198 PMID: 11742086