Pathotyping of Salmonella enterica by analysis of single-nucleotide polymorphisms in cyaA and flanking 23S ribosomal sequences

Environmental Microbiology

Volumn 9, Issue 4, 2007, Pages 1047-1059

  Morales, Cesar A ^a   Musgrove, Michael ^a   Humphrey, T J ^b   Cates, Carolyn ^a   Gast, Richard ^a   Guard Bouldin, J ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; BACTERIAL PROTEIN;

ANIMAL; ARTICLE; BIOFILM; CHICKEN; CLASSIFICATION; EGG; FOOD POISONING; GENETIC DRIFT; GENETICS; HUMAN; METHODOLOGY; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHENOTYPE; POINT MUTATION; RIBOTYPING; SALMONELLA ENTERICA; SEROTYPING; SINGLE NUCLEOTIDE POLYMORPHISM;

ADENYLATE CYCLASE; ANIMALS; BACTERIAL PROTEINS; BIOFILMS; CHICKENS; EGGS; EVOLUTION, MOLECULAR; GENETIC DRIFT; HUMANS; MOLECULAR SEQUENCE DATA; PHENOTYPE; POINT MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; RIBOTYPING; SALMONELLA ENTERICA; SALMONELLA FOOD POISONING; SEROTYPING;

SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS;

EID: 33947124163     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2006.01233.x     Document Type: Article

References (70)

1. Alami, N., and Hallenbeck, P.C. (1995) Cloning and characterization of a gene cluster, phsBCDEF, necessary for the production of hydrogen sulfide from thiosulfate by Salmonella typhimurium. Gene 156: 53-57.
2. Anonymous (2004) Salmonella serotype Typhimurium outbreak associated with commercially processed egg salad - Oregon, 2003. MMWR Morb Mortal Wkly Rep 53: 1132-1134.
3. Anonymous (2005) Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food - 10 sites, United States, 2004. MMWR Morb Mortal Wkly Rep 54: 352-356.
4. Aravind, L., and Koonin, E.V. (1999) DNA polymerase betalike nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res 27: 1609-1618.
5. Baker, D.A., and Kelly, J.M. (2004) Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol Microbiol 52: 1229-1242.
6. Barak, J.D., Gorski, L., Naraghi-Arani, P., and Charkowski, A.O. (2005) Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl Environ Microbiol 71: 5685-5691.
7. Brosious, J., Ullrich, A., and Raker, M.A. (1981) Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal operon of E. coli. Plasmid 6: 112-118.
8. Byrd, J.A., DeLoach, J.R., Corrier, D.E., Nisbet, D.J., and Stanker, L.H. (1999) Evaluation of Salmonella serotype distributions from commercial broiler hatcheries and grower houses. Avian Dis 43: 39-47.
9. Currie, A., MacDougall, L., Aramini, J., Gaulin, C., Ahmed, R., and Isaacs, S. (2005) Frozen chicken nuggets and strips and eggs are leading risk factors for Salmonella Heidelberg infections in Canada. Epidemiol Infect 133: 809-816.
10. Curtiss, R., III, and Hassan, J.O. (1996) Nonrecombinant and recombinant avirulent Salmonella vaccines for poultry. Vet Immunol Immunopathol 54: 365-372.
11. De Buck, J., Van Immerseel, F., Haesebrouck, F., and Ducatelle, R. (2004) Effect of type 1 fimbriae of Salmonella enterica serotype Enteritidis on bacteraemia and reproductive tract infection in laying hens. Avian Pathol 33: 314-320.
12. Elson, R., Little, C.L., and Mitchell, R.T. (2005) Salmonella and raw shell eggs: results of a cross-sectional study of contamination rates and egg safety practices in the United Kingdom catering sector in 2003. J Food Prot 68: 256-264.
13. Erdem, B., Threlfall, E.J., Schofield, S.L., Ward, L.R., and Rowe, B. (1994) Plasmid profile typing provides a method for the differentiation of strains of Salmonella enteritidis phage type 4 isolated in Turkey. Lett Appl Microbiol 19: 265-267.
14. Fakhr, M.K., Nolan, L.K., and Logue, C.M. (2005) Multilocus sequence typing lacks the discriminatory ability of pulsed-field gel electrophoresis for typing Salmonella enterica serovar Typhimurium. J Clin Microbiol 43: 2215-2219.
15. Falkow, S. (2004) Molecular Koch's postulates applied to bacterial pathogenicity - a personal recollection 15 years later. Nat Rev Microbiol 2: 67-72.
16. Finlay, B.B., and Brumell, J.H. (2000) Salmonella interactions with host cells: in vitro to in vivo. Philos Trans R Soc Lond B Biol Sci 355: 623-631.
17. Finlay, B.B., and Falkow, S. (1989) Common themes in microbial pathogenicity. Microbiol Rev 53: 210-230.
18. Fisher, I.S. (1999) Salmonella Enteritidis in Western Europe 1995-98 - a surveillance report from Enter-net. Euro Surveill 4: 56.
19. Galan, J.E. (2001) Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17: 53-86.
20. Galan, J.E., and Curtiss, R., III (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA 86: 6383-6387.
21. Guard-Bouldin, J., Gast, R.K., Humphrey, T.J., Henzler, D.J., Morales, C., and Coles, K. (2004) Subpopulation characteristics of egg-contaminating Salmonella enterica serovar Enteritidis as defined by the lipopolysaccharide O chain. Appl Environ Microbiol 70: 2756-2763.
22. Guard-Petter, J. (1998) Variants of smooth Salmonella enterica serovar Enteritidis that grow to higher cell density than the wild type are more virulent. App Environ Microbiol 64: 2166-2172.
23. Guard-Petter, J. (2001) The chicken, the egg and Salmonella Enteritidis. Environ Microbiol 3: 421-430.
24. Guard-Petter, J., Keller, L.H., Rahman, M.M., Carlson, R.W., and Silvers, S. (1996) A novel relationship between O-antigen variation, matrix formation, and invasiveness of Salmonella Enteritidis. Epidemiol Infect 117: 219-231.
25. Guard-Petter, J., Parker, C.T., Asokan, K., and Carlson, R.W. (1999) Clinical and veterinary isolates of Salmonella enterica serovar enteritidis defective in lipopolysaccharide O-chain polymerization. Appl Environ Microbiol 65: 2195-2201.
26. Healy, M., Huong, J., Bittner, T., Lising, M., Frye, S., Raza, S., et al. (2005) Microbial DNA typing by automated repetitive-sequence-based PCR. J Clin Microbiol 43: 199-207.
27. Hennessy, T.W., Cheng, L.H., Kassenborg, H., Ahuja, S.D., Mohle-Boetani, J., Marcus, R., et al. (2004) Egg consumption is the principal risk factor for sporadic Salmonella serotype Heidelberg infections: a case-control study in FoodNet sites. Clin Infect Dis 38 (Suppl. 3): S237-S243.
28. Horswill, A.R., and Escalante-Semerena, J.C. (2001) In vitro conversion of propionate to pyruvate by Salmonella enterica enzymes: 2-methylcitrate dehydratase (PrpD) and aconitase enzymes catalyze the conversion of 2-methylcitrate to 2-methylisocitrate. Biochemistry 40: 4703-4713.
29. Hudson, C.R., Garcia, M., Gast, R.K., and Maurer, J.J. (2001) Determination of close genetic relatedness of the major Salmonella enteritidis phage types by pulsed-field gel electrophoresis and DNA sequence analysis of several Salmonella virulence genes. Avian Dis 45: 875-886.
30. Humphrey, T.J., Williams, A., McAlpine, K., Lever, M.S., Guard-Petter, J., and Cox, J.M. (1996) Isolates of Salmonella enterica Enteritidis PT4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chickens. Epidemiol Infect 117: 79-88.
31. Isaacs, S., Aramini, J., Ciebin, B., Farrar, J.A., Ahmed, R., Middleton, D., et al. (2005) An international outbreak of salmonellosis associated with raw almonds contaminated with a rare phage type of Salmonella Enteritidis. J Food Prot 68: 191-198.
32. Jones, B.D. (2005) Salmonella invasion gene regulation: a story of environmental awareness. J Microbiol 43 Spec No.: 110-117.
33. Kennedy, M.J., Yancey, R.J., Jr, Sanchez, M.S., Rzepkowski, R.A., Kelly, S.M., and Curtiss, R., III (1999) Attenuation and immunogenicity of Deltacya Deltacrp derivatives of Salmonella choleraesuis in pigs. Infect Immun 67: 4628-4636.
34. Kimura, A.C., Reddy, V., Marcus, R., Cieslak, P.R., Mohle-Boetani, J.C., Kassenborg, H.D., et al. (2004) Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a case-control study in FoodNet sites. Clin Infect Dis 38 (Suppl. 3): S244-S252.
35. Levy, D.D., Sharma, B., and Cebula, T.A. (2004) Singlenucleotide polymorphism mutation spectra and resistance to quinolones in Salmonella enterica serovar Enteritidis with a mutator phenotype. Antimicrob Agents Chemother 48: 2355-2363.
36. Liebana, E. (2002) Molecular tools for epidemiological investigations of S. enterica subspecies enterica infections. Res Vet Sci 72: 169-175.
37. Liebana, E., Garcia-Migura, L., Breslin, M.F., Davies, R.H., and Woodward, M.J. (2001) Diversity of strains of Salmonella enterica serotype Enteritidis from English poultry farms assessed by multiple genetic fingerprinting. J Clin Microbiol 39: 154-161.
38. Liebana, E., Garcia-Migura, L., Guard-Petter, J., McDowell, S.W., Rankin, S., Opitz, H.M., et al. (2002) Salmonella enterica serotype Enteritidis phage types 4, 7, 6, 8, 13a, 29 and 34: a comparative analysis of genomic fingerprints from geographically distant isolates. J Appl Microbiol 92: 196-209.
39. Lindstedt, B.A., Vardund, T., Aas, L., and Kapperud, G. (2004) Multiple-locus variable-number tandem-repeats analysis of Salmonella enterica subsp. enterica serovar Typhimurium using PCR multiplexing and multicolor capillary electrophoresis. J Microbiol Methods 59: 163-172.
40. Lory, S., Wolfgang, M., Lee, V., and Smith, R. (2004) The multi-talented bacterial adenylate cyclases. Int J Med Microbiol 293: 479-482.
41. Lu, P.L., Hwang, I.J., Tung, Y.L., Hwang, S.J., Lin, C.L., and Siu, L.K. (2004) Molecular and epidemiologic analysis of a county-wide outbreak caused by Salmonella enterica subsp. enterica serovar Enteritidis traced to a bakery. BMC Infect Dis 4: 48.
42. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
43. McKeever, W.G., and Neidhardt, F.C. (1976) Growth rate modulation of four aminoacyl-transfer ribonucleic acid synthetases in enteric bacteria. J Bacteriol 126: 634-645.
44. Mattoo, S., Foreman-Wykert, A.K., Cotter, P.A., and Miller, J.F. (2001) Mechanisms of Bordetella pathogenesis. Front Biosci 6: E168-E186.
45. Mazurek, J., Holbert, L., Parrish, M.K., and Salehi, E. (2005) Raw eggs - lessons learned from an outbreak of Salmonella serotype Enteritidis infections associated with meringue pie. J Public Health Manag Pract 11: 201-207.
46. Merrell, D.S., and Falkow, S. (2004) Frontal and stealth attack strategies in microbial pathogenesis. Nature 430: 250-256.
47. Morales, C.A., Porwollik, S., Frye, J.G., Kinde, H., McClelland, M., and Guard-Bouldin, J. (2005) Correlation of phenotype with the genotype of egg-contaminating Salmonella enterica serovar Enteritidis. Appl Environ Microbiol 71: 4388-4399.
48. Mumma, G.A., Griffin, P.M., Meltzer, M.I., Braden, C.R., and Tauxe, R.V. (2004) Egg quality assurance programs and egg-associated Salmonella Enteritidis infections, United States. Emerg Infect Dis 10: 1782-1789.
49. Nayak, R., Kenney, P.B., Keswani, J., and Ritz, C. (2003) Isolation and characterization of Salmonella in a turkey production facility. Br Poult Sci 44: 192-202.
50. Parker, C.T., Liebana, E., Henzler, D.J., and Guard-Petter, J. (2001) Lipopolysaccharide O-chain microheterogeneity of Salmonella serotypes Enteritidis and Typhimurium. Environ Microbiol 3: 332-342.
51. Parker, C.T., Harmon, B., and Guard-Petter, J. (2002) Mitigation of avian reproductive tract function by Salmonella Enteritidis producing high-molecular-mass lipopolysaccharide. Environ Microbiol 4: 538-545.
52. Patel, J.C., and Galan, J.E. (2005) Manipulation of the host actin cytoskeleton by Salmonella - all in the name of entry. Curr Opin Microbiol 8: 10-15.
53. Porwollik, S., Santiviago, C.A., Cheng, P., Florea, L., and McClelland, M. (2005) Differences in gene content between Salmonella enterica serovar Enteritidis isolates and comparison to closely related serovars Gallinarum and Dublin. J Bacteriol 187: 6545-6555.
54. Redkar, R.J., Dube, M.P., McCleskey, F.K., Rinaldi, M.G., and Del Vecchio, V.G. (1996) DNA fingerprinting of Candida rugosa via repetitive sequence-based PCR. J Clin Microbiol 34: 1677-1681.
55. Shivaprasad, H.L. (2003) Pullorum disease and fowl typhoid. In Diseases of Poultry. Saif, Y.M. (ed.). Ames, IA, USA: Iowa State Press, pp. 568-582.
56. Smith, R.S., Wolfgang, M.C., and Lory, S. (2004) An adenylate cyclase-controlled signaling network regulates Pseudomonas aeruginosa virulence in a mouse model of acute pneumonia. Infect Immun 72: 1677-1684.
57. Stanley, J., Goldsworthy, M., and Threlfall, E.J. (1992) Molecular phylogenetic typing of pandemic isolates of Salmonella enteritidis. FEMS Microbiol Lett 69: 153-160.
58. Stern, M.J., Ames, G.F., Smith, N.H., Robinson, E.C., and Higgins, C.F. (1984) Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell 37: 1015-1026.
59. Sukhnanand, S., Alcaine, S., Warnick, L.D., Su, W.L., Hof, J., Craver, M.P., et al. (2005) DNA sequence-based subtyping and evolutionary analysis of selected Salmonella enterica serotypes. J Clin Microbiol 43: 3688-3698.
60. Swaminathan, B., Barrett, T.J., Hunter, S.B., and Tauxe, R.V. (2001) PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis 7: 382-389.
61. Tang, Y., Guest, J.R., Artymiuk, P.J., Read, R.C., and Green, J. (2004) Post-transcriptional regulation of bacterial motility by aconitase proteins. Mol Microbiol 51: 1817-1826.
62. Thong, K.L., Ngeow, Y.F., Altwegg, M., Navaratnam, P., and Pang, T. (1995) Molecular analysis of Salmonella enteritidis by pulsed-field gel electrophoresis and ribotyping. J Clin Microbiol 33: 1070-1074.
63. Tribe, I.G., Cowell, D., Cameron, P., and Cameron, S. (2002) An outbreak of Salmonella typhimurium phage type 135 infection linked to the consumption of raw shell eggs in an aged care facility. Commun Dis Intell 26: 38-39.
64. Versalovic, J., and Lupski, J.R. (2002) Molecular detection and genotyping of pathogens: more accurate and rapid answers. Trends Microbiol 10: S15-S21.
65. Versalovic, J., Koeuth, T., and Lupski, J.R. (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19: 6823-6831.
66. Ward, L.R., de Sa, J.D., and Rowe, B. (1987) A phage-typing scheme for Salmonella Enteritidis. Epidemiol Infect 99: 291-294.
67. Wigley, P., Hulme, S.D., Powers, C., Beal, R.K., Berchieri, A., Jr, Smith, A., and Barrow, P. (2005) Infection of the reproductive tract and eggs with Salmonella enterica serovar Pullorum in the chicken is associated with suppression of cellular immunity at sexual maturity. Infect Immun 73: 2986-2990.
68. Wolfgang, M.C., Lee, V.T., Gilmore, M.E., and Lory, S. (2003) Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 4: 253-263.
69. Woodward, M.J., Sojka, M., Sprigings, K.A., and Humphrey, T.J. (2000) The role of SEF14 and SEF17 fimbriae in the adherence of Salmonella enterica serotype Enteritidis to inanimate surfaces. J Med Microbiol 49: 481-487.
70. Zhang, X., Kelly, S.M., Bollen, W., and Curtiss, R., III (1999) Protection and immune responses induced by attenuated Salmonella typhimurium UK-1 strains. Microb Pathog 26: 121-130.