1887

Abstract

Twenty genes encoding enterotoxin and enterotoxin-like proteins have been described in strains. Five of these occur commonly in the enterotoxin gene cluster (: , , , and ). In the intergenic region, two pseudogenes, and , can be present or an additional gene designated or a variant . Whilst frequencies of loci bearing pseudogenes () or the gene () have been reported, the distinction between bearing and -bearing () loci has rarely been made. A PCR-RFLP procedure involving cleavage of the intergenic region by restriction endonuclease I or I was developed that allowed differentiation of and loci. In addition, PCR primers were designed to yield a 203 bp amplimer for sequencing of a or intragenic region, which encompassed ten signature nucleotide differences. A total of 43 human nasal isolates and 53 bovine, ovine, caprine, leporine and gallinaceous isolates were typed and typed. None of the animal isolates was of type III. A total of 12 out of 17 human nasal isolates were of type III, the other 5 being type I. On the basis of representative multilocus sequence typing, type III/ strains belonged to CC30. Human nasal isolates bearing an locus were distributed evenly across types I, II and III. Only two nasal isolates had an locus. All 14 type IV isolates, only 1 of which was of human origin, possessed an locus. The IV nasal isolate was fusidic acid sensitive and was found to be ST123 (CC121). There were strong associations between bovine, leporine and gallinaceous clonal types and locus types. The PCR-RFLP procedure was used to screen an additional 45 isolates from dogs, cats, rats, pigs and horses for locus types. Of these, 33 were . Six equine isolates were . One canine and three porcine isolates possessed pseudogenes and . One porcine and one canine isolate each had the gene. Putative relationships between disease-causing propensity and egc type need (re-)evaluation.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.005215-0
2009-01-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jmm/58/1/13.html?itemId=/content/journal/jmm/10.1099/jmm.0.005215-0&mimeType=html&fmt=ahah

References

  1. Ayyadevara S., Thaden J. J., Shmookler Reis R. J. 2000; Discrimination of primer 3′-nucleotide mismatch by Taq DNA polymerase during polymerase chain reaction. Anal Biochem 284:11–18 [CrossRef]
    [Google Scholar]
  2. Bania J., Dabrowska A., Korzekwa K., Zarczynska A., Bystron J., Chrzanowska J., Molenda J. 2006a; The profiles of enterotoxin genes in Staphylococcus aureus from nasal carriers. Lett Appl Microbiol 42:315–320 [CrossRef]
    [Google Scholar]
  3. Bania J., Dabrowska A., Bystron J., Korzekwa K., Chrzanowska J., Molenda J. 2006b; Distribution of newly described enterotoxin-like genes in Staphylococcus aureus from food. Int J Food Microbiol 108:36–41 [CrossRef]
    [Google Scholar]
  4. Becker K., Friedrich A. W., Peters G., von Eiff C. 2004; Systematic survey on the prevalence of genes coding for staphylococcal enterotoxins SElM, SElO, and SElN. Mol Nutr Food Res 48:488–495 [CrossRef]
    [Google Scholar]
  5. Blaiotta G., Ercolini D., Pennacchia C., Fusco V., Casaburi A., Pepe O., Villani F. 2004; PCR detection of staphylococcal enterotoxin genes in Staphylococcus spp. strains isolated from meat and dairy products. Evidence for new variants of se G and seI in S. aureus AB-8802. J Appl Microbiol 97:719–730 [CrossRef]
    [Google Scholar]
  6. Blaiotta G., Fusco V., von Eiff C., Villani F., Becker K. 2006; Biotyping of Staphylococcus aureus by enterotoxin gene cluster ( egc ) polymorphism and spa typing analysis. Appl Environ Microbiol 72:6117–6123 [CrossRef]
    [Google Scholar]
  7. Boerema J. A., Clemens R., Brightwell G. 2006; Evaluation of molecular methods to determine enterotoxigenic status and molecular genotype of bovine, ovine, human and food isolates of Staphylococcus aureus . Int J Food Microbiol 107:192–201 [CrossRef]
    [Google Scholar]
  8. Chen T.-R., Chiou C.-S., Tsen H.-Y. 2004; Use of novel PCR primers specific to the genes of staphylococcal enterotoxin G, H, I for the survey of Staphylococcus aureus strains isolated from food-poisoning cases and food samples in Taiwan. Int J Food Microbiol 92:189–197 [CrossRef]
    [Google Scholar]
  9. Chiang Y.-C., Liao W.-W., Fan C.-M., Pai W.-Y., Chiou C.-H., Tsen H.-Y. 2008; PCR detection of staphylococcal enterotoxins (SEs. N O., P Q., R U. and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. Int J Food Microbiol 12166–73 [CrossRef]
    [Google Scholar]
  10. Chini V., Dimitracopoulos G., Spiliopoulou I. 2006; Occurrence of enterotoxin gene cluster and the toxic shock syndrome toxin 1 among clinical isolates of methicillin-resistant Staphylococcus aureus is related to clonal type and agr group. J Clin Microbiol 44:1881–1883 [CrossRef]
    [Google Scholar]
  11. Collery M. M., Smyth C. J. 2007; Rapid differentiation of Staphylococcus aureus isolates harbouring egc loci with pseudogenes ψent1 and ψent2 and the selu or selu v gene using PCR-RFLP. J Med Microbiol 56:208–216 [CrossRef]
    [Google Scholar]
  12. Collery M. M., Smyth D. S., Twohig J. M., Shore A. C., Coleman D. C., Smyth C. J. 2008; Molecular typing of nasal carriage isolates of Staphylococcus aureus from an Irish university student population based on toxin gene PCR, agr locus types and multiple locus, variable number tandem repeat analysis. J Med Microbiol 57:348–358 [CrossRef]
    [Google Scholar]
  13. Diep B. A., Carleton H. A., Chang R. F., Sensabaugh G. F., Perdreau-Remington F. 2006; Roles of 34 virulence genes in the evolution of hospital- and community-associated strains of methicillin-resistant Staphylococcus aureus . J Infect Dis 193:1495–1503 [CrossRef]
    [Google Scholar]
  14. Fitzgerald J. R. 1997; Population analysis of Staphylococcus aureus from bovine mastitis . PhD thesis University of Dublin;
  15. Fitzgerald J. R., Meaney W. J., Hartigan P. J., Smyth C. J., Kapur V. 1997; Fine-structure molecular epidemiological analysis of Staphylococcus aureus recovered from cows. Epidemiol Infect 119:261–269 [CrossRef]
    [Google Scholar]
  16. Fitzgerald J. R., Hartigan P. J., Meaney W. J., Smyth C. J. 2000; Molecular population and virulence factor analysis of Staphylococcus aureus from bovine intramammary infection. J Appl Microbiol 88:1028–1037 [CrossRef]
    [Google Scholar]
  17. Fitzgerald J. R., Monday S. R., Foster T. J., Bohach G. A., Hartigan P. J., Meaney W. J., Smyth C. J. 2001; Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183:63–70 [CrossRef]
    [Google Scholar]
  18. Gilot P., Lina G., Cochard T., Poutrel B. 2002; Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol 40:4060–4067 [CrossRef]
    [Google Scholar]
  19. Herron-Olson L., Fitzgerald J. R., Musser J. M., Kapur V. 2007; Molecular correlates of host specialization in Staphylococcus aureus . PLoS One 2:e1120 [CrossRef]
    [Google Scholar]
  20. Holden M. T. G., Feil E. J., Lindsay J. A., Peacock S. J., Day N. P. J., Enright M. C., Foster T. J., Moore C. E., Hurst L. other authors 2004; Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A 101:9786–9791 [CrossRef]
    [Google Scholar]
  21. Holtfreter S., Grumann D., Schmudde M., Nguyen H. T. T., Eichler P., Strommenger B., Kopron K., Kolata J., Giedrys-Kalemba S. other authors 2007; Clonal distribution of superantigen genes in clinical Staphylococcus isolates. J Clin Microbiol 45:2669–2680 [CrossRef]
    [Google Scholar]
  22. Hwang S. Y., Kim S. H., Jang E. J., Kwon N. H., Park Y. K., Koo H. C., Jung W. K., Kim J. M., Park Y. H. 2007; Novel multiplex PCR for the detection of the Staphyloccus aureus superantigen and its application to raw meat isolates in Korea. Int J Food Microbiol 117:99–105 [CrossRef]
    [Google Scholar]
  23. Iandolo J. J., Worrell V., Groicher K. H., Qian Y., Tian R., Kenton S., Dorman A., Ji H., Loh P. other authors 2002; Comparative analysis of the genomes of the temperate bacteriophages φ 11, φ 12 and φ 13 of Staphylococcus aureus 8325. Gene 289:109–118 [CrossRef]
    [Google Scholar]
  24. Jarraud S., Peyrat M. A., Lim A., Tristan A., Bes M., Mougel C., Etienne J., Vandenesch F., Bonneville M., Lina G. 2001; egc , a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus . J Immunol 166:669–677 [CrossRef]
    [Google Scholar]
  25. Jarraud S., Mougel C., Thioulouse J., Lina G., Meugnier H., Forey F., Nesme X., Etienne J., Vandenesch F. 2002; Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70:631–641 [CrossRef]
    [Google Scholar]
  26. Kapur V., Sischo W. M., Greer R. S., Whittam T. S., Musser J. M. 1995; Molecular population genetic analysis of Staphylococcus aureus recovered from cows. J Clin Microbiol 33:376–380
    [Google Scholar]
  27. Kuhn G., Francioli P., Blanc C. S. 2006; Evidence for clonal evolution among highly polymorphic genes in methicillin-resistant Staphylococcus aureus . J Bacteriol 188:169–178 [CrossRef]
    [Google Scholar]
  28. Kuroda M., Ohta T., Uchiyama I., Baba T., Yuzawa H., Kobayashi I., Cu L., Oguchi A., Aoki K.-I. other authors 2001; Whole genome sequencing of meticillin-resistant Staphylococcus aureus . Lancet 357:1225–1240 [CrossRef]
    [Google Scholar]
  29. Larsen A. R., Skov R. L., Jarlier V., Henriksen A. S. 2008; Epidemiological differences between the UK and Ireland versus France in Staphylococcus aureus isolates resistant to fusidic acid from community-acquired skin and soft tissue infections. J Antimicrob Chemother 61:589–594 [CrossRef]
    [Google Scholar]
  30. Letertre C., Perelle S., Dilasser F., Fach P. 2003; Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus . J Appl Microbiol 95:38–43 [CrossRef]
    [Google Scholar]
  31. Lina G., Bohach G. A., Nair S. P., Hiramatsu K., Jouvin-Marche E., Mariuzza R. 2004; Standard nomenclature for the superantigens expressed by Staphylococcus . J Infect Dis 189:2334–2336 [CrossRef]
    [Google Scholar]
  32. McCullagh J. J., McNamee P. T., Smyth J. A., Ball H. J. 1998; The use of pulsed field gel electrophoresis to investigate the epidemiology of Staphylococcus aureus infection in commercial broiler flocks. Vet Microbiol 63:275–281 [CrossRef]
    [Google Scholar]
  33. Monday S. R., Bohach G. A. 1999; Use of multiplex PCR to detect classical and newly described pyrogenic exotoxin genes in staphylococcal isolates. J Clin Microbiol 37:3411–3414
    [Google Scholar]
  34. Monday S. R., Bohach G. A. 2001; Genes encoding staphylococcal enterotoxins G and I are linked and separated by DNA related to other staphylococcal enterotoxins. J Nat Toxins 10:1–8
    [Google Scholar]
  35. Monecke S., Slickers P., Ehricht R. 2008; Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53:237–251 [CrossRef]
    [Google Scholar]
  36. Munson S. H., Tremaine M. T., Betley M. J., Welch R. A. 1998; Identification and characterization of enterotoxins G and I from Staphylococcus aureus . Infect Immun 66:3337–3348
    [Google Scholar]
  37. Nashev D., Toshkova K., Bizeva L., Akideden Ö., Lämmler C., Zschöck M. 2007; Distribution of enterotoxin genes among carriage- and infection-associated isolates of Staphylococcus aureus . Lett Appl Microbiol 45:681–685 [CrossRef]
    [Google Scholar]
  38. Nitzsche S., Sweifel C., Stephan R. 2007; Phenotypic and genotypic traits of Staphylococcus aureus strains from pig carcasses. Vet Microbiol 120:292–299 [CrossRef]
    [Google Scholar]
  39. Novick R. 1967; Properties of cryptic high-frequency transducing phages in Staphylococcus aureus . Virology 33:155–166 [CrossRef]
    [Google Scholar]
  40. Omoe K., Hu D.-L., Takahashi-Omoe H., Nakane A., Shinagawa K. 2005; Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol Lett 246:191–198 [CrossRef]
    [Google Scholar]
  41. O'Neill A. J., Larsen A. R., Henriksen A. S., Chopra I. 2007; Characterization of the epidemic European fusidic acid-resistant impetigo clone of Staphylococcus aureus . J Clin Microbiol 45:1505–1510 [CrossRef]
    [Google Scholar]
  42. Peacock S. J., Moore C. E., Justice A., Kantzanou M., Story L., Mackie K., O'Neill G., Day N. P. J. 2002; Virulent combinations of adhesion and toxin genes in natural populations of Staphylococcus aureus . Infect Immun 70:4987–4996 [CrossRef]
    [Google Scholar]
  43. Selander R. K., Caugant D. A., Ochman H., Musser J. M., Gilmour M. N., Whittam T. S. 1986; Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol 51:873–884
    [Google Scholar]
  44. Simsek M., Adnan H. 2000; Effect of single mismatches at 3′-end of primers on polymerase chain reaction. Med Sci 2:11–14
    [Google Scholar]
  45. Smyth D. S. 2006; Molecular genetic typing of Staphylococcus aureus from cows, goats, sheep, rabbits and chickens . PhD thesis University of Dublin;
  46. Smyth D. S., Hartigan P. J., Meaney W. J., Fitzgerald J. R., Deobald C. F., Bohach G. A., Smyth C. J. 2005; Superantigen genes encoded by the egc cluster and SaPlbov are predominant among Staphylococcus aureus isolates from cows, goats, sheep, rabbits and poultry. J Med Microbiol 54:401–411 [CrossRef]
    [Google Scholar]
  47. Thomas D. Y., Jarraud S., Lemercier B., Cozon G., Echasserieau K., Etienne J., Gougeon M.-L., Lina G., Vandenesch F. 2006; Staphylococcal enterotoxin-like toxins U2 and V, two new staphylococcal superantigens arising from recombination within the enterotoxin gene cluster. Infect Immun 74:4724–4734 [CrossRef]
    [Google Scholar]
  48. Vancraeynest D., Hermans K., Haesebrouck F. 2006a; Prevalence of genes encoding exfoliative toxins, leucotoxins and superantigens among high and low virulence rabbit Staphylococcus aureus strains. Vet Microbiol 117:211–218 [CrossRef]
    [Google Scholar]
  49. Vancraeynest D., Haesebrouck F., Deplano A., Denis O., Godard C., Wildemauwe C., Hermans K. 2006b; International dissemination of a high virulence rabbit Staphylococcus aureus clone. J Vet Med B Infect Dis Vet Public Health 53:418–422 [CrossRef]
    [Google Scholar]
  50. van Wamel W. J. B., Rooijakkers S. H. M., Ruyken M., van Kessel K. P. M., van Strijp J. A. G. 2006; The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on β -hemolysin-converting bacteriophages. J Bacteriol 188:1310–1315 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.005215-0
Loading
/content/journal/jmm/10.1099/jmm.0.005215-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error