1887

Abstract

is an important pathogen of man, but is also able to colonize and cause disease in a wide variety of mammals and birds. An extended multilocus sequencing approach, involving multilocus sequence typing (MLST), typing, typing and typing, was used to examine the molecular diversity of 118 isolates recovered from a range of host species and to compare these data with the known diversity of human-derived isolates. MLST revealed that the commonest animal-associated MLST types were ST133, ST5, ST71, ST97, ST126 and ST151. ST133 appears to be an ungulate-animal-specific genotype, as no evidence of ST133 associating with humans has yet been found in the literature. Novel and unique alleles were identified in the animal-associated strains that may represent animal-associated alleles. However, typing exhibited a lower typeability than MLST for the animal strains (91.3 %). Phylogenetic analyses using neighbour-joining and maximum-parsimony trees localized ruminant-associated MLST lineages to both previously identified subspecies subgroups, thus explaining the finding of all four types within the ruminant-associated strains. isolates recovered from chickens and rabbits were genotypically more similar to known human genotypes than the ruminant-associated lineages.

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2009-10-01
2024-12-08
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References

  1. Aires-de-Sousa M., Parente C. E., Vieira-da-Motta O., Bonna I. C., Silva D. A., de Lencastre H. 2007; Characterization of Staphylococcus aureus isolates from buffalo, bovine, ovine, and caprine milk samples collected in Rio de Janeiro State. Brazil. Appl Environ Microbiol 73:3845–3849 [CrossRef]
    [Google Scholar]
  2. Barkema H. W., Schukken Y. H., Zadoks R. N. 2006; Invited Review: The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci 89:1877–1895 [CrossRef]
    [Google Scholar]
  3. Ben Zakour N. L., Sturdevant D. E., Even S., Guinane C. M., Barbey C., Alves P. D., Cochet M. F., Gautier M., Otto M. other authors 2008; Genome-wide analysis of ruminant Staphylococcus aureus reveals diversification of the core genome. J Bacteriol 190:6302–6317 [CrossRef]
    [Google Scholar]
  4. Cooper J. E., Feil E. J. 2006; The phylogeny of Staphylococcus aureus – which genes make the best intra-species markers?. Microbiology 152:1297–1305 [CrossRef]
    [Google Scholar]
  5. Devriese L. A. 1981; Baird-Parker medium supplemented with acriflavine, polymyxins and sulphonamide for the selective isolation of Staphylococcus aureus from heavily contaminated materials. J Appl Bacteriol 50:351–357 [CrossRef]
    [Google Scholar]
  6. Enright M. C., Day N. P., Davies C. E., Peacock S. J., Spratt B. G. 2000; Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus . J Clin Microbiol 38:1008–1015
    [Google Scholar]
  7. Feil E. J., Cooper J. E., Grundmann H., Robinson D. A., Enright M. C., Berendt T., Peacock S. J., Smith J. M., Murphy M. & other authors; 2003; How clonal is Staphylococcus aureus ?. J Bacteriol 185:3307–3316 [CrossRef]
    [Google Scholar]
  8. Feil E. J., Li B. C., Aanensen D. M., Hanage W. P., Spratt B. G. 2004; eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186:1518–1530 [CrossRef]
    [Google Scholar]
  9. 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]
  10. 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]
  11. Fitzgerald J. R., Sturdevant D. E., Mackie S. M., Gill S. R., Musser J. M. 2001; Evolutionary genomics of Staphylococcus aureus : insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc Natl Acad Sci U S A 98:8821–8826 [CrossRef]
    [Google Scholar]
  12. Foschino R., Invernizzi A., Barucco R., Stradiotto K. 2002; Microbial composition, including the incidence of pathogens, of goat milk from the Bergamo region of Italy during a lactation year. J Dairy Res 69:213–225
    [Google Scholar]
  13. Gilot P., van Leeuwen W. 2004; Comparative analysis of agr locus diversification and overall genetic variability among bovine and human Staphylococcus aureus isolates. J Clin Microbiol 42:1265–1269 [CrossRef]
    [Google Scholar]
  14. Gilot P., Lina G., Cochard T., Poutrel B. 2002; Analysis of the genetic variability of genes encoding the RNA III-activating components Agric and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol 40:4060–4067 [CrossRef]
    [Google Scholar]
  15. Goerke C., Kummel M., Dietz K., Wolz C. 2003; Evaluation of intraspecies interference due to agr polymorphism in Staphylococcus aureus during infection and colonization. J Infect Dis 188:250–256 [CrossRef]
    [Google Scholar]
  16. Grundmann H., Hori S., Tanner G. 2001; Determining confidence intervals when measuring genetic diversity and the discriminatory abilities of typing methods for microorganisms. J Clin Microbiol 39:4190–4192 [CrossRef]
    [Google Scholar]
  17. Guinane C. M., Sturdevant D. E., Herron-Olson L., Otto M., Smyth D. S., Villaruz A. E., Kapur V., Hartigan P. J., Smyth C. J. other authors 2008; Pathogenomic analysis of the common bovine Staphylococcus aureus clone (ET3): emergence of a virulent subtype with potential risk to public health. J Infect Dis 197:205–213 [CrossRef]
    [Google Scholar]
  18. Hermans K., Haesebrouck F., Vaneechoutte M., Devriese L. A., Godard C., De Herdt P. 2000; Differentiation between high and low virulence Staphylococcus aureus strains from rabbits by randomly amplified polymorphic DNA (RAPD) analysis. Vet Microbiol 72:311–319 [CrossRef]
    [Google Scholar]
  19. Hermans K., Devriese L. A., Haesebrouck F. 2003; Rabbit staphylococcosis: difficult solutions for serious problems. Vet Microbiol 91:57–64 [CrossRef]
    [Google Scholar]
  20. 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]
  21. Jorgensen H. J., Mork T., Caugant D. A., Kearns A., Rorvik L. M. 2005; Genetic variation among Staphylococcus aureus strains from Norwegian bulk milk. Appl Environ Microbiol 71:8352–8361 [CrossRef]
    [Google Scholar]
  22. 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]
  23. Korber B. 2000; HIV signature and sequence variation analysis. In Computational Analysis of HIV Molecular Sequences , Chapter 4. pp 55–72 Edited by Rodrigo A. G., Learn G. H. Dordrecht: Kluwer;
  24. Leonard F. C., Markey B. K. 2008; Meticillin-resistant Staphylococcus aureus in animals: a review. Vet J 175:27–36 [CrossRef]
    [Google Scholar]
  25. Lina G., Boutite F., Tristan A., Bes M., Etienne J., Vandenesch F. 2003; Bacterial competition for human nasal cavity colonization: role of Staphylococcal agr alleles. Appl Environ Microbiol 69:18–23 [CrossRef]
    [Google Scholar]
  26. Linares J. A., Wigle W. L. 2001; Staphylococcus aureus pneumonia in turkey poults with gross lesions resembling aspergillosis. Avian Dis 45:1068–1072 [CrossRef]
    [Google Scholar]
  27. Melles D. C., Gorkink R. F., Boelens H. A., Snijders S. V., Peeters J. K., Moorhouse M. J., van der Spek P. J., van Leeuwen W. B., Simons G. other authors 2004; Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus . J Clin Invest 114:1732–1740 [CrossRef]
    [Google Scholar]
  28. Monecke S., Kuhnert P., Hotzel H., Slickers P., Ehricht R. 2007; Microarray based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle. Vet Microbiol 125:128–140 [CrossRef]
    [Google Scholar]
  29. Mork T., Tollersrud T., Kvitle B., Jorgensen H. J., Waage S. 2005; Comparison of Staphylococcus aureus genotypes recovered from cases of bovine, ovine, and caprine mastitis. J Clin Microbiol 43:3979–3984 [CrossRef]
    [Google Scholar]
  30. Rabello R. F., Moreira B. M., Lopes R. M., Teixeira L. M., Riley L. W., Castro A. C. 2007; Multilocus sequence typing of Staphylococcus aureus isolates recovered from cows with mastitis in Brazilian dairy herds. J Med Microbiol 56:1505–1511 [CrossRef]
    [Google Scholar]
  31. Robinson D. A., Enright M. C. 2003; Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus . Antimicrob Agents Chemother 47:3926–3934 [CrossRef]
    [Google Scholar]
  32. Robinson D. A., Enright M. C. 2004; Multilocus sequence typing and the evolution of methicillin-resistant Staphylococcus aureus . Clin Microbiol Infect 10:92–97 [CrossRef]
    [Google Scholar]
  33. Robinson D. A., Monk A. B., Cooper J. E., Feil E. J., Enright M. C. 2005; Evolutionary genetics of the accessory gene regulator ( agr ) locus in Staphylococcus aureus . J Bacteriol 187:8312–8321 [CrossRef]
    [Google Scholar]
  34. Rodgers J. D., McCullagh J. J., McNamee P. T., Smyth J. A., Ball H. J. 1999; Comparison of Staphylococcus aureus recovered from personnel in a poultry hatchery and in broiler parent farms with those isolated from skeletal disease in broilers. Vet Microbiol 69:189–198 [CrossRef]
    [Google Scholar]
  35. Smith E. M., Green L. E., Medley G. F., Bird H. E., Fox L. K., Schukken Y. H., Kruze J. V., Bradley A. J., Zadoks R. N., Dowson C. G. 2005; Multilocus sequence typing of intercontinental bovine Staphylococcus aureus isolates. J Clin Microbiol 43:4737–4743 [CrossRef]
    [Google Scholar]
  36. 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 SaPIbov are predominant among Staphylococcus aureus isolates from cows, goats, sheep, rabbits and poultry. J Med Microbiol 54:401–411 [CrossRef]
    [Google Scholar]
  37. Smyth D. S., Kennedy J., Twohig J., Miajlovic H., Bolton D., Smyth C. J. 2006; Staphylococcus aureus isolates from Irish domestic refrigerators possess novel enterotoxin and enterotoxin-like genes and are clonal in nature. J Food Prot 69:508–515
    [Google Scholar]
  38. Smyth D. S., Meaney W. J., Hartigan P. J., Smyth C. J. 2007; Occurrence of ssl genes in isolates of Staphylococcus aureus from animal infection. J Med Microbiol 56:418–425 [CrossRef]
    [Google Scholar]
  39. Sung J. M., Lindsay J. A. 2007; Staphylococcus aureus strains that are hypersusceptible to resistance gene transfer from enterococci. Antimicrob Agents Chemother 51:2189–2191 [CrossRef]
    [Google Scholar]
  40. Sung J. M., Lloyd D. H., Lindsay J. A. 2008; Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology 154:1949–1959 [CrossRef]
    [Google Scholar]
  41. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [CrossRef]
    [Google Scholar]
  42. Vancraeynest D., Haesebrouck F., Deplano A., Denis O., Godard C., Wildemauwe C., Hermans K. 2006; 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]
  43. van Leeuwen W. B., Melles D. C., Alaidan A., Al-Ahdal M., Boelens H. A., Snijders S. V., Wertheim H., van Duijkeren E., Peeters J. K. other authors 2005; Host- and tissue-specific pathogenic traits of Staphylococcus aureus . J Bacteriol 187:4584–4591 [CrossRef]
    [Google Scholar]
  44. Vautor E., Jay C., Chevalier N., Visomblin N., Vernet G., Pepin M. 2005; Characterization of 26 isolates of Staphylococcus aureus , predominantly from dairy sheep, using four different techniques of molecular epidemiology. J Vet Diagn Invest 17:363–368 [CrossRef]
    [Google Scholar]
  45. Vautor E., Magnone V., Rios G., Le Brigand K., Bergonier D., Lina G., Meugnier H., Barbry P., Thiéry R. other authors 2009; Genetic differences among Staphylococcus aureus isolates from dairy ruminant species: a single-dye DNA microarray approach. Vet Microbiol 133:105–114 [CrossRef]
    [Google Scholar]
  46. Vimercati C., Cremonesi P., Castiglioni B., Pisoni G., Boettcher P. J., Stella A., Vicenzoni G., Moroni P. 2006; Molecular typing of Staphylococcus aureus isolated from cows, goats and sheep with intramammary infections on the basis of gene polymorphisms and toxins genes. J Vet Med B Infect Dis Vet Public Health 53:423–428 [CrossRef]
    [Google Scholar]
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