1887

Abstract

The zoonotic pathogen subsp. () is commonly found harmlessly colonizing the equine nasopharynx. Occasionally, strains can invade host tissues or cross species barriers, and is associated with numerous different diseases in a variety of hosts, including inflammatory airway disease and abortion in horses, pneumonia in dogs and meningitis in humans. A biovar of , subsp. , is the causative agent of strangles, one of the most important infections of horses worldwide. We report here the development of the first multilocus sequence typing (MLST) scheme for and its exploitation to define the population genetic structure of these related pathogens. A total of 130 unique sequence types were identified from 277 isolates of diverse geographical and temporal origin. Isolates of shared a recent evolutionary ancestor with isolates of that were significantly associated with cases of uterine infection or abortion in horses (<0.001). Isolates of from three UK outbreaks of acute fatal haemorrhagic pneumonia in dogs during 1999, 2001 and 2008 were found to be related to isolates from three outbreaks of this disease in the USA during 2005, 1993 and 2006, respectively. Our data provide strong evidence that evolved from an ancestral strain and that certain related strains of have a greater propensity to infect particular hosts and tissues.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/018911-0
2008-10-01
2019-10-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/10/3016.html?itemId=/content/journal/micro/10.1099/mic.0.2008/018911-0&mimeType=html&fmt=ahah

References

  1. Bradley, S. F., Gordon, J. J., Baumgartner, D. D., Marasco, W. A. & Kauffman, C. A. ( 1991; ). Group C streptococcal bacteremia: analysis of 88 cases. Rev Infect Dis 13, 270–280.[CrossRef]
    [Google Scholar]
  2. Breiman, R. F. & Silverblatt, F. J. ( 1986; ). Systemic Streptococcus equi infection in a horse handler – a case of human strangles. West J Med 145, 385–386.
    [Google Scholar]
  3. Brooks, D. E., Andrew, S. E., Biros, D. J., Denis, H. M., Cutler, T. J., Strubbe, D. T. & Gelatt, K. N. ( 2000; ). Ulcerative keratitis caused by beta-hemolytic Streptococcus equi in 11 horses. Vet Ophthalmol 3, 121–125.[CrossRef]
    [Google Scholar]
  4. Chalker, V. J., Brooks, H. W. & Brownlie, J. ( 2003; ). The association of Streptococcus equi subsp. zooepidemicus with canine infectious respiratory disease. Vet Microbiol 95, 149–156.[CrossRef]
    [Google Scholar]
  5. Chanter, N., Collin, N., Holmes, N., Binns, M. & Mumford, J. ( 1997; ). Characterization of the Lancefield group C Streptococcus 16S–23S RNA gene intergenic spacer and its potential for identification and sub-specific typing. Epidemiol Infect 118, 125–135.[CrossRef]
    [Google Scholar]
  6. Coffey, T. J., Pullinger, G. D., Urwin, R., Jolley, K. A., Wilson, S. M., Maiden, M. C. & Leigh, J. A. ( 2006; ). First insights into the evolution of Streptococcus uberis: a multilocus sequence typing scheme that enables investigation of its population biology. Appl Environ Microbiol 72, 1420–1428.[CrossRef]
    [Google Scholar]
  7. Didelot, X. & Falush, D. ( 2007; ). Inference of bacterial microevolution using multilocus sequence data. Genetics 175, 1251–1266.
    [Google Scholar]
  8. Downar, J., Willey, B. M., Sutherland, J. W., Mathew, K. & Low, D. E. ( 2001; ). Streptococcal meningitis resulting from contact with an infected horse. J Clin Microbiol 39, 2358–2359.[CrossRef]
    [Google Scholar]
  9. Elsayed, S., Hammerberg, O., Massey, V. & Hussain, Z. ( 2003; ). Streptococcus equi subspecies equi (Lancefield group C) meningitis in a child. Clin Microbiol Infect 9, 869–872.[CrossRef]
    [Google Scholar]
  10. Enright, M. C. & Spratt, B. G. ( 1998; ). A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144, 3049–3060.[CrossRef]
    [Google Scholar]
  11. Enright, M. C., Spratt, B. G., Kalia, A., Cross, J. H. & Bessen, D. E. ( 2001; ). Multilocus sequence typing of Streptococcus pyogenes and the relationships between emm type and clone. Infect Immun 69, 2416–2427.[CrossRef]
    [Google Scholar]
  12. Feil, E. J., Holmes, E. C., Bessen, D. E., Chan, M. S., Day, N. P., Enright, M. C., Goldstein, R., Hood, D. W., Kalia, A. & other authors ( 2001; ). Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci U S A 98, 182–187.[CrossRef]
    [Google Scholar]
  13. 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]
  14. Hashikawa, S., Iinuma, Y., Furushita, M., Ohkura, T., Nada, T., Torii, K., Hasegawa, T. & Ohta, M. ( 2004; ). Characterization of group C and G streptococcal strains that cause streptococcal toxic shock syndrome. J Clin Microbiol 42, 186–192.[CrossRef]
    [Google Scholar]
  15. Holmes, E. C., Urwin, R. & Maiden, M. C. ( 1999; ). The influence of recombination on the population structure and evolution of the human pathogen Neisseria meningitidis. Mol Biol Evol 16, 741–749.[CrossRef]
    [Google Scholar]
  16. Hong, C. B., Donahue, J. M., Giles, R. C., Jr, Petrites-Murphy, M. B., Poonacha, K. B., Roberts, A. W., Smith, B. J., Tramontin, R. R., Tuttle, P. A. & Swerczek, T. W. ( 1993; ). Etiology and pathology of equine placentitis. J Vet Diagn Invest 5, 56–63.[CrossRef]
    [Google Scholar]
  17. Jolley, K. A., Feil, E. J., Chan, M. S. & Maiden, M. C. ( 2001; ). Sequence type analysis and recombinational tests (START). Bioinformatics 17, 1230–1231.[CrossRef]
    [Google Scholar]
  18. Jolley, K. A., Chan, M. S. & Maiden, M. C. ( 2004; ). mlstdbNet – distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5, 86 [CrossRef]
    [Google Scholar]
  19. Jorm, L. R., Love, D. N., Bailey, G. D., McKay, G. M. & Briscoe, D. A. ( 1994; ). Genetic structure of populations of beta-haemolytic Lancefield group C streptococci from horses and their association with disease. Res Vet Sci 57, 292–299.[CrossRef]
    [Google Scholar]
  20. Kelly, C., Bugg, M., Robinson, C., Mitchell, Z., Davis-Poynter, N., Newton, J. R., Jolley, K. A., Maiden, M. C. & Waller, A. S. ( 2006; ). Sequence variation of the SeM gene of Streptococcus equi allows discrimination of the source of strangles outbreaks. J Clin Microbiol 44, 480–486.[CrossRef]
    [Google Scholar]
  21. Ladlow, J., Scase, T. & Waller, A. ( 2006; ). Canine strangles case reveals a new host susceptible to infection with Streptococcus equi. J Clin Microbiol 44, 2664–2665.[CrossRef]
    [Google Scholar]
  22. Las Heras, A., Vela, A. I., Fernandez, E., Legaz, E., Dominguez, L. & Fernandez-Garayzabal, J. F. ( 2002; ). Unusual outbreak of clinical mastitis in dairy sheep caused by Streptococcus equi subsp. zooepidemicus. J Clin Microbiol 40, 1106–1108.[CrossRef]
    [Google Scholar]
  23. Lindmark, H., Jonsson, P., Engvall, E. & Guss, B. ( 1999; ). Pulsed-field gel electrophoresis and distribution of the genes zag and fnz in isolates of Streptococcus equi. Res Vet Sci 66, 93–99.[CrossRef]
    [Google Scholar]
  24. Maiden, M. C. ( 2006; ). Multilocus sequence typing of bacteria. Annu Rev Microbiol 60, 561–588.[CrossRef]
    [Google Scholar]
  25. Maiden, M. C., Bygraves, J. A., Feil, E., Morelli, G., Russell, J. E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K. & other authors ( 1998; ). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95, 3140–3145.[CrossRef]
    [Google Scholar]
  26. Nei, M. & Gojobori, T. ( 1986; ). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418–426.
    [Google Scholar]
  27. Newton, J. R., Laxton, R., Wood, J. L. & Chanter, N. ( 2008; ). Molecular epidemiology of Streptococcus zooepidemicus infection in naturally occurring equine respiratory disease. Vet J 175, 338–345.[CrossRef]
    [Google Scholar]
  28. Pesavento, P. A., Hurley, K. F., Bannasch, M. J., Artiushin, S. & Timoney, J. F. ( 2008; ). A clonal outbreak of acute fatal hemorrhagic pneumonia in intensively housed (shelter) dogs caused by Streptococcus equi subsp. zooepidemicus. Vet Pathol 45, 51–53.[CrossRef]
    [Google Scholar]
  29. Popescu, G. A., Fuerea, R. & Benea, E. ( 2006; ). Meningitis due to an unusual human pathogen: Streptococcus equi subspecies equi. South Med J 99, 190–191.[CrossRef]
    [Google Scholar]
  30. Salasia, S. I., Wibawan, I. W., Pasaribu, F. H., Abdulmawjood, A. & Lammler, C. ( 2004; ). Persistent occurrence of a single Streptococcus equi subsp. zooepidemicus clone in the pig and monkey population in Indonesia. J Vet Sci 5, 263–265.
    [Google Scholar]
  31. 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]
  32. Sharp, M. W., Prince, M. J. & Gibbens, J. ( 1995; ). S. zooepidemicus infection and bovine mastitis. Vet Rec 137, 128
    [Google Scholar]
  33. Smith, K. C., Blunden, A. S., Whitwell, K. E., Dunn, K. A. & Wales, A. D. ( 2003; ). A survey of equine abortion, stillbirth and neonatal death in the UK from 1988 to 1997. Equine Vet J 35, 496–501.
    [Google Scholar]
  34. Soedarmanto, I., Pasaribu, F. H., Wibawan, I. W. & Lammler, C. ( 1996; ). Identification and molecular characterization of serological group C streptococci isolated from diseased pigs and monkeys in Indonesia. J Clin Microbiol 34, 2201–2204.
    [Google Scholar]
  35. Stevenson, R. G. ( 1974; ). Streptococcus zooepidemicus infection in sheep. Can J Comp Med 38, 243–250.
    [Google Scholar]
  36. Sweeney, C. R., Timoney, J. F., Newton, J. R. & Hines, M. T. ( 2005; ). Streptococcus equi infections in horses: guidelines for treatment, control and prevention of strangles. J Vet Intern Med 19, 123–134.[CrossRef]
    [Google Scholar]
  37. Swofford, D. L. ( 2003; ). paup*: Phylogenetic analysis using parsimony (and other methods). Sunderland, MA: Sinauer Associates.
  38. Timoney, J. F. ( 1993; ). Strangles. Vet Clin North Am Equine Pract 9, 365–374.
    [Google Scholar]
  39. Walker, J. A. & Timoney, J. F. ( 1998; ). Molecular basis of variation in protective SzP proteins of Streptococcus zooepidemicus. Am J Vet Res 59, 1129–1133.
    [Google Scholar]
  40. Waller, A. S. & Jolley, K. A. ( 2007; ). Getting a grip on strangles: recent progress towards improved diagnostics and vaccines. Vet J 173, 492–501.[CrossRef]
    [Google Scholar]
  41. Wood, J. L., Burrell, M. H., Roberts, C. A., Chanter, N. & Shaw, Y. ( 1993; ). Streptococci and Pasteurella spp. associated with disease of the equine lower respiratory tract. Equine Vet J 25, 314–318.[CrossRef]
    [Google Scholar]
  42. Wood, J. L., Newton, J. R., Chanter, N. & Mumford, J. A. ( 2005; ). Association between respiratory disease and bacterial and viral infections in British racehorses. J Clin Microbiol 43, 120–126.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/018911-0
Loading
/content/journal/micro/10.1099/mic.0.2008/018911-0
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