1887

Abstract

A recent increase in virulence of pathogenic subsp (SDSE) has been widely proposed. Such an increase may be partly explained by the acquisition of new virulence traits by horizontal gene transfer from related streptococci such as (GAS) and (GBS). A collection of 54 SDSE strains isolated in Italy in the years 2000–2010 from different sources (paediatric throat carriage, invasive and non-invasive diseases) was characterized by typing and pulsed-field gel electrophoresis (PFGE) analysis. The virulence repertoire was evaluated by PCR for the presence of GAS superantigen () genes, the streptolysin S () gene, the group G fibronectin-binding protein () gene and GAS–GBS alpha-like protein family ( genes; moreover, the ability to invade human epithelial cells was investigated. Resistance to tetracycline, erythromycin and clindamycin was assessed. The combined use of typing and PFGE proved to be a reliable strategy for the epidemiological analysis of SDSE isolates. The most frequent types were the same as those more frequently reported in other studies, thus indicating the diffusion of a limited number of a few successful types fit to disseminate in humans. The gene was detected in SDSE strains of different genetic backgrounds. Erythromycin resistance determined by the (T) gene, and the unusual, foggy MLS phenotype, observed in one and seven strains, respectively, have never previously, to our knowledge, been reported in SDSE. Moreover, a new member of the family was identified. The identification of new antibiotic and virulence determinants, despite the small size of the sample analysed, shows the importance of constant attention to monitoring the extent of lateral gene transfer in this emerging pathogen.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.062109-0
2014-01-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/1/90.html?itemId=/content/journal/jmm/10.1099/jmm.0.062109-0&mimeType=html&fmt=ahah

References

  1. Ahmad Y., Gertz R. E. Jr, Li Z., Sakota V., Broyles L. N., Van Beneden C., Facklam R., Shewmaker P. L., Reingold A.& other authors ( 2009; Genetic relationships deduced from emm and multilocus sequence typing of invasive Streptococcus dysgalactiae subsp. equisimilis and S. canis recovered from isolates collected in the United States. J Clin Microbiol 47:2046–2054 [View Article][PubMed]
    [Google Scholar]
  2. Bessen D. E., Carapetis J. R., Beall B., Katz R., Hibble M., Currie B. J., Collingridge T., Izzo M. W., Scaramuzzino D. A., Sriprakash K. S. 2000; Contrasting molecular epidemiology of group A streptococci causing tropical and nontropical infections of the skin and throat. J Infect Dis 182:1109–1116 [View Article][PubMed]
    [Google Scholar]
  3. Brandt C. M., Spellerberg B. 2009; Human infections due to Streptococcus dysgalactiae subspecies equisimilis. Clin Infect Dis 49:766–772 [View Article][PubMed]
    [Google Scholar]
  4. Broyles L. N., Van Beneden C., Beall B., Facklam R., Shewmaker P. L., Malpiedi P., Daily P., Reingold A., Farley M. M. 2009; Population-based study of invasive disease due to beta-hemolytic streptococci of groups other than A and B. Clin Infect Dis 48:706–712 [View Article][PubMed]
    [Google Scholar]
  5. Choi S. C., Rasmussen M. D., Hubisz M. J., Gronau I., Stanhope M. J., Siepel A. 2012; Replacing and additive horizontal gene transfer in Streptococcus. Mol Biol Evol 29:3309–3320 [View Article][PubMed]
    [Google Scholar]
  6. Creti R., Fabretti F., Orefici G., von Hunolstein C. 2004; Multiplex PCR assay for direct identification of group B streptococcal alpha-protein-like protein genes. J Clin Microbiol 42:1326–1329 [View Article][PubMed]
    [Google Scholar]
  7. Creti R., Imperi M., Baldassarri L., Pataracchia M., Recchia S., Alfarone G., Orefici G. 2007a; emm types, virulence factors, and antibiotic resistance of invasive Streptococcus pyogenes isolates from Italy: what has changed in 11 years?. J Clin Microbiol 45:2249–2256 [View Article][PubMed]
    [Google Scholar]
  8. Creti R., Imperi M., Baldassarri L., Pataracchia M., Alfarone G., Orefici G. 2007b; Lateral transfer of alpha-like protein gene cassettes among streptococci: identification of a new family member in Streptococcus dysgalactiae subsp. equisimilis.. Lett Appl Microbiol 44:224–227 [View Article][PubMed]
    [Google Scholar]
  9. Creti R., Baldassarri L., Montanaro L., Arciola C. R. 2008; The alpha-like surface proteins: an example of an expanding family of adhesins. Int J Artif Organs 31:834–840[PubMed]
    [Google Scholar]
  10. DiPersio L. P., DiPersio J. R., Beach J. A., Loudon A. M., Fuchs A. M. 2011; Identification and characterization of plasmid-borne erm(T) macrolide resistance in group B and group A Streptococcus. Diagn Microbiol Infect Dis 71:217–223 [View Article][PubMed]
    [Google Scholar]
  11. Facinelli B., Spinaci C., Magi G., Giovanetti E., Varaldo P. E. 2001; Association between erythromycin resistance and ability to enter human respiratory cells in group A streptococci. Lancet 358:30–33 [View Article][PubMed]
    [Google Scholar]
  12. Haidan A., Talay S. R., Rohde M., Sriprakash K. S., Currie B. J., Chhatwal G. S. 2000; Pharyngeal carriage of group C and group G streptococci and acute rheumatic fever in an Aboriginal population. Lancet 356:1167–1169 [View Article][PubMed]
    [Google Scholar]
  13. 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 [View Article][PubMed]
    [Google Scholar]
  14. Igwe E. I., Shewmaker P. L., Facklam R. R., Farley M. M., Van Beneden C., Beall B. 2003; Identification of superantigen genes speM, ssa, and smeZ in invasive strains of beta-hemolytic group C and G streptococci recovered from humans. FEMS Microbiol Lett 229:259–264 [View Article][PubMed]
    [Google Scholar]
  15. Jensen A., Kilian M. 2012; Delineation of Streptococcus dysgalactiae, its subspecies, and its clinical and phylogenetic relationship to Streptococcus pyogenes.. J Clin Microbiol 50:113–126 [View Article][PubMed]
    [Google Scholar]
  16. Korem M., Hidalgo-Grass C., Michael-Gayego A., Nir-Paz R., Salameh S., Moses A. E. 2013; Streptococcal pyrogenic exotoxin G gene in blood and pharyngeal isolates of Streptococcus dysgalactiae subspecies equisimilis has a limited role in pathogenesis. J Microbiol Immunol Infect [View Article][PubMed]
    [Google Scholar]
  17. Makarova K. S., Haft D. H., Barrangou R., Brouns S. J., Charpentier E., Horvath P., Moineau S., Mojica F. J., Wolf Y. I.& other authors ( 2011; Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9:467–477 [View Article][PubMed]
    [Google Scholar]
  18. Malhotra-Kumar S., Lammens C., Piessens J., Goossens H. 2005; Multiplex PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob Agents Chemother 49:4798–4800 [View Article][PubMed]
    [Google Scholar]
  19. McDonald M., Towers R. J., Andrews R. M., Carapetis J. R., Currie B. J. 2007; Epidemiology of Streptococcus dysgalactiae subsp. equisimilis in tropical communities, Northern Australia. Emerg Infect Dis 13:1694–1700 [View Article][PubMed]
    [Google Scholar]
  20. McMillan D. J., Bessen D. E., Pinho M., Ford C., Hall G. S., Melo-Cristino J., Ramirez M. 2010; Population genetics of Streptococcus dysgalactiae subspecies equisimilis reveals widely dispersed clones and extensive recombination. PLoS ONE 5:e11741 [View Article][PubMed]
    [Google Scholar]
  21. Ng L. K., Martin I., Alfa M., Mulvey M. 2001; Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215 [View Article][PubMed]
    [Google Scholar]
  22. Okumura K., Shimomura Y., Murayama S. Y., Yagi J., Ubukata K., Kirikae T., Miyoshi-Akiyama T. 2012; Evolutionary paths of streptococcal and staphylococcal superantigens. BMC Genomics 13:404 [View Article][PubMed]
    [Google Scholar]
  23. Palmieri C., Rätsch I. M., Princivalli M. S., Candelaresi C., Magi G., Spinaci C., Coppa G. V., Facinelli B. 2007; erm(A)-mediated macrolide resistance and ability to invade human respiratory cells in a Streptococcus dysgalactiae subspecies equisimilis pharyngeal isolate. J Antimicrob Chemother 60:1405–1406 [View Article][PubMed]
    [Google Scholar]
  24. Palmieri C., Magi G., Creti R., Baldassarri L., Imperi M., Gherardi G., Facinelli B. 2013; Interspecies mobilization of an erm (T)-carrying plasmid of Streptococcus dysgalactiae subsp. equisimilis by a coresident ICE of the ICESa2603 family. J Antimicrob Chemother 68:23–26 [View Article][PubMed]
    [Google Scholar]
  25. Pinho M. D., Melo-Cristino J., Ramirez M. 2006; Clonal relationships between invasive and noninvasive Lancefield group C and G streptococci and emm-specific differences in invasiveness. J Clin Microbiol 44:841–846 [View Article][PubMed]
    [Google Scholar]
  26. Rantala S., Vahakuopus S., Vuopio-Varkila J., Vuento R., Syrjanen J. 2010; Streptococcus dysgalactiae subsp. equisimilis bacteremia, Finland, 1995–2004. Emerg Infect Dis 16:843–846 [View Article][PubMed]
    [Google Scholar]
  27. Rohde M., Graham R. M., Branitzki-Heinemann K., Borchers P., Preuss C., Schleicher I., Zähner D., Talay S. R., Fulde M.& other authors ( 2011; Differences in the aromatic domain of homologous streptococcal fibronectin-binding proteins trigger different cell invasion mechanisms and survival rates. Cell Microbiol 13:450–468 [View Article][PubMed]
    [Google Scholar]
  28. Rohde M., Talay S. R., Rasmussen M. 2012; Molecular mechanisms of Streptococcus dysgalactiae subsp. equisimilis enabling intravascular persistence. Microbes Infect 14:329–334 [View Article][PubMed]
    [Google Scholar]
  29. Shimomura Y., Okumura K., Murayama S. Y., Yagi J., Ubukata K., Kirikae T., Miyoshi-Akiyama T. 2011; Complete genome sequencing and analysis of a Lancefield group G Streptococcus dysgalactiae subsp. equisimilis strain causing streptococcal toxic shock syndrome (STSS). BMC Genomics 12:17 [View Article][PubMed]
    [Google Scholar]
  30. Sitkiewicz I., Green N. M., Guo N., Mereghetti L., Musser J. M. 2011; Lateral gene transfer of streptococcal ICE element RD2 (region of difference 2) encoding secreted proteins. BMC Microbiol 11:65 [View Article][PubMed]
    [Google Scholar]
  31. Stanton T. B., Humphrey S. B. 2003; Isolation of tetracycline-resistant Megasphaera elsdenii strains with novel mosaic gene combinations of tet(O) and tet(W) from swine. Appl Environ Microbiol 69:3874–3882 [View Article][PubMed]
    [Google Scholar]
  32. Suzuki H., Lefébure T., Hubisz M. J., Pavinski Bitar P., Lang P., Siepel A., Stanhope M. J. 2011; Comparative genomic analysis of the Streptococcus dysgalactiae species group: gene content, molecular adaptation, and promoter evolution. Genome Biol Evol 3:168–185 [View Article][PubMed]
    [Google Scholar]
  33. van Belkum A., Tassios P. T., Dijkshoorn L., Haeggman S., Cookson B., Fry N. K., Fussing V., Green J., Feil E.& other authors ( 2007; Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect 13:Suppl. 31–46 [View Article][PubMed]
    [Google Scholar]
  34. Vandamme P., Pot B., Falsen E., Kersters K., Devriese L. A. 1996; Taxonomic study of Lancefield streptococcal groups C, G, and L (Streptococcus dysgalactiae) and proposal of S. dysgalactiae subsp. equisimilis subsp. nov. Int J Syst Bacteriol 46:774–781 [View Article][PubMed]
    [Google Scholar]
  35. Varaldo P. E., Montanari M. P., Giovanetti E. 2009; Genetic elements responsible for erythromycin resistance in streptococci. Antimicrob Agents Chemother 53:343–353 [View Article][PubMed]
    [Google Scholar]
  36. Watanabe S., Kirikae T., Miyoshi-Akiyama T. 2013; Complete genome sequence of Streptococcus dysgalactiae subsp. equisimilis 167 carrying Lancefield group C antigen and comparative genomics of S. dysgalactiae subsp. equisimilis strains. Genome Biol Evol 5:1644–1651 [View Article][PubMed]
    [Google Scholar]
  37. Yoon E. J., Kwon A. R., Min Y. H., Choi E. C. 2008; Foggy D-shaped zone of inhibition in Staphylococcus aureus owing to a dual character of both inducible and constitutive resistance to macrolide–lincosamide–streptogramin B. J Antimicrob Chemother 61:533–540 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.062109-0
Loading
/content/journal/jmm/10.1099/jmm.0.062109-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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