Skip to main content
SpringerLink
Log in

A new staphylococcal cassette chromosome mec IV encoding a novel cell-wall-anchored surface protein in a major ST8 community-acquired methicillin-resistant Staphylococcus aureus clone in Japan

  • Original Article
  • Published:
Journal of Infection and Chemotherapy

Abstract

Community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA), which has staphylococcal cassette chromosome mec (SCCmec) type IV or V, has become a major concern worldwide. However, the involvement of SCCmecIV (or V) in community spread is still not fully understood. In this study, we searched for a possible adhesin gene in SCCmecIV, which could contribute to community colonization and spread. For this, we determined the entire SCCmecIV sequence of CA-MRSA in Japan, which was previously characterized as multilocus sequence type (ST) 8/SCCmecIVx (type IV with unknown subtypes). The SCCmecIV was 25,555 bp in size and flanked by 15-bp att sequences. The 8.2-kb J1 region was unique (through recombination) and contained a 4.8-kb orf (named spj), encoding for a novel 1,604-amino acid cell-wall-anchored surface protein (CWASP/J) with the LPXTG motif. The spj gene had no homology with any sequence submitted to GenBank, indicating a novel gene sequence. The new SCCmec IV was tentatively designated SCCmecIVl. A PCR assay specific to the spj gene was developed. Two steps of PCR for detection of the spj gene and SCCmecIV showed that ST8/SCCmecIVl MRSA is spreading widely in the community. This study demonstrates a new SCCmecIV encoding a novel CWASP, which could contribute to community spread as a potential colonization factor. Because ST8 CA-MRSA with SCCmecIVl causes skin and soft tissue infections and occasionally invasive infections, surveillance is needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements. Classification of staphylococcal cassette chromosome mec (SCCmec): Guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother. 2009;53:4961–7.

  2. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet. 2006;368:874–85.

    Article  PubMed  Google Scholar 

  3. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis. 2003;9:978–84.

    PubMed  Google Scholar 

  4. Zetola N, Francis JS, Nuermberger EL, Bishai WR. Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis. 2005;5:275–86.

    Article  PubMed  Google Scholar 

  5. Tenover FC, McDougal LK, Goering RV, Killgore G, Projan SJ, Patel JB, et al. Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. J Clin Microbiol. 2006;44:108–18.

    Article  PubMed  CAS  Google Scholar 

  6. Yamamoto T, Nishiyama A, Takano T, Yabe S, Higuchi W, Razvina O, et al. Community-acquired methicillin-resistant Staphylococcus aureus: community transmission, pathogenesis, and drug resistance. J Infect Chemother. 2010;16:225–54.

    Article  PubMed  Google Scholar 

  7. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, des Etages SA, et al. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis. 2008;197:1523–30.

    Article  PubMed  CAS  Google Scholar 

  8. Takano T, Higuchi W, Yamamoto T. Superior in vitro activity of carbapenems over anti-methicillin-resistant Staphylococcus aureus (MRSA) and some related antimicrobial agents for community-acquired MRSA but not for hospital-acquired MRSA. J Infect Chemother. 2009;15:54–7.

    Article  PubMed  CAS  Google Scholar 

  9. Tenover FC, Goering RV. Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology. J Antimicrob Chemother. 2009;64:441–6.

    Article  PubMed  CAS  Google Scholar 

  10. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet. 2006;367:731–9.

    Article  PubMed  CAS  Google Scholar 

  11. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, et al. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA. 2003;290:2976–84.

    Article  PubMed  CAS  Google Scholar 

  12. Takizawa Y, Taneike I, Nakagawa S, Oishi T, Nitahara Y, Iwakura N, et al. A Panton–Valentine leucocidin (PVL)-positive community-acquired methicillin-resistant Staphylococcus aureus (MRSA) strain, another such strain carrying a multiple-drug resistance plasmid, and other more-typical PVL-negative MRSA strains found in Japan. J Clin Microbiol. 2005;43:3356–63.

    Article  PubMed  CAS  Google Scholar 

  13. Takano T, Higuchi W, Otsuka T, Baranovich T, Enany S, Saito K, et al. Novel characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains belonging to multilocus sequence type 59 in Taiwan. Antimicrob Agents Chemother. 2008;52:837–45.

    Article  PubMed  CAS  Google Scholar 

  14. Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:5026–33.

    Article  PubMed  CAS  Google Scholar 

  15. Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, Tiensasitorn C, et al. Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother. 2006;50:1001–12.

    Article  PubMed  CAS  Google Scholar 

  16. Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother. 2007;51:264–74.

    Article  PubMed  CAS  Google Scholar 

  17. Berglund C, Ito T, Ma XX, Ikeda M, Watanabe S, Söderquist B, et al. Genetic diversity of methicillin-resistant Staphylococcus aureus carrying type IV SCCmec in Orebro County and the western region of Sweden. J Antimicrob Chemother. 2009;63:32–41.

    Article  PubMed  CAS  Google Scholar 

  18. Noto MJ, Kreiswirth BN, Monk AB, Archer GL. Gene acquisition at the insertion site for SCCmec, the genomic island conferring methicillin resistance in Staphylococcus aureus. J Bacteriol. 2008;190:1276–83.

    Article  PubMed  CAS  Google Scholar 

  19. Höök M, Foster TJ. Staphylococcal surface proteins. In: Fischetti VA, Novick RP, Fischetti JJ, Potnoy DA, Rood JI, editors. Gram-positive pathogen. Washington, DC: American Society for Microbiology; 2000. p. 386–91.

    Google Scholar 

  20. Clinical and Laboratory Standards Institute. Performance standard for antimicrobial susceptibility testing; 21st informational supplement. M100-S21. Wayne: Clinical and Laboratory Standards Institute; 2011.

  21. Queck SY, Khan BA, Wang R, Bach TH, Kretschmer D, Chen L, et al. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. PLoS Pathog. 2009;5:e1000533.

    Google Scholar 

  22. Mazmanian SK, Ton-That H, Schneewind O. Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol Microbiol. 2001;40:1049–57.

    Article  PubMed  CAS  Google Scholar 

  23. Dedent AC, Marraffini LA, Schneewind O. Staphylococcal sortase and surface proteins. In: Fischetti VA, Novick RP, Fischetti JJ, Potnoy DA, Rood JI, editors. Gram-positive pathogens. 2nd ed. Washington, DC: American Society for Microbiology; 2006. p. 486–95.

    Google Scholar 

  24. Josefsson E, McCrea KW, Ní Eidhin D, O’Connell D, Cox J, Höök M, et al. Three new members of the serine-aspartate repeat protein multigene family of Staphylococcus aureus. Microbiology. 1998;144(Pt 12):3387–95.

    Article  PubMed  CAS  Google Scholar 

  25. Bae T, Schneewind O. The YSIRK-G/S motif of staphylococcal protein A and its role in efficiency of signal peptide processing. J Bacteriol. 2003;185:2910–9.

    Article  PubMed  CAS  Google Scholar 

  26. Zong Y, Xu Y, Liang X, Keene DR, Höök A, Gurusiddappa S, et al. A ‘Collagen Hug’ model for Staphylococcus aureus CNA binding to collagen. EMBO J. 2005;24:4224–36.

    Article  PubMed  CAS  Google Scholar 

  27. Komatsuzawa H, Ohta K, Sugai M, Fujiwara T, Glanzmann P, Berger-Bächi B, et al. Tn551-mediated insertional inactivation of the fmtB gene encoding a cell wall-associated protein abolishes methicillin resistance in Staphylococcus aureus. J Antimicrob Chemother. 2000;45:421–31.

    Article  PubMed  CAS  Google Scholar 

  28. Kahl BC, Peters G. Microbiology. Mayhem in the lung. Science. 2007;315:1082–3.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank and L. K. McDougal and L. L. McDonald for the USA300 type strain, H. de Lencastre for epidemic HA-MRSA-type strains, and Akihito Nishiyama for helpful discussion.

Author information

Authors and Affiliations

  1. Division of Bacteriology, Department of Infectious Disease Control and International Medicine, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan

    Yasuhisa Iwao, Tomomi Takano, Wataru Higuchi & Tatsuo Yamamoto

Authors
  1. Yasuhisa Iwao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomomi Takano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wataru Higuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tatsuo Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tatsuo Yamamoto.

About this article

Cite this article

Iwao, Y., Takano, T., Higuchi, W. et al. A new staphylococcal cassette chromosome mec IV encoding a novel cell-wall-anchored surface protein in a major ST8 community-acquired methicillin-resistant Staphylococcus aureus clone in Japan. J Infect Chemother 18, 96–104 (2012). https://doi.org/10.1007/s10156-011-0348-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10156-011-0348-5

Keywords

Search

Navigation