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Characteristics and distribution of plasmids in a clonally diverse set of methicillin-resistant Staphylococcus aureus strains

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Abstract

The aim of this study was to compare the plasmid contents of methicillin-resistant Staphylococcus aureus (MRSA) strains classified into different clonal clusters (CCs). The isolates were collected from 15 Czech hospitals in 2000–2008. Plasmid DNA was detected in 65 (89%) strains, and 33 of them harbored more than one plasmid type. Altogether 24 different types of plasmids were identified, ranging in size from 1.3 to 55 kb. Restriction endonuclease analysis, plasmid elimination, DNA hybridization, and sequencing were used for their further characterization. It has been found that the conjugative, erythromycin resistance and enterotoxin D encoding plasmids are harbored by strains from different CCs. On the other hand, chloramphenicol and tetracycline resistance plasmids, and most of the penicillinase and cryptic plasmids were only detected in certain CCs. Especially, the pUSA300-like plasmids were found exclusively in the USA300 clone strains. The high diversity in plasmid content detected in the study strains implies that plasmids play a major role in evolution of MRSA clonal lineages.

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References

  • Booth MC, Pence LM, Mahasreshti P, Callegan MC, Gilmore MS (2001) Clonal associations among Staphylococcus aureus isolates from various sites of infection. Infect Immun 69:345–352

    Article  PubMed  CAS  Google Scholar 

  • Brady JM, Stemper ME, Weigel A, Chyou PH, Reed KD, Shukla SK (2007) Sporadic “transitional” community-associated methicillin-resistant Staphylococcus aureus strains from health care facilities in the United States. J Clin Microbiol 45:2654–2661

    Article  PubMed  CAS  Google Scholar 

  • Caddick JM, Hilton AC, Rollason J, Lambert PA, Worthington T, Elliott TS (2005) Molecular analysis of methicillin-resistant Staphylococcus aureus reveals an absence of plasmid DNA in multidrug-resistant isolates. FEMS Immunol Med Microbiol 44:297–302

    Article  PubMed  CAS  Google Scholar 

  • Catchpole I, Thomas C, Davies A, Dyke KG (1988) The nucleotide sequence of Staphylococcus aureus plasmid pT48 conferring inducible macrolide–lincosamide–streptogramin B resistance and comparison with similar plasmids expressing constitutive resistance. J Gen Microbiol 134:697–709

    PubMed  CAS  Google Scholar 

  • CLSI (2010) Performance standards for antimicrobial susceptibility testing: 20th informational supplement. CLSI publication M100-S20. Clinical and Laboratory Standard Institute, Wayne

  • Cockfield JD, Pathak S, Edgeworth JD, Lindsay JA (2007) Rapid determination of hospital-acquired meticillin-resistant Staphylococcus aureus lineages. J Med Microbiol 56:614–619

    Article  PubMed  CAS  Google Scholar 

  • Coia JE, Noor-Hussain I, Platt DJ (1988) Plasmid profiles and restriction enzyme fragmentation patterns of plasmids of methicillin-sensitive and methicillin-resistant isolates of Staphylococcus aureus from hospital and the community. J Med Microbiol 27:271–276

    Article  PubMed  CAS  Google Scholar 

  • Corvaglia AR, Francois P, Hernandez D, Perron K, Linder P, Schrenzel J (2010) A type III-like restriction endonuclease functions as a major barrier to horizontal gene transfer in clinical Staphylococcus aureus strains. Proc Natl Acad Sci USA 107:11954–11958

    Article  PubMed  CAS  Google Scholar 

  • Cristino JAG, Pereira AT (1989) Plasmid analysis of 219 methicillin-resistant Staphylococcus aureus strains with uncommon profiles isolated in Lisbon. J Hosp Infect 13:133–141

    Article  PubMed  CAS  Google Scholar 

  • Diep BA, Carleton HA, Chang RF, Sensabaugh GF, Perdreau-Remington F (2006a) 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

    Article  PubMed  CAS  Google Scholar 

  • Diep BA, Gill SR, Chang RF et al (2006b) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367:731–739

    Article  PubMed  CAS  Google Scholar 

  • Goerke C, Pantucek R, Holtfreter S et al (2009) Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191:3462–3468

    Article  PubMed  CAS  Google Scholar 

  • Highlander SK, Hulten KG, Qin X et al (2007) Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiol 7:99

    Article  PubMed  Google Scholar 

  • Hiramatsu K, Suzuki E, Takayama H, Katayama Y, Yokota T (1990) Role of penicillinase plasmids in the stability of the mecA gene in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 34:600–604

    PubMed  CAS  Google Scholar 

  • Holden MT, Feil EJ, Lindsay JA et al (2004) Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA 101:9786–9791

    Article  PubMed  CAS  Google Scholar 

  • Holtfreter S, Grumann D, Schmudde M et al (2007) Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol 45:2669–2680

    Article  PubMed  CAS  Google Scholar 

  • Horinouchi S, Weisblum B (1982) Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J Bacteriol 150:815–825

    PubMed  CAS  Google Scholar 

  • Jarraud S, Mougel C, Thioulouse J et al (2002) Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70:631–641

    Article  PubMed  CAS  Google Scholar 

  • Johnson WM, Tyler SD, Ewan EP, Ashton FE, Pollard DR, Rozee KR (1991) Detection of genes for enterotoxins, exfoliative toxins, and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reaction. J Clin Microbiol 29:426–430

    PubMed  CAS  Google Scholar 

  • Kennedy AD, Porcella SF, Martens C et al (2010) Complete nucleotide sequence analysis of plasmids in strains of Staphylococcus aureus clone USA300 reveals a high level of identity among isolates with closely related core genome sequences. J Clin Microbiol 48:4504–4511

    Article  PubMed  CAS  Google Scholar 

  • Khan SA, Novick RP (1983) Complete nucleotide sequence of pT181, a tetracycline-resistance plasmid from Staphylococcus aureus. Plasmid 10:251–259

    Article  PubMed  CAS  Google Scholar 

  • Lina G, Piemont Y, Godail-Gamot F et al (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29:1128–1132

    Article  PubMed  CAS  Google Scholar 

  • Lindsay JA, Moore CE, Day NP et al (2006) Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J Bacteriol 188:669–676

    Article  PubMed  CAS  Google Scholar 

  • Martineau F, Picard FJ, Grenier L, Roy PH, Ouellette M, Bergeron MG (2000) Multiplex PCR assays for the detection of clinically relevant antibiotic resistance genes in staphylococci isolated from patients infected after cardiac surgery. The ESPRIT Trial. J Antimicrob Chemother 46:527–534

    Article  PubMed  CAS  Google Scholar 

  • Melter O, Aires de Sousa M, Urbaskova P, Jakubu V, Zemlickova H, de Lencastre H (2003) Update on the major clonal types of methicillin-resistant Staphylococcus aureus in the Czech Republic. J Clin Microbiol 41:4998–5005

    Article  PubMed  CAS  Google Scholar 

  • Milheirico C, Oliveira DC, de Lencastre H (2007) Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob Agents Chemother 51:3374–3377

    Article  PubMed  CAS  Google Scholar 

  • Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215

    Article  PubMed  CAS  Google Scholar 

  • Novick RP (1987) Plasmid incompatibility. Microbiol Rev 51:381–395

    PubMed  CAS  Google Scholar 

  • Novick RP (2008) The mobile genetic elements of Staphylococcus aureus. In: Hensel M, Schmidt H (eds) Horizontal gene transfer in the evolution of pathogenesis. Cambridge University Press, Cambridge, pp 237–272

    Chapter  Google Scholar 

  • Oliveira DC, Wu SW, de Lencastre H (2000) Genetic organization of the downstream region of the mecA element in methicillin-resistant Staphylococcus aureus isolates carrying different polymorphisms of this region. Antimicrob Agents Chemother 44:1906–1910

    Article  PubMed  CAS  Google Scholar 

  • Omoe K, Hu DL, Takahashi-Omoe H, Nakane A, Shinagawa K (2003) Identification and characterization of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect Immun 71:6088–6094

    Article  PubMed  CAS  Google Scholar 

  • Pantucek R, Gotz F, Doskar J, Rosypal S (1996) Genomic variability of Staphylococcus aureus and the other coagulase-positive Staphylococcus species estimated by macrorestriction analysis using pulsed-field gel electrophoresis. Int J Syst Bacteriol 46:216–222

    Article  PubMed  CAS  Google Scholar 

  • Rolain JM, Francois P, Hernandez D et al (2009) Genomic analysis of an emerging multiresistant Staphylococcus aureus strain rapidly spreading in cystic fibrosis patients revealed the presence of an antibiotic inducible bacteriophage. Biol Direct 4:1

    Article  PubMed  Google Scholar 

  • Růžičková V, Voller J, Pantůček R, Petráš P, Doškař J (2005) Multiplex PCR for detection of three exfoliative toxin serotype genes in Staphylococcus aureus. Folia Microbiol 50:499–502

    Article  Google Scholar 

  • Shopsin B, Gomez M, Montgomery SO et al (1999) Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37:3556–3563

    PubMed  CAS  Google Scholar 

  • Skov RL, Jensen KS (2009) Community-associated meticillin-resistant Staphylococcus aureus as a cause of hospital-acquired infections. J Hosp Infect 73:364–370

    Article  PubMed  CAS  Google Scholar 

  • Sonstein SA, Baldwin JN (1972) Loss of the penicillinase plasmid after treatment of Staphylococcus aureus with sodium dodecyl sulfate. J Bacteriol 109:262–265

    PubMed  CAS  Google Scholar 

  • Strommenger B, Kettlitz C, Werner G, Witte W (2003) Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol 41:4089–4094

    Article  PubMed  CAS  Google Scholar 

  • Strommenger B, Kettlitz C, Weniger T, Harmsen D, Friedrich AW, Witte W (2006) Assignment of Staphylococcus isolates to groups by spa typing, SmaI macrorestriction analysis, and multilocus sequence typing. J Clin Microbiol 44:2533–2540

    Article  PubMed  CAS  Google Scholar 

  • Taylor DE, Gibreel A, Lawley TD, Tracz DM (2004) Antibiotic resistance plasmids. In: Funnell BE, Phillips GJ (eds) Plasmid biology. ASM Press, Washington, pp 473–491

    Google Scholar 

  • Waldron DE, Lindsay JA (2006) Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J Bacteriol 188:5578–5585

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank M. Kolářová, A. Ševčíková, and M. Hanslianová from the University Hospital Brno for collecting MRSA isolates and Eva Kodytková for valuable help. We gratefully acknowledge the financial support of the European Union (grant LSHM-CT-2006-019064) (StaphDynamics), Czech Science Foundation (310/09/0459), and Ministry of Education, Youth and Sports of the Czech Republic (MSM 0021622415).

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Authors and Affiliations

  1. Department of Experimental Biology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37, Brno, Czech Republic

    Lucie Kuntová, Roman Pantůček, Jana Rájová, Vladislava Růžičková, Ivana Mašlaňová & Jiří Doškař

  2. National Reference Laboratory for Staphylococci, National Institute of Public Health, 100 42, Prague, Czech Republic

    Petr Petráš

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  1. Lucie Kuntová
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  2. Roman Pantůček
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  3. Jana Rájová
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  4. Vladislava Růžičková
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  6. Ivana Mašlaňová
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  7. Jiří Doškař
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Correspondence to Jiří Doškař.

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Communicated by Sebastian Suerbaum.

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Kuntová, L., Pantůček, R., Rájová, J. et al. Characteristics and distribution of plasmids in a clonally diverse set of methicillin-resistant Staphylococcus aureus strains. Arch Microbiol 194, 607–614 (2012). https://doi.org/10.1007/s00203-012-0797-y

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  • DOI: https://doi.org/10.1007/s00203-012-0797-y

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