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Relationship Between Adhesin Genes and Biofilm Formation in Vancomycin-Intermediate Staphylococcus aureus Clinical Isolates

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Abstract

The adherence ability and biofilm production are the characteristic of enhanced virulence among isolates of vancomycin-intermediate Staphylococcus aureus (VISA) strains. Although biofilm-forming properties have been well demonstrated in S. aureus, they still remain unclear among the recently emerged types of VISA strains. The aim of this study was to investigate correlations between the distribution of genes encoding staphylococcal microbial surface components which recognise adhesive matrix molecules (MSCRAMMs), the surface protein A (Spa) types, MLST types and the ability of VISA strains to biofilm formation. Microtiter plate assay (Mtp) results showed that all eleven biofilm producer isolates were adherent at various levels. PCR experiments showed that nine MSCRAMM genes, clfA, clfB, fnbA and fib were detected in all of the strains, indicating a high prevalence. The prevalences of other MSCRAMMs and icaABCD genes were found to be variable and not equally distributed among the VISA strains. There was no direct correlation between the distribution of adhesion-related genes and biofilm formation, which indicates that the presence or absence of these genes cannot be employed as an indicator of the ability to biofilm formation. Isolates which belong to the same Spa and ST types showed similar adherence capacities in the Mtp assay, but significant differences were observed between different Spa types. The findings of this study, using quantitative methods, have shown that genotypically different strains of VISA have different capabilities to produce biofilms. This may be caused by a difference in the spa types of VISA isolates or due to their differences in the expression of MSCRAMM and icaABCD genes.

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References

  1. Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW (2012) Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 33(26):5967–5982

    Article  CAS  PubMed  Google Scholar 

  2. Atshan SS, Nor Shamsudin M, Sekawi Z, Lung LT, Hamat RA, Karunanidhi A, Mateg Ali A, Ghaznavi-Rad E, Ghasemzadeh-Moghaddam H, Chong Seng JS, Nathan JJ, Pei CP (2012) Prevalence of adhesion and regulation of biofilm-related genes in different clones of Staphylococcus aureus. J Biomed Biotechnol 2012:976972

  3. Azimian A, Asghar Havaei S, Fazeli H, Naderi M, Ghazvini K, Mirab Samiee S, Soleimani M, Najar Peerayeh S (2012) Genetic analysis of a vancomycin-resistant Staphylococcus aureus strain isolated in Iran. J Clin Microbiol 50(11):3581–3585

    Article  PubMed Central  PubMed  Google Scholar 

  4. Azimian A, Havaei SA, Fazeli H, Naderi M, Ghazvini K, Samiee SM, Soleimani M, Peerayeh SN (2012) Genetic characterization of a vancomycin-resistant Staphylococcus aureus isolate from the respiratory tract of a patient in a university hospital in northeastern Iran. J Clin Microbiol 50(11):3581–3585

    Article  PubMed Central  PubMed  Google Scholar 

  5. Butt T, Ahmad RN, Usman M, Mahmood A (2003) Vancomycin-resistance Staphylococcus aureus. J Coll Phys Surg Pak 13(7):428–429

    Google Scholar 

  6. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322

    Article  CAS  PubMed  Google Scholar 

  7. Croes S, Deurenberg RH, Boumans M-LL, Beisser PS, Neef C, Stobberingh EE (2009) Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiol 9(1):229

    Article  PubMed Central  PubMed  Google Scholar 

  8. Cucarella C, Tormo MA, Knecht E, Amorena B, Lasa I, Foster TJ, Penades JR (2002) Expression of the biofilm-associated protein interferes with host protein receptors of Staphylococcus aureus and alters the infective process. Infect Immun 70(6):3180–3186

    Article  PubMed Central  PubMed  Google Scholar 

  9. Cucarella C, Tormo MA, Ubeda C, Trotonda MP, Monzon M, Peris C, Amorena B, Lasa I, Penades JR (2004) Role of biofilm-associated protein bap in the pathogenesis of bovine Staphylococcus aureus. Infect Immun 72(4):2177–2185

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Cue D, Lei MG, Luong TT, Kuechenmeister L, Dunman PM, O’Donnell S, Rowe S, O’Gara JP, Lee CY (2009) Rbf promotes biofilm formation by Staphylococcus aureus via repression of icaR, a negative regulator of icaADBC. J Bacteriol 191(20):6363–6373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23(3):616–687

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38(3):1008–1015

    PubMed Central  CAS  PubMed  Google Scholar 

  13. Havaei SA, Azimian A, Fazeli H, Naderi M, Ghazvini K, Samiee SM, Masoumi Z, Akbari M (2012) Genetic characterization of methicillin resistant and sensitive, vancomycin intermediate Staphylococcus aureus strains isolated from different Iranian Hospitals. ISRN Microbiol 2012:6

    Article  Google Scholar 

  14. Hiramatsu K (2001) Vancomycin-resistant Staphylococcus aureus: a new model of antibiotic resistance. Lancet Infect Dis 1(3):147–155

    Article  CAS  PubMed  Google Scholar 

  15. Howden BP, Davies JK, Johnson PD, Stinear TP, Grayson ML (2010) Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev 23(1):99–139

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Howden BP, Johnson PD, Ward PB, Stinear TP, Davies JK (2006) Isolates with low-level vancomycin resistance associated with persistent methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 50(9):3039–3047

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Jefferson KK, Pier DB, Goldmann DA, Pier GB (2004) The teicoplanin-associated locus regulator (TcaR) and the intercellular adhesin locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus. J Bacteriol 186(8):2449–2456

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Kiem S, Oh WS, Peck KR, Lee NY, Lee JY, Song JH, Hwang ES, Kim EC, Cha CY, Choe KW (2004) Phase variation of biofilm formation in Staphylococcus aureus by IS 256 insertion and its impact on the capacity adhering to polyurethane surface. J Korean Med Sci 19(6):779–782

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48(6):1429–1449

    Article  CAS  PubMed  Google Scholar 

  20. Periasamy S, Joo HS, Duong AC, Bach TH, Tan VY, Chatterjee SS, Cheung GY, Otto M (2012) How Staphylococcus aureus biofilms develop their characteristic structure. Proc Natl Acad Sci USA 109(4):1281–1286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, Buckingham-Meyer K, Stewart PS (2007) Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189(11):4223–4233

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Rohde H, Knobloch JK, Horstkotte MA, Mack D (2001) Correlation of Staphylococcus aureus icaADBC genotype and biofilm expression phenotype. J Clin Microbiol 39(12):4595–4596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Sakoulas G, Eliopoulos GM, Moellering RC Jr, Wennersten C, Venkataraman L, Novick RP, Gold HS (2002) Accessory gene regulator (agr) locus in geographically diverse Staphylococcus aureus isolates with reduced susceptibility to vancomycin. Antimicrob Agents Chemother 46(5):1492–1502

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Seo YS, Lee DY, Rayamahji N, Kang ML, Yoo HS (2008) Biofilm-forming associated genotypic and phenotypic characteristics of Staphylococcus spp. isolated from animals and air. Res Vet Sci 85(3):433–438

    Article  CAS  PubMed  Google Scholar 

  25. Shopsin B, Gomez M, Montgomery S, Smith D, Waddington M, Dodge D, Bost D, Riehman M, Naidich S, Kreiswirth B (1999) Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37(11):3556–3563

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Stepanovic S, Vukovic D, Hola V, Di Bonaventura G, Djukic S, Cirkovic I, Ruzicka F (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115(8):891–899

    Article  PubMed  Google Scholar 

  27. Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G (2003) Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol 41(9):4465–4467

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the Tarbiat Modares University and conducted in the Department of Bacteriology, Faculty of Medical Sciences as part of Ph.D thesis.The authors would like to thank Dr. Ehsanollah Ghaznavi-Rad (Arak University of Medical Sciences) for providing control strains.

Disclosure

All authors report no conflicts of interest relevant to this article.

Funding

This work was supported by Grants from Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran.

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Authors and Affiliations

  1. Department of Bacteriology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

    Mohsen Mirzaee & Shahin Najar-Peerayeh

  2. Department of Genetics, School of Biological Science, Tarbiat Modares University, Tehran, Iran

    Mehrdad Behmanesh

  3. Department of Biotechnology, Faculty of Medicine, Tarbiat Modares University, Tehran, Iran

    Mahdi Forouzandeh Moghadam

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  1. Mohsen Mirzaee
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  2. Shahin Najar-Peerayeh
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  3. Mehrdad Behmanesh
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  4. Mahdi Forouzandeh Moghadam
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Correspondence to Shahin Najar-Peerayeh.

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Mirzaee, M., Najar-Peerayeh, S., Behmanesh, M. et al. Relationship Between Adhesin Genes and Biofilm Formation in Vancomycin-Intermediate Staphylococcus aureus Clinical Isolates. Curr Microbiol 70, 665–670 (2015). https://doi.org/10.1007/s00284-014-0771-9

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  • DOI: https://doi.org/10.1007/s00284-014-0771-9

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