Skip to main content
Log in

The exoproteomes of clonally related Staphylococcus aureus strains are diverse

  • Short Communication
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Several studies have shown that protein expression patterns vary in unrelated bacterial strains due to genomic plasticity and gene regulation, resulting in enhanced heterogeneity in the infection potential. However, exoprotein expression patterns of closely related clonal strains have not been well characterized. Here, we used medium-range (pH 4–7) immobilized pH gradient–two-dimensional gel electrophoresis to investigate the exoproteome from closely related Staphylococcus aureus clonal isolates. Interestingly, we found that, under identical in vitro experimental conditions, a number of protein spots were uniquely present in samples from each clonal isolate irregardless of the similarity of the genotype and the same virulence gene profile. Only a few abundant invariant proteins were found among identical genotypic isolates. Our results clearly shown that heterogeneity in the exoproteome was present even among clonally related strains. We suggest that this heterogeneity may contribute to the degree of virulence even within one clonal genotype. The heterogeneity in the exoproteome of closely related S. aureus strains observed in the current study postulates that pre-existing antibodies are not very protective during recurrent infection with the same strain. Therefore, our findings underscore the importance of taking all clonally related strains into account during proteome analyses.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Alibayov B, Zdeňková K, Purkrtová S, Demnerová K, Karpíšková R (2014) Detection of some phenotypic and genotypic characteristics of Staphylococcus aureus isolated from food items in the Czech Republic. Ann Microbiol 64:1587–1596

    Article  CAS  Google Scholar 

  • Alonzo F III, Benson MA, Chen J, Novick RP, Shopsin B, Torres VJ (2012) Staphylococcus aureus leucocidin ED contributes to systemic infection by targeting neutrophils and promoting bacterial growth in vivo. Mol Microbiol 83:423–435

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bernardo K, Fleer S, Pakulat N, Krut O, Hünger F, Krönke M (2002) Identification of Staphylococcus aureus exotoxins by combined sodium dodecyl sulfate gel electrophoresis and matrix-assisted laser desorption/ionization-time of flight mass spectrometry. Proteomics 2:740–746

    Article  CAS  PubMed  Google Scholar 

  • Goering RV (2010) Pulsed field gel electrophoresis: a review of application and interpretation in the molecular epidemiology of infectious disease. Infect Genet Evol 10:866–875

    Article  CAS  PubMed  Google Scholar 

  • Hongo I, Baba T, Oishi K, Morimoto Y, Ito T, Hiramatsu K (2009) Phenol-soluble modulin α3 enhances the human neutrophil lysis mediated by panton-valentine leukocidin. J Infect Dis 200:715–723

    Article  CAS  PubMed  Google Scholar 

  • Jamrozy DM, Fielder MD, Butaye P, Coldham NG (2012) Comparative genotypic and phenotypic characterisation of methicillin-resistant Staphylococcus aureus ST398 isolated from animals and humans. PLoS One 7:e40458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Le Maréchal C, Seyffert N, Jardin J, Hernandez D, Jan G, Rault L, Azevedo V, François P, Schrenzel J, van de Guchte M, Even S, Berkova N, Thiéry R, Fitzgerald JR, Vautor E, Le Loir Y (2011) Molecular basis of virulence in Staphylococcus aureus mastitis. PLoS One 6:e27354

    Article  PubMed Central  PubMed  Google Scholar 

  • Liew YK, Neela V, Hamat RA, Nordin SA, Chong PP (2013) Modified silver staining in 2DE improves protein detection even at extremely low sample concentration. Electrophoresis 34:397–400

    Article  CAS  PubMed  Google Scholar 

  • Munsky B, Neuert G, van Oudenaarden A (2012) Using gene expression noise to understand gene regulation. Science 336:183–187

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Muthukrishnan G, Quinn GA, Lamers RP, Diaz C, Cole AL, Chen S, Cole AM (2011) Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage. J Proteome Res 10:2064–2078

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakano M, Kawano Y, Kawagishi M, Hasegawa T, Iinuma Y, Ohta M (2002) Two-dimensional analysis of exoproteins of methicillin-resistant Staphylococcus aureus (MRSA) for possible epidemiological applications. Microbiol Immunol 46:11–22

    Article  CAS  PubMed  Google Scholar 

  • Sakoulas G, Moellering RC (2008) Increasing antibiotic resistance among methicillin-resistant Staphylococcus aureus strains. Clin Infect Dis 46:S360–S367

    Article  CAS  PubMed  Google Scholar 

  • Shambat S, Nadig S, Prabhakara S, Bes M, Etienne J, Arakere G (2012) Clonal complexes and virulence factors of Staphylococcus aureus from several cities in India. BMC Microbiol 12:64

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ventura CL, Malachowa N, Hammer CH, Nardone GA, Robinson MA, Kobayashi SD, DeLeo FR (2010) Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS One 5:e11634

    Article  PubMed Central  PubMed  Google Scholar 

  • Vydra J, Selicharová I, Smutná K, Sanda M, Matousková E, Bursíková E, Prchalová M, Velenská Z, Coufal D, Jirácek J (2008) Two-dimensional electrophoretic comparison of metastatic and non-metastatic human breast tumors using in vitro cultured epithelial cells derived from the cancer tissues. BMC Cancer 8:107

    Article  PubMed Central  PubMed  Google Scholar 

  • Ziebandt A, Kusch H, Degner M, Jaglitz S, Sibbald MJJB, Arends JP, Chlebowicz MA, Albrecht D, Pantucek R, Doskar J, Ziebuhr W, Bröker BM, Hecker M, van Dijl JM, Engelmann S (2010) Proteomics uncovers extreme heterogeneity in the Staphylococcus aureus exoproteome due to genomic plasticity and variant gene regulation. Proteomics 10:1634–1644

Download references

Acknowledgments

This study was supported by Research University Grant Scheme (04-01-09-0795RU) from Universiti Putra Malaysia.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vasanthakumari Neela.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liew, Y.K., Hamat, R.A., Nordin, S.A. et al. The exoproteomes of clonally related Staphylococcus aureus strains are diverse. Ann Microbiol 65, 1809–1813 (2015). https://doi.org/10.1007/s13213-015-1064-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-015-1064-7

Keywords

Navigation