1887

Journal of Medical Microbiology logo

Volume 68, Issue 3

Characterization of the mechanism and impact of staphylokinase on the formation of Candida albicans and Staphylococcus aureus polymicrobial biofilms Free

Abstract

Purpose. Candida albicans and Staphylococcus aureus can be co-isolated in biofilm-associated infections. However, treatments have not been well established due to a lack of antibiofilm strategies. Hence, this study aims to characterize the mechanism and impact of Staphylokinase (Sak) on fungal-bacterial polymicrobial biofilms.

Methodology. Sak generation levels were obtained via chromogenic analysis. C. albicans and S. aureus polymicrobial biofilm formation and integrity were analysed using a bright-field microscope and scanning electron microscopy (SEM). Metabolic mitochondrial activity, growth rate and adhesive capacity were also measured. Quantification real-time RT-PCR (qRT-PCR) was carried out to evaluate the expression levels of biofilm-related genes. Furthermore, the biofilm inhibitory potential of Sak alone or combined with antimicrobials was investigated.

Results. Sak production levels varied, ranging from 0.130 to 0.648. A strong decrease of biomass, metabolic activity andearly stage growth rate was demonstrated in the Sak-treated group. SEM showed S. aureus attached on hyphae of C. albicans in sporadic small microcolonies after Sak treatment. Moreover, the gene expression levels of HWP1, EFG1 and NRG1 were significantly altered, while no obvious difference was observed in ALS3. Finally, Sak had a notable impact on mature polymicrobial biofilms alone or when combined with vancomycin and fluconazole.

Conclusion.The effect induced by Sak to C. albicans and S. aureus polymicrobial biofilms is caused by decreased biomass, biofilm integrity, metabolic activity and early stage growth rate. Alterations of gene expression levels were consistent with Sak-induced phenotypic change. Combined treatment strategies are essential for optimal activities against fungal-bacterial polymicrobial biofilms.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Candida albicans , polymicrobial biofilms , qRT-PCR , Staphylococcus aureus and Staphylokinase
© 2019 The Authors
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000914
2019-01-10
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jmm/68/3/355.html?itemId=/content/journal/jmm/10.1099/jmm.0.000914&mimeType=html&fmt=ahah

References

  1. Gkana EN, Doulgeraki AI, Chorianopoulos NG, Nychas GE. Anti-adhesion and anti-biofilm potential of organosilane nanoparticles against foodborne pathogens. Front Microbiol 2017; 8:1295 [View Article][PubMed]
     [Google Scholar]
  2. Faix RG, Kovarik SM. Polymicrobial sepsis among intensive care nursery infants. J Perinatol 1989; 9:131–136[PubMed]
     [Google Scholar]
  3. Peters BM, Ward RM, Rane HS, Lee SA, Noverr MC. Efficacy of ethanol against Candida albicans and Staphylococcus aureus polymicrobial biofilms. Antimicrob Agents Chemother 2013; 57:74–82 [View Article][PubMed]
     [Google Scholar]
  4. Lohse MB, Gulati M, Johnson AD, Nobile CJ. Development and regulation of single- and multi-species Candida albicans biofilms. Nat Rev Microbiol 2018; 16:19–31 [View Article]
     [Google Scholar]
  5. de Carvalho Dias K, Barbugli PA, de Patto F, Lordello VB, de Aquino Penteado L et al. Soluble factors from biofilm of Candida albicans and Staphylococcus aureus promote cell death and inflammatory response. BMC Microbiol 2017; 17:146 [View Article][PubMed]
     [Google Scholar]
  6. Baena-Monroy T, Moreno-Maldonado V, Franco-Martínez F, Aldape-Barrios B, Quindós G et al. Candida albicans, Staphylococcus aureus and Streptococcus mutans colonization in patients wearing dental prosthesis. Med Oral Patol Oral Cir Bucal 2005; 10 Suppl 1:E2739[PubMed]
     [Google Scholar]
  7. Kean R, Rajendran R, Haggarty J, Townsend EM, Short B et al. Candida albicans mycofilms support Staphylococcus aureus colonization and enhances miconazole resistance in dual-species interactions. Front Microbiol 2017; 8:258 [View Article][PubMed]
     [Google Scholar]
  8. Carlson E. Effect of strain of Staphylococcus aureus on synergism with Candida albicans resulting in mouse mortality and morbidity. Infect Immun 1983; 42:285–292[PubMed]
     [Google Scholar]
  9. Peters BM, Noverr MC. Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infect Immun 2013; 81:2178–2189 [View Article][PubMed]
     [Google Scholar]
  10. Shirtliff ME, Peters BM, Jabra-Rizk MA. Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett 2009; 299:1–8 [View Article][PubMed]
     [Google Scholar]
  11. Bazari PAM, Honarmand Jahromy S, Zare Karizi S. Phenotypic and genotypic characterization of biofilm formation among Staphylococcus aureus isolates from clinical specimens, an Atomic Force Microscopic (AFM) study. Microb Pathog 2017; 110:533–539 [View Article][PubMed]
     [Google Scholar]
  12. Schlecht LM, Peters BM, Krom BP, Freiberg JA, Hänsch GM et al. Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology 2015; 161:168–181 [View Article][PubMed]
     [Google Scholar]
  13. Bokarewa MI, Jin T, Tarkowski A. Staphylococcus aureus: Staphylokinase. Int J Biochem Cell Biol 2006; 38:504–509 [View Article][PubMed]
     [Google Scholar]
  14. Kwiecinski J, Peetermans M, Liesenborghs L, Na M, Björnsdottir H et al. Staphylokinase Control of Staphylococcus aureus biofilm formation and detachment through host plasminogen activation. J Infect Dis 2016; 213:139–148 [View Article][PubMed]
     [Google Scholar]
  15. Kwiecinski J, Jacobsson G, Karlsson M, Zhu X, Wang W et al. Staphylokinase promotes the establishment of Staphylococcus aureus skin infections while decreasing disease severity. J Infect Dis 2013; 208:990–999 [View Article][PubMed]
     [Google Scholar]
  16. Aubin GG, Lavigne JP, Guyomarch B, Dina C, Gouin F et al. Staphylokinase and ABO group phenotype: new players in Staphylococcus aureus implant-associated infections development. Future Microbiol 2015; 10:1929–1938 [View Article][PubMed]
     [Google Scholar]
  17. Kong EF, Tsui C, Kucharíková S, Andes D, van Dijck P et al. Commensal protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix. MBio 2016; 7: [View Article][PubMed]
     [Google Scholar]
  18. Walencka E, Sadowska B, Rozalska S, Hryniewicz W, Rózalska B. Lysostaphin as a potential therapeutic agent for staphylococcal biofilm eradication. Pol J Microbiol 2005; 54:191–200[PubMed]
     [Google Scholar]
  19. Stewart EJ, Payne DE, Ma TM, Vanepps JS, Boles BR et al. Effect of antimicrobial and physical treatments on growth of multispecies staphylococcal biofilms. Appl Environ Microbiol 2017; 83: [View Article][PubMed]
     [Google Scholar]
  20. Tan Y, Leonhard M, Ma S, Moser D, Schneider-Stickler B. Efficacy of carboxymethyl chitosan against Candida tropicalis and Staphylococcus epidermidis monomicrobial and polymicrobial biofilms. Int J Biol Macromol 2018; 110:150–156 [View Article][PubMed]
     [Google Scholar]
  21. James KM, Macdonald KW, Chanyi RM, Cadieux PA, Burton JP. Inhibition of Candida albicans biofilm formation and modulation of gene expression by probiotic cells and supernatant. J Med Microbiol 2016; 65:328–336 [View Article][PubMed]
     [Google Scholar]
  22. Townsend EM, Sherry L, Kean R, Hansom D, Mackay WG et al. Implications of antimicrobial combinations in complex wound biofilms containing fungi. Antimicrob Agents Chemother 2017; 61: [View Article][PubMed]
     [Google Scholar]
  23. Gabrilska RA, Rumbaugh KP. Biofilm models of polymicrobial infection. Future Microbiol 2015; 10:1997–2015 [View Article][PubMed]
     [Google Scholar]
  24. Harriott MM, Noverr MC. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 2009; 53:3914–3922 [View Article][PubMed]
     [Google Scholar]
  25. Pedrazzoli A, dall'asta L, Guzzon V, Ferrero E. [Synthesis and pharmacological activity of some adamantane derivatives]. Farmaco Sci 1970; 25:822–829[PubMed]
     [Google Scholar]
  26. Bamford CV, D'Mello A, Nobbs AH, Dutton LC, Vickerman MM et al. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect Immun 2009; 77:3696–3704 [View Article][PubMed]
     [Google Scholar]
  27. Brambilla E, Ionescu AC, Cazzaniga G, Ottobelli M, Samaranayake LP. Levorotatory carbohydrates and xylitol subdue Streptococcus mutans and Candida albicans adhesion and biofilm formation. J Basic Microbiol 2016; 56:480–492 [View Article][PubMed]
     [Google Scholar]
  28. Kaplan JB. Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res 2010; 89:205–218 [View Article][PubMed]
     [Google Scholar]
  29. Ibarra-Trujillo C, Villar-Vidal M, Gaitán-Cepeda LA, Pozos-Guillen A, Mendoza-de Elias R et al. [Formation and quantification assay of Candida albicans and Staphylococcus aureus mixed biofilm]. Rev Iberoam Micol 2012; 29:214–222 [View Article][PubMed]
     [Google Scholar]
  30. Uppuluri P, Pierce CG, Thomas DP, Bubeck SS, Saville SP et al. The transcriptional regulator Nrg1p controls Candida albicans biofilm formation and dispersion. Eukaryot Cell 2010; 9:1531–1537 [View Article][PubMed]
     [Google Scholar]
  31. Liu Y, Filler SG. Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot Cell 2011; 10:168–173 [View Article][PubMed]
     [Google Scholar]
  32. Nobile CJ, Nett JE, Andes DR, Mitchell AP. Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot Cell 2006; 5:1604–1610 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000914
Loading
Characterization of the mechanism and impact of staphylokinase on the formation of Candida albicans and Staphylococcus aureus polymicrobial biofilms
J. Med. Microbiol. 68, 355 (2019); https://doi.org/10.1099/jmm.0.000914
/content/journal/jmm/10.1099/jmm.0.000914
/content/journal/jmm/10.1099/jmm.0.000914
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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