Research Article
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The inhibitory effects of tyrosol on clinical Candida glabrata planktonic and biofilm cells

Year 2022, Volume: 7 Issue: 3, 327 - 337, 31.12.2022
https://doi.org/10.31797/vetbio.1153190

Abstract

Biofilm formation is an important problem in the healthcare industry and veterinary medicine and is very common in natural, industrial or hospital environments. Microorganisms can become very resistant to antimicrobials and environmental factors by biofilm forming on biotic or abiotic surfaces. There is a need to develop new, effective and specific antimicrobials that can reduce pathogenicity in biofilm formation that threatens public health due to their role in medical device-related or infectious diseases. Candida species are opportunistic pathogenic yeasts and can cause superficial or disseminated infections. Especially C. glabrata is one of the most common microorganisms causing fungal infections in immunocompromised patients and drug resistance is observed when associated with biofilm. Tyrosol (2-[4-hydroxyphenyl] ethanol) can act as both a quorum sensing molecule and an exogenous agent on Candida species. In this study, the antifungal activity of tyrosol against a clinical C. glabrata isolate was investigated on both planktonic and biofilm forms. Broth microdilution test results demonstrated the inhibitory effect of tyrosol on C. glabrata. Transmission electron microscopic findings showed that tyrosol affected the planktonic C. glabrata cells in a multi targeted manner, and in the groups treated with tyrosol, significant damage was observed in the cell wall, cell membrane, cytoplasm, nucleus and mitochondria. Also, scanning electron microscopic images confirmed biofilm reduction in pre-/post-biofilm applications as a result of tyrosol treatment. In conclusion, tyrosol may be a potential alternative candidate for reducing the C. glabrata biofilm.

Supporting Institution

Eskisehir Osmangazi University Scientific Research Projects Coordination Unit

Project Number

FDK-2022-2228

Thanks

We thank Eskisehir Osmangazi University Central Research Laboratory Application and Research Center (ARUM) for allowing all facilities and infrastructure to use.

References

  • Arias, L. S., Delbem, A. C. B., Fernandes, R. A., Barbosa, D. B., & Monteiro, D.R.(2016). Activity of tyrosol against single and mixed‐species oral biofilms. Journal of applied microbiology, 120(5), 1240-1249. https://doi.org/10.1111/jam.13070.
  • Bajunaid, S. O., Baras, B. H., Weir, M. D., & Xu, H. H. (2022). Denture Acrylic Resin Material with Antibacterial and Protein-Repelling Properties for the Prevention of Denture Stomatitis. Polymers, 14(2), 230. https://doi.org/10.3390/polym14020230.
  • Bianchi, C.M.P.D.C.; Bianchi, H.A.; Tadano, T.; De Paula, C.R.; Hoffmann-Santos, H.D.; Leite, D.P.L.; Hahn, R.C. (2016). Factors related to oral candidiasis in elderly users and non-users of removable dental prostheses. Revista do Instituto de Medicina Tropical de São Paulo, 58, e17. https://doi.org/10.1590/S1678-9946201658017.
  • Chen, L., Wen, Y. M. (2011). The role of bacterial biofilm in persistent infections and control strategies. International Journal of Oral Science, 3(2), 66-73.
  • Clinical Laboratory Standards Institute, (CLSI). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. Approved Standard-Third Edition, CLSI document M27-A3. Wayne, PA: Clinical and Laboratory Standards Institute; 2008.
  • Cordeiro, R. D. A., Teixeira, C. E., Brilhante, R. S., Castelo-Branco, D. S., Alencar, L. P., de Oliveira, J. S., Monteiro A.J., Bandeira T.J.P.G., Sidrim J.J.C, Moreira, J.L.B., Rocha, M. F. (2015). Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their susceptibility to antifungals. FEMS Yeast Research, 15(4), fov012. https://doi.org/10.1093/femsyr/fov012.
  • Dağ, İ., Yenice Gürsu, Bükay., Dikmen, G., Ulken, Z. (2018). Influence of Carvacrol on the Planktonıc and Biofılm Forms of Salmonella spp And Listerıa Monocytogenes. Fresenius Environmental Bulletin, 27(11), 7270-7277.
  • Décanis, N., Tazi, N., Correia, A., Vilanova, M., & Rouabhia, M. (2011). Farnesol, a fungal quorum-sensing molecule triggers Candida albicans morphological changes by downregulating the expression of different secreted aspartyl proteinase genes. The Open Microbiology Journal, 5: 119-126. doi: 10.2174/1874285801105010119.
  • Donlan, R. M. (2002). Biofilms: microbial life on surfaces. Emerging Infectious Diseases, 8(9), 881. Do Vale, L. R., Delbem, A. C. B., Arias, L. S., Fernandes, R. A., Vieira, A. P. M., Barbosa, D. B., Monteiro, D. R. (2017). Differential effects of the combination of tyrosol with chlorhexidine gluconate on oral biofilms. Oral Diseases, 23(4), 537-541. doi:10.1111/odi.12648.
  • Fidel Jr, P. L., Vazquez, J. A., Sobel, J. D. (1999). Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clinical Microbiology Reviews, 12(1), 80-96. DOI: https://doi.org/10.1128/CMR.12.1.80.
  • Li, L., Redding, S., Dongari-Bagtzoglou, A. (2007). Candida glabrata, an emerging oral opportunistic pathogen. Journal of Dental Research, 86(3), 204-215. https://doi.org/10.1177/154405910708600304.
  • Luo, G., Samaranayake, L. P. (2002). Candida glabrata, an emerging fungal pathogen, exhibits superior relative cell surface hydrophobicity and adhesion to denture acrylic surfaces compared with Candida albicans. Apmis, 110(9), 601-610. https://doi.org/10.1034/j.1600-0463.2002.1100902.x.
  • Monteiro, D. R., Feresin, L. P., Arias, L. S., Barão, V. A. R., Barbosa, D. B., & Delbem, A. C. B. (2015). Effect of tyrosol on adhesion of Candida albicans and Candida glabrata to acrylic surfaces. Medical Mycology, 53(7), 656-665. https://doi.org/10.1093/mmy/myv052.
  • Monteiro, D. R., Arias, L. S., Fernandes, R. A., Deszo da Silva, L. F., de Castilho, M. O. V. F., Da Rosa, T. O., Vieria, A.P.M., Straioto, F.G., Barbosa , D.B., Delbem A.C.B. (2017). Antifungal activity of tyrosol and farnesol used in combination against Candida species in the planktonic state or forming biofilms. Journal of Applied Microbiology, 123(2), 392-400. https://doi.org/10.1111/jam.13513.
  • Odds, F. C. (1994). Pathogenesis of Candida infections. Journal of the American Academy of Dermatology, 31(3), S2-S5. https://doi.org/10.1016/S0190-9622(08)81257-1.
  • Öztürk, B. Y., Gürsu, B. Y., & Dağ, İ. (2020). Antibiofilm and antimicrobial activities of green synthesized silver nanoparticles using marine red algae Gelidium corneum. Process Biochemistry, 89, 208-219. https://doi.org/10.1016/j.procbio.2019.10.027.
  • Ramage, G., Saville, S. P., Wickes, B. L., López-Ribot, J. L. (2002). Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Applied and environmental microbiology, 68(11), 5459-5463. DOI: https://doi.org/10.1128/AEM.68.11.5459-5463.2002.
  • Ramage, G., Saville, S. P., Thomas, D. P., Lopez-Ribot, J. L. (2005). Candida biofilms: an update. Eukaryotic cell, 4(4), 633-638. DOI: https://doi.org/10.1128/EC.4.4.633-638.2005.
  • Rodrigues, C. F., Černáková, L. (2020). Farnesol and tyrosol: secondary metabolites with a crucial quorum-sensing role in Candida biofilm development. Genes, 11(4), 444. https://doi.org/10.3390/genes11040444.
  • Seneviratne, C. J., Silva, W. J., Jin, L. J., Samaranayake, Y. H., Samaranayake, L. P. (2009). Architectural analysis, viability assessment and growth kinetics of Candida albicans and Candida glabrata biofilms. Archives of oral biology, 54(11), 1052-1060. https://doi.org/10.1016/j.archoralbio.2009.08.002.
  • Sharma, D., Misba, L., & Khan, A. U. (2019). Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrobial Resistance & Infection Control, 8(1), 1-10. https://doi.org/10.1186/s13756-019-0533-3.
  • Srinivasan, A., Torres, N. S., Leung, K. P., Lopez-Ribot, J. L., Ramasubramanian, A. K. (2017). nBio chip, a lab-on-a-chip platform of mono-and polymicrobial biofilms for high-throughput downstream applications. Msphere, 2(3), e00247-17. DOI: https://doi.org/10.1128/mSphere.00247-17.
  • Yapıcı, M., Gürsu, B. Y., & Dağ, İ. (2021). In vitro antibiofilm efficacy of farnesol against Candida species. International Microbiology, 24(2), 251-262. https://doi.org/10.1007/s10123-021-00162-4.
  • Yenice Gürsu, B. (2020). Potential antibiofilm activity of farnesol-loaded poly (DL-lactide-co-glycolide)(PLGA) nanoparticles against Candida albicans. Journal of Analytical Science and Technology, 11(1), 1-10. https://doi.org/10.1186/s40543-020-00241-7.
Year 2022, Volume: 7 Issue: 3, 327 - 337, 31.12.2022
https://doi.org/10.31797/vetbio.1153190

Abstract

Project Number

FDK-2022-2228

References

  • Arias, L. S., Delbem, A. C. B., Fernandes, R. A., Barbosa, D. B., & Monteiro, D.R.(2016). Activity of tyrosol against single and mixed‐species oral biofilms. Journal of applied microbiology, 120(5), 1240-1249. https://doi.org/10.1111/jam.13070.
  • Bajunaid, S. O., Baras, B. H., Weir, M. D., & Xu, H. H. (2022). Denture Acrylic Resin Material with Antibacterial and Protein-Repelling Properties for the Prevention of Denture Stomatitis. Polymers, 14(2), 230. https://doi.org/10.3390/polym14020230.
  • Bianchi, C.M.P.D.C.; Bianchi, H.A.; Tadano, T.; De Paula, C.R.; Hoffmann-Santos, H.D.; Leite, D.P.L.; Hahn, R.C. (2016). Factors related to oral candidiasis in elderly users and non-users of removable dental prostheses. Revista do Instituto de Medicina Tropical de São Paulo, 58, e17. https://doi.org/10.1590/S1678-9946201658017.
  • Chen, L., Wen, Y. M. (2011). The role of bacterial biofilm in persistent infections and control strategies. International Journal of Oral Science, 3(2), 66-73.
  • Clinical Laboratory Standards Institute, (CLSI). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. Approved Standard-Third Edition, CLSI document M27-A3. Wayne, PA: Clinical and Laboratory Standards Institute; 2008.
  • Cordeiro, R. D. A., Teixeira, C. E., Brilhante, R. S., Castelo-Branco, D. S., Alencar, L. P., de Oliveira, J. S., Monteiro A.J., Bandeira T.J.P.G., Sidrim J.J.C, Moreira, J.L.B., Rocha, M. F. (2015). Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their susceptibility to antifungals. FEMS Yeast Research, 15(4), fov012. https://doi.org/10.1093/femsyr/fov012.
  • Dağ, İ., Yenice Gürsu, Bükay., Dikmen, G., Ulken, Z. (2018). Influence of Carvacrol on the Planktonıc and Biofılm Forms of Salmonella spp And Listerıa Monocytogenes. Fresenius Environmental Bulletin, 27(11), 7270-7277.
  • Décanis, N., Tazi, N., Correia, A., Vilanova, M., & Rouabhia, M. (2011). Farnesol, a fungal quorum-sensing molecule triggers Candida albicans morphological changes by downregulating the expression of different secreted aspartyl proteinase genes. The Open Microbiology Journal, 5: 119-126. doi: 10.2174/1874285801105010119.
  • Donlan, R. M. (2002). Biofilms: microbial life on surfaces. Emerging Infectious Diseases, 8(9), 881. Do Vale, L. R., Delbem, A. C. B., Arias, L. S., Fernandes, R. A., Vieira, A. P. M., Barbosa, D. B., Monteiro, D. R. (2017). Differential effects of the combination of tyrosol with chlorhexidine gluconate on oral biofilms. Oral Diseases, 23(4), 537-541. doi:10.1111/odi.12648.
  • Fidel Jr, P. L., Vazquez, J. A., Sobel, J. D. (1999). Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clinical Microbiology Reviews, 12(1), 80-96. DOI: https://doi.org/10.1128/CMR.12.1.80.
  • Li, L., Redding, S., Dongari-Bagtzoglou, A. (2007). Candida glabrata, an emerging oral opportunistic pathogen. Journal of Dental Research, 86(3), 204-215. https://doi.org/10.1177/154405910708600304.
  • Luo, G., Samaranayake, L. P. (2002). Candida glabrata, an emerging fungal pathogen, exhibits superior relative cell surface hydrophobicity and adhesion to denture acrylic surfaces compared with Candida albicans. Apmis, 110(9), 601-610. https://doi.org/10.1034/j.1600-0463.2002.1100902.x.
  • Monteiro, D. R., Feresin, L. P., Arias, L. S., Barão, V. A. R., Barbosa, D. B., & Delbem, A. C. B. (2015). Effect of tyrosol on adhesion of Candida albicans and Candida glabrata to acrylic surfaces. Medical Mycology, 53(7), 656-665. https://doi.org/10.1093/mmy/myv052.
  • Monteiro, D. R., Arias, L. S., Fernandes, R. A., Deszo da Silva, L. F., de Castilho, M. O. V. F., Da Rosa, T. O., Vieria, A.P.M., Straioto, F.G., Barbosa , D.B., Delbem A.C.B. (2017). Antifungal activity of tyrosol and farnesol used in combination against Candida species in the planktonic state or forming biofilms. Journal of Applied Microbiology, 123(2), 392-400. https://doi.org/10.1111/jam.13513.
  • Odds, F. C. (1994). Pathogenesis of Candida infections. Journal of the American Academy of Dermatology, 31(3), S2-S5. https://doi.org/10.1016/S0190-9622(08)81257-1.
  • Öztürk, B. Y., Gürsu, B. Y., & Dağ, İ. (2020). Antibiofilm and antimicrobial activities of green synthesized silver nanoparticles using marine red algae Gelidium corneum. Process Biochemistry, 89, 208-219. https://doi.org/10.1016/j.procbio.2019.10.027.
  • Ramage, G., Saville, S. P., Wickes, B. L., López-Ribot, J. L. (2002). Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Applied and environmental microbiology, 68(11), 5459-5463. DOI: https://doi.org/10.1128/AEM.68.11.5459-5463.2002.
  • Ramage, G., Saville, S. P., Thomas, D. P., Lopez-Ribot, J. L. (2005). Candida biofilms: an update. Eukaryotic cell, 4(4), 633-638. DOI: https://doi.org/10.1128/EC.4.4.633-638.2005.
  • Rodrigues, C. F., Černáková, L. (2020). Farnesol and tyrosol: secondary metabolites with a crucial quorum-sensing role in Candida biofilm development. Genes, 11(4), 444. https://doi.org/10.3390/genes11040444.
  • Seneviratne, C. J., Silva, W. J., Jin, L. J., Samaranayake, Y. H., Samaranayake, L. P. (2009). Architectural analysis, viability assessment and growth kinetics of Candida albicans and Candida glabrata biofilms. Archives of oral biology, 54(11), 1052-1060. https://doi.org/10.1016/j.archoralbio.2009.08.002.
  • Sharma, D., Misba, L., & Khan, A. U. (2019). Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrobial Resistance & Infection Control, 8(1), 1-10. https://doi.org/10.1186/s13756-019-0533-3.
  • Srinivasan, A., Torres, N. S., Leung, K. P., Lopez-Ribot, J. L., Ramasubramanian, A. K. (2017). nBio chip, a lab-on-a-chip platform of mono-and polymicrobial biofilms for high-throughput downstream applications. Msphere, 2(3), e00247-17. DOI: https://doi.org/10.1128/mSphere.00247-17.
  • Yapıcı, M., Gürsu, B. Y., & Dağ, İ. (2021). In vitro antibiofilm efficacy of farnesol against Candida species. International Microbiology, 24(2), 251-262. https://doi.org/10.1007/s10123-021-00162-4.
  • Yenice Gürsu, B. (2020). Potential antibiofilm activity of farnesol-loaded poly (DL-lactide-co-glycolide)(PLGA) nanoparticles against Candida albicans. Journal of Analytical Science and Technology, 11(1), 1-10. https://doi.org/10.1186/s40543-020-00241-7.
There are 24 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

Zarifeh Adampour 0000-0001-6505-4999

Betül Yılmaz Öztürk 0000-0002-1817-8240

İlknur Dağ 0000-0002-7352-8653

Project Number FDK-2022-2228
Publication Date December 31, 2022
Submission Date August 4, 2022
Acceptance Date December 13, 2022
Published in Issue Year 2022 Volume: 7 Issue: 3

Cite

APA Adampour, Z., Yılmaz Öztürk, B., & Dağ, İ. (2022). The inhibitory effects of tyrosol on clinical Candida glabrata planktonic and biofilm cells. Journal of Advances in VetBio Science and Techniques, 7(3), 327-337. https://doi.org/10.31797/vetbio.1153190

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