FTIR SPECTRAL CHANGES IN Candida albicans BIOFILM FOLLOWING EXPOSURE TO ANTIFUNGALS
Keywords:
Candida, fungal pathogen, biofilm formation, antibiofilm , FTIR spectroscopyAbstract
Candida albicans is a microbial fungus that exists as a commensal member of the human microbiome and an opportunistic pathogen. Biofilm formation by this fungal pathogen occurs mostly in the mucosa or endothelium associated with candidiasis and colonizes medical devices. The present work was performed to determine the efficacy of the antifungal creams on the viability and biochemical composition of C. albicans biofilm. Four commercial antifungal creams were used herein namely econazole nitrate, miconazole nitrate, ketoconazole and tolnaftate. Resazurin assay and Fourier transform infrared (FTIR) spectroscopy were performed to determine the viability and biochemical composition of C. albicans biofilm, respectively. Results demonstrated that the antifungal creams inhibited C. albicans biofilm. The highest percent inhibition shown by econazole nitrate, miconazole nitrate, ketoconazole, and tolnaftate were 16.5%, 17.1%, 15.8%, and 6.9%, respectively. Econazole nitrate with the lowest IC50 value of 43.42 µg/mL caused changes in the FTIR spectral peak shape at 1377 cm-1 and 1736 cm-1. On the other hand, miconazole nitrate with the second lowest IC50 value of 118.26 µg/mL caused spectral peak shifting from 1237 cm-1 to 1228 cm-1. In conclusion, the inhibition of C. albicans biofilm may be mediated by the changes in protein, lipid, and nucleic acid compositions.
Downloads
Metrics
References
Abd, E.R.M., Mohamed, D., Abo, M., Ela, E., Fadl, G. & Gad, M. 2014. N-acetylcysteine inhibits and eradicates Candida albicans biofilms. American Journal of Infectious Diseases and Microbiology, 2(5): 122–130. DOI: https://doi.org/10.12691/ajidm-2-5-5
Adt, I., Toubas, D., Pinon, J., Mi., Manfait, M. & Sockalingum, G.D. 2006. FTIR spectroscopy as a potential tool to analyse structural modifications during morphogenesis of Candida albicans. Archives of Microbiology, 185(4): 277–285. DOI: https://doi.org/10.1007/s00203-006-0094-8
Aging, T. & Munajad, A. 2018. Fourier transform infrared (FTIR) spectroscopy analysis of transformer paper in mineral oil-paper composite insulation under accelerated thermal aging. Energies, 11: 364. DOI: https://doi.org/10.3390/en11020364
Alsterholm, M., Karami, N. & Faergemann, J. 2010. Antimicrobial activity of topical skin pharmaceuticals – an in vitro study. Acta Dermato-Venereologica, 90: 239–245. DOI: https://doi.org/10.2340/00015555-0840
Berthomieu, C. & Hienerwadel, R. 2009. Fourier transform infrared (FTIR) spectroscopy. Photosysnthesis Research, 101(2): 157–170. DOI: https://doi.org/10.1007/s11120-009-9439-x
Bhat, R. 2013. Potential use of Fourier transform infrared spectroscopy for identification of molds capable of producing mycotoxins. International Journal of Food Properties, 16(8): 1819–1829. DOI: https://doi.org/10.1080/10942912.2011.609629
Bojsen, R., Regenberg, B. & Folkesson, A. 2014. Saccharomyces cerevisiae biofilm tolerance towards systemic antifungals depends on growth phase. BMC Microbiology, 14(1): 1–10. DOI: https://doi.org/10.1186/s12866-014-0305-4
Bombalska, A., Mularczyk-Oliwa, M., Kwaśny, M., Włodarski, M., Kaliszewski, M., Kopczyński, K. & Trafny, E.A. 2011. Classification of the biological material with use of FTIR spectroscopy and statistical analysis. Spectrochimica Acta - Part A: Molecular and Biomolecular Spectroscopy, 78(4): 1221–1226. DOI: https://doi.org/10.1016/j.saa.2010.10.025
Coban, A.Y., Uzun, M., Akgunes, A. & Durupinar, B. 2012. Comparative evaluation of the microplate nitrate reductase assay and the rezasurin microtitre assay for the rapid detection of multidrug resistant Mycobacterium tuberculosis clinical isolates. Memórias Do Instituto Oswaldo Cruz, 107(5): 578–581. DOI: https://doi.org/10.1590/S0074-02762012000500002
Essendoubi, M., Toubas, D., Bouzaggou, M., Pinon, J.M., Manfait, M. & Sockalingum, G.D. 2005. Rapid identification of Candida species by FT-IR microspectroscopy. Biochimica et Biophysica Acta - General Subjects, 1724(3): 239–247. DOI: https://doi.org/10.1016/j.bbagen.2005.04.019
Fiołka, M.J., Mieszawska, S., Czaplewska, P., Szymańska, A., Stępnik, K., Chmiel, W.S. & Lewtak, K. 2020. Candida albicans cell wall as a target of action for the protein – carbohydrate fraction from coelomic fluid of Dendrobaena veneta. Scientific Reports, 10: 1–19. DOI: https://doi.org/10.1038/s41598-020-73044-w
Gebremedhin, S., Dorocka-Bobkowska, B., Prylinski, M., Konopka, K. & Duzgunes, N. 2014. Miconazole activity against Candida biofilms developed on acrylic discs. Journal of Physiology and Pharmacology, 65(4): 593–600.
Gulati, M. & Nobile, C.J. 2016. Candida albicans biofilms: development, regulation and molecular mechanisms. Microbes and Infection, 18(5): 310–321. DOI: https://doi.org/10.1016/j.micinf.2016.01.002
Hani, U., Shiva, G., Vaghela, R., Osmani, R.A.M. & Shrivastava, A. 2015. Candidiasis : A fungal infection- current challenges and progress in prevention and treatment. Infectious Disorders – Drug Targets, 15(1): 42–52. https://doi.org/10.2174/1871526515666150320162036 DOI: https://doi.org/10.2174/1871526515666150320162036
Hasan, F., Xess, I., Wang, X., Jain, N. & Fries, B.C. 2009. Biofilm formation in clinical Candida isolates and its association with virulence. Microbes and Infection, 11(8–9): 753–761. DOI: https://doi.org/10.1016/j.micinf.2009.04.018
Isa, S.F.M., Hamid, U.M.A. & Yahya, M.F.Z.R. 2022. Treatment with the combined antimicrobials triggers proteomic changes in P. aeruginosa-C. albicans polyspecies
biofilms. ScienceAsia, 48(2): 215-222.
Johari, N.A., Amran, S.S.D., Kamaruzzaman, A.N.A., Man, C.A.I.C. & Yahya, M.F.Z.R. 2020. Anti-biofilm potential and mode of action of malaysian plant species: A review. Science Letters, 14: 34–46. DOI: https://doi.org/10.24191/sl.v14i2.9541
Križková, L., Ďuračková, Z., Šandula, J., Sasinková, V. & Krajčovič, J. 2001. Antioxidative and antimutagenic activity of yeast cell wall mannans in vitro. Mutation Research - Genetic Toxicology and Environmental Mutagenesis, 497(1–2): 213–222. DOI: https://doi.org/10.1016/S1383-5718(01)00257-1
Lal, P., Sharma, D., Pruthi, P. & Pruthi, V. 2010. Exopolysaccharide analysis of biofilm-forming Candida albicans. Journal of Applied Microbiology, 109(1): 128–136. DOI: https://doi.org/10.1111/j.1365-2672.2009.04634.x
Marak, M.B. & Dhanashree, B. 2018. Antifungal susceptibility and biofilm production of Candida spp. isolated from clinical samples. International Journal of Microbiology, 2018: 7495218. DOI: https://doi.org/10.1155/2018/7495218
Naseer, K., Ali, S. & Qazi, J. 2020. ATR-FTIR spectroscopy as the future of diagnostics: a systematic review of the approach using bio-fluids. Applied Spectroscopy Reviews, 56: 85–97. DOI: https://doi.org/10.1080/05704928.2020.1738453
Natalello, A., Ami, D., Brocca, S., Lotti, M. & Doglia, S.M. 2005. Secondary structure, conformational stability and glycosylation of a recombinant Candida rugosa lipase studied by Fourier-transform infrared spectroscopy. Biochemical Journal, 385(2): 511–517. DOI: https://doi.org/10.1042/BJ20041296
Othman, N.A. & Yahya, M.F.Z.R. 2019. In silico analysis of essential gene and non-homologous proteins in Salmonella typhimurium biofilm. Journal of Physics: Conference Series, 1349: 012133. DOI: https://doi.org/10.1088/1742-6596/1349/1/012133
Pebotuwa, S., Kochan, K., Peleg, A., Wood, B.R. & Heraud, P. 2020. Influence of the sample preparation method in discriminating Candida spp. using ATR-FTIR spectroscopy. Molecules, 25(7): 1551. DOI: https://doi.org/10.3390/molecules25071551
Qiu, W., Ren, B., Dai, H., Zhang, L., Zhang, Q., Zhou, X. & Li, Y. 2017. Clotrimazole and econazole inhibit Streptococcus mutans biofilm and virulence in vitro. Archives of Oral Biology, 73: 113–120. DOI: https://doi.org/10.1016/j.archoralbio.2016.10.011
Quilès, F., Accoceberry, I., Couzigou, C., Francius, G., Noël, T. & El-Kirat-Chatel, S. 2017. AFM combined to ATR-FTIR reveals Candida cell wall changes under caspofungin treatment. Nanoscale, 9(36): 13731–13738. DOI: https://doi.org/10.1039/C7NR02170D
Ramage, G., Martinez, J.P. & Lopez-ribot, J.L. 2006. Candida biofilm on implanted biomaterials: a clinically significant problem. FEMS Yeast Research, 6(7): 979–986. DOI: https://doi.org/10.1111/j.1567-1364.2006.00117.x
Ryder, N.S., Frank, I. & Dupont, M. 1986. Ergosterol biosynthesis inhibition by the thiocarbamate antifungal agents tolnaftate and tolciclate. Antimicrobial Agents and Chemotheraphy, 29(5): 858–860. DOI: https://doi.org/10.1128/AAC.29.5.858
Sandt, C., Sockalingum, G.D., Aubert, D., Lepan, H., Lepouse, C., Jaussaud, M. & Toubas, D. 2003. Use of fourier-transform infrared spectroscopy for typing of Candida albicans strains isolated in intensive care units. Journal of Clinical Microbiology, 41(3): 954–959. DOI: https://doi.org/10.1128/JCM.41.3.954-959.2003
Shapaval, V., Brandenburg, J., Blomqvist, J., Tafintseva, V. & Passoth, V. 2019. Biotechnology for biofuels biochemical profiling , prediction of total lipid content and fatty acid profile in oleaginous yeasts by FTIR spectroscopy. Biotechnology for Biofuels, 12(1): 1–12. DOI: https://doi.org/10.1186/s13068-019-1481-0
Shi, Q., Câmara, C.R.S. & Schlegel, V. 2018. Biochemical alterations of Candida albicans during the phenotypic transition from yeast to hyphae captured by Fourier transform mid-infrared- attenuated reflectance spectroscopy. The Analyst, 143: 5404–5416. DOI: https://doi.org/10.1039/C8AN01452C
Silva, S., Rodrigues, C.F., Ara, D., Rodrigues, M.E. & Henriques, M. 2017. Candida species biofilms’ antifungal resistance. Journal of Fungi, 3(1): 8. DOI: https://doi.org/10.3390/jof3010008
Suci, P.A., Mittelman, M.W., Yu, F.P. & Geesey G.G. 1994. Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother, 38: 2125–2133. DOI: https://doi.org/10.1128/AAC.38.9.2125
Sockalingum, G.D., Sandt, C., Toubas, D., Gomez, J., Pina, P., Beguinot, I. & Manfait, M. 2002. FTIR characterization of Candida species: A study on some reference strains and pathogenic C. albicans isolates from HIV+patients. Vibrational Spectroscopy, 28(1): 137–146. DOI: https://doi.org/10.1016/S0924-2031(01)00152-7
Taha, M., Hassan, M., Essa, S. & Tartor, Y. 2013. Use of Fourier transform infrared spectroscopy (FTIR) spectroscopy for rapid and accurate identification of yeasts isolated from human and animals. International Journal of Veterinary Science and Medicine, 1(1): 15–20. DOI: https://doi.org/10.1016/j.ijvsm.2013.03.001
Vandenbosch, D., Braeckmans, K., Nelis, H.J. & Coenye, T. 2010. Fungicidal activity of miconazole against Candida spp. biofilms. Journal of Antimicrobial Chemotheraphy, 65(4): 694–700. DOI: https://doi.org/10.1093/jac/dkq019
Villa, F., Secundo, F., Forlani, F. et al. 2010. Biochemical and molecular changes of the zosteric acid-treated Escherichia coli biofilm on a mineral surface. Annals of Microbiology, 71(3). DOI: https://doi.org/10.1186/s13213-020-01617-1
Waghule, T., Sankar, S., Rapalli, V.K., Gorantla, S., Dubey, S.K., Chellappan, D.K. & Singhvi, G. 2020. Emerging role of nanocarriers based topical delivery of anti-fungal agents in combating growing fungal infections. Dermatologic Therapy, 33(6): 1–34. DOI: https://doi.org/10.1111/dth.13905
Yaacob M.F., Murata, A., Nor, N.H.M., Jesse, F.F.A & Yahya, M.F.Z.R. 2021. Biochemical composition, morphology and antimicrobial susceptibility pattern of Corynebacterium pseudotuberculosis biofilm. Journal of King Saudi University – Science, 33: 101225. DOI: https://doi.org/10.1016/j.jksus.2020.10.022
Yahya, M.F.Z.R., Hamid, U.M.A., Norfatimah, M.Y. & Kambol, R. 2014. In silico analysis of essential tricarboxylic acid cycle enzymes from biofilm-forming bacteria. Trends in Bioinformatics, 7: 26. DOI: https://doi.org/10.3923/tb.2014.19.26
Yahya, M.F.Z., Alias, Z. & Karsani, S.A. 2018. Antibiofilm activity and mode of action of DMSO alone and its combination with afatinib against Gram-negative pathogens. Folia Microbiologica, 63: 23–30. DOI: https://doi.org/10.1007/s12223-017-0532-9
Zawawi, W.M.A.W.M., Ibrahim, M.S.A., Rahmad, N., Hamid, U.M.A. & Yahya, M.F.Z.R. 2020. Proteomic analysis of Pseudomonas aeruginosa treated with Chromolaena odorata extracts. Malaysian Journal of Microbiology, 16(2): 124-133. DOI: https://doi.org/10.21161/mjm.190512
Zhang, Li, B., Wang, Q., Wei, X., Feng, W., Chen, Y. & Huang, P. 2017. Application of Fourier transform infrared spectroscopy with chemometrics on postmortem interval estimation based on pericardial fluids. Scientific Reports, 7(1): 1–8. DOI: https://doi.org/10.1038/s41598-017-18228-7
Published
How to Cite
Issue
Section
Any reproduction of figures, tables and illustrations must obtain written permission from the Chief Editor (wicki@ukm.edu.my). No part of the journal may be reproduced without the editor’s permission