Antifungal potential of extracts of the microalgae Pyramimonas virginica against dermatophyte fungi
DOI:
https://doi.org/10.33448/rsd-v13i3.45297Keywords:
Microalgae; Chlorophycea; Herbal medicine; Dermatophytosis.Abstract
The aim of this study was to evaluate the antifungal potential of the extracts centrifuged and electroflocculated of the microalgae Pyramimonas virginica against dermatophyte fungi. To obtain the microalgal biomass, the culture was carried out in a 10 L tubular photobioreactor, in triplicates. The harvesting of microalgal biomass was performed by two methods, centrifugation and electroflocculation. For the extraction of microalgal biomass, the absolute ethanol (99.9%) solvent was used. The antifungal activity of the extracts was evaluated by broth microdilution method, in the concentration range of 0.0115 to 6 mg mL-1. The Minimum Inhibitory Concentration (MIC) was determined visually, by the absence of fungal growth. Extracts were tested against the dermatophytes Nannizzia gypsea, Trichophyton mentagrophytes and Trichophyton tonsurans. Both centrifuged and electroflocculated extracts were able to inhibit the growth of all dermatophytes evaluated, and the centrifuged extract was more active than the electroflocculated. The extracts showed lower MIC values against T. tonsurans (MIC: 0.75 mg mL-1) and N. gypsea (MIC: 0.75 mg mL-1), followed by T. mentagrophytes (MIC: 6 mg mL-1). Regarding the type of activity recorded, against the fungus T. mentagrophytes it was of the fungiostatic type and for the fungi T. tonsurans and N. gypsea it was of the fungicide type. This was a pioneering study on the antifungal activity of the microalgae P. virginica, as well as the method of fractionation of its biomass. The microalgae demonstrated antifungal potential against the dermatophyte fungi evaluated, showing to be promising in the development of new herbal medicines and treatments.
References
Abo-Elyazeed, H.; Soliman, R.; Hassan, H.; El-Seedy, F. R.; & Aboul-Ella, H. (2023). Development, preparation, and evaluation of a novel non-adjuvanted polyvalent dermatophytes vaccine. Scientific Reports, 157(13). https://doi.org/10.1038/s41598-022-26567-3
Al-Khafaji, Z. H. A. (2023). The antagonistic effect of Anabaena circinalis on some dermatophyte. Biomedicine, 43(4), 1261-1265. https://doi.org/10.51248/.v43i4.302
Andrade, B. B.; Lima, S. T. C.; Rodrigues, E. D.; Druzian, J. I.; Cardoso, L. G. Reator de eletrofloculação para separação das microalgas Phaeodactylum tricornutum e Isochrysis galbana com alta atividade antioxidante e sem toxicidade. Instituto Nacional da Propriedade Intelectual - INPI, N° BR202020019742-3, 28 de set de 2020.
Barkia, I.; Saari, N.; & Manning, S. R. (2019). Microalgae for High-Value Products Towards Human Health and Nutrition. Marine Drugs, 17(5). Doi: https://doi.org/10.3390/md17050304
Bona, E. A. M.; Pinto, F. G. S.; Fruet, T. K.; Jorge, T. C. M.; & Moura, A. C. (2014). Comparação de métodos para avaliação da atividade antimicrobiana e determinação da concentração inibitória mínima (CIM) de extratos vegetais aquosos e etanólicos. Arquivos do Instituto Biológico, 81(3), 218-225. https://doi.org/10.1590/1808-1657001192012
Campos, V. B.; Barbarino, E.; & Lourenço, S. O. (2010). Crescimento e composição química de dez espécies de microalgas marinhas em cultivos estanques. Ciência Rural, 40, 339-347.
Chu, C. Y.; Liao, W. R.; Huang, R.; & Lin, L. P. (2004). Haemagglutinating and antibiotic activities of freshwater microalgae. World Journal of Microbiology and Biotechnology, 20, 817-825. https://doi.org/10.1007/s11274-004-8712-6
Curatolo, R.; Juricevic, N.; Leong, C.; & Bosshard, P. P. (2020). Antifungal susceptibility testing of dermatophytes: Development and evaluation of an optimised broth microdilution method. Mycoses, 64, 282-291. https://doi.org/10.1111/myc.13202
Falaise, C.; François, C.; Travers, M. A.; Morga, B.; Haure, J.; Tremblay, R.; Turcotte, F.; Pasetto, P.; Gastineau, R.; Hardivillier, Y.; Leignel, V.; & Mouget, J. L. (2016). Antimicrobial compounds from eukaryotic microalgae against human pathogens and diseases in aquaculture. Marine drugs, 14(9). https://doi.org/10.3390/md14090159
Fernandes M. S. M.; França K. B.; Alves R. V.; Pearson H. W.; Lima S. A.; & Costa T. S. (2017). Microalgae growth rate Scenedesmus sp. in different NaCl concentration. Engevista, 19(1), 185-193.
Gharbi, K.; Fathalli, A.; Essid, R.; Fassatoui, C.; Romdhane, M. S.; Limam, F.; & Jenhani, A. B. R. (2021). Tunisian inland water microflora as a source of phycobiliproteins and biological activity with beneficial effects on human health. Oceanological and Hydrobiological Studies, 50(4), 385-397. https://doi.org/10.2478/oandhs-2021-0033
Guedes, E. A. C.; Araújo, M. A. S.; Souza, A. K. P.; de Souza, L. I. O.; de Barros, L. D.; Maranhao, F. C. A.; & Sant’Ana, A. E. G. (2012). Antifungal activities of different extracts of marine macroalgae against dermatophytes and Candida species. Mycopathologia, 174, 223-232. https://doi.org/10.1007/s11046-012-9541-z.
Guleria, S.; Chawla, P.; Relhan, A.; Kumar, A.; Bhasin, A.; & Zhou, J. L. (2024). Antibacterial and photocatalytic potential of bioactive compounds extracted from freshwater microalgae species (Spirogyra and Ocillatoria): A comparative analysis. Science of The Total Environment, 912(20). https://doi.org/10.1016/j.scitotenv.2023.169224
Hoog, G. S.; Dukik, K.; Monod, M.; Packeu, A.; Stubbe, D.; Hendrickx, M.; Kupsch, C.; Stielow, B.; Freeke, J.; Goker, M.; Rezaei-Matehkolaei, A.; Mirhendi, H.; & Graser, Y. (2017). Toward a Novel Multilocus Phylogenetic Taxonomy for the Dermatophytes. Mycopathologia, 182, 5-31. https://doi.org/10.1007/s11046-016-0073-9
Hori, T.; Moestrup, O.; & Hoffman, L. R. (1995). Fine structural studies on an ultraplanktonic species of Pyramimonas, P. virginica (Prasinophyceae), with a discussion of subgenera within the genus Pyramimonas. European Journal of Phycology, 30(3), 219-234. https://doi.org/10.1080/09670269500651001
Hotos, G. N.; Avramidou, D.; & Bekiari, V. (2020). Calibration Curves of Culture Density Assessed by Spectrophotometer for Three Microalgae (Nephroselmis sp., Amphidinium carterae and Phormidium sp.). European Journal of Biology & Biotechnology, 6(1). https://doi.org/10.24018/ejbio.2020.1.6.132
Ibrahim, T.N.B.T.; Feisal, N.A.S.; Kamaludin, N.H.; Cheah, W.Y.; How, V.; Bhatnagar, A.; Ma, Z.; & Show, P.L. (2023). Biological active metabolites from microalgae for healthcare and pharmaceutical industries: A comprehensive review. Bioresource Technology, 372, 128661. https://doi.org/10.1016/j.biortech.2023.128661
Khurana, A.; Sardana, K.; & Chowdhary, A. (2019). Antifungal resistance in dermatophytes: Recent trends and therapeutic implications. Fungal Genetics and Biology, 132, 1087-1845. https://doi.org/10.1016/j.fgb.2019.103255
Krishnamoorthy, N.; Unpaprom, Y.; Ramaraj, R.; Maniam, G. P.; Govindan, N.; Arunachalam, T.; & Paramasivan, B. (2021). Recent advances and future prospects of electrochemical processes for microalgae harvesting. Journal of Environmental Chemical Engineering, 9(5), 105875. https://doi.org/10.1016/j.jece.2021.105875
Lage, V. M. G. B.; Deegan, K. R.; Santos, G. F.; & Lima, S. T. C. (2022). Atividade biológica das microalgas em dermatófitos: Revisão. Research, Society and Development, 11(11), e126111133404-e126111133404. https://doi.org/10.33448/rsd-v11i11.33404
Lage, V. M. G. B.; Deegan, K. R.; Santos, G. F.; Fernandez, L. G.; Barbosa, C. J.; & Lima, S. T. C. (2023). Antifungal activity of eukaryotic microalgae extracts in dermatophytes. Revista de Ciências Médicas e Biológicas, 22(4), 615-622. https://doi.org/10.9771/cmbio.v22i4.52706
Lee, A. K.; Lewis, D. M.; & Ashman, P. J. (2013). Harvesting of marine microalgae by electroflocculation: The energetics, plant design, and economics. Applied Energy,108, 45-53. https://doi.org/10.1016/j.apenergy.2013.03.003
Lourenço, S. O. (2016). Cultivo de Microalgas Marinhas: Princípios e Aplicações. Editora Rima, 1 ed.
Magagnin, C. M.; Stopiglia, C. D. O.; Vieira, F. J.; Heidrich, D.; Machado, M.; Vetoratto, G.; Lamb, F. M.; & Scroferneker, M. L. (2011). Perfil de suscetibilidade a antifúngicos de dermatófitos isolados de pacientes com insuficiência renal crônica. Anais Brasileiros De Dermatologia, 86(4), 694-701. https://doi.org/10.1590/S0365-05962011000400011
Majekodunmi, S. O. (2015). A Review on Centrifugation in the Pharmaceutical Industry. American Journal of Biomedical Engineering, 5(2), 67-78. https://doi.org/10.5923/j.ajbe.20150502.03
Moskaluk, A. E.; & VandeWoude, S. (2022). Current Topics in Dermatophyte Classification and Clinical Diagnosis. Pathogens, 11(9). https://doi.org/10.3390/pathogens11090957
Najjar, Y. S. H.; & Abu-Shamleh, A. (2020). Harvesting of microalgae by centrifugation for biodiesel production: A review. Algal Research, 51, 102046. https://doi.org/10.1016/j.algal.2020.102046
NCCLS - Clinical and Laboratory Standards Institute. (2008). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi: Approved Standard-Second Edition (M38-A2). https://clsi.org/media/1455/m38a2_sample.pdf
Park, Y. H.; Han, S.; Oh, B.; Kim, H. S.; Jeon, M. S.; Kim, S.; & Choi, Y-E. (2022). Microalgal secondary metabolite productions as a component of biorefinery: A review. Bioresource Technology, 344, 26206.
Pereira, M. S. V.; Ribeiro, A. D.; Júnior, E. C. F.; Freire, J. C. P.; Costa, M. M. A.; & Pereira, J. V. (2022). Estudo sobre métodos utilizados para a determinação da atividade antimicrobiana de extratos de plantas medicinais: elucidações e limitações das técnicas. Brazilian Journal of Development, 8(4), 26085-26104. https://doi.org/10.34117/bjdv8n4-222
Ramos, L. C.; Batista, R.; Carneiro, D. C.; Sousa, L. J.; Sales, A. N.; & Lima, S. T. C. (2020). Evaluation of electroflocculation harvesting on the antioxidant activity and toxicity of extracts from the microalgae Isochrysis galbana and Phaeodactylum tricornutum. Journal of Applied Phycology, 32, 3853–3859. https://doi.org/10.1007/s10811-020-02265-3
Sacheli, R.; & Hayette, M. P. (2021). Antifungal Resistance in Dermatophytes: Genetic Considerations, Clinical Presentations and Alternative Therapies. Journal of Fungi, 7(11). https://doi.org/10.3390/jof7110983
Sathasivam, R.; Radhakrishnan, R.; Hashem, A.; & Allah, E. F. A. (2019). Microalgae metabolites: A rich source for food and medicine. Saudi Journal of Biological Sciences, 26(4), 709-722. https://doi.org/10.1016/j.sjbs.2017.11003
Singh, G.; & Patidar, S. K. (2018). Microalgae harvesting techniques: A review. Journal of Environmental Management, 217(1), 499-508. https://doi.org/10.1016/j.jenvman.2018.04.010
Suda, S.; Bhuiyan, M. A. H.; & Faria, D. G. (2013). Genetic diversity of Pyramimonas from Ryukyu Archipelago, Japan (Chlorophyceae, Pyramimonadales). Journal of Marine Science and Technology, 21(7). https://doi.org/10.6119/JMST-013-1220-16
Turkmen, A.; & Akyurt, I. (2021). Antiviral Effects of Microalgae. Turkish Journal of Agriculture - Food Science and Technology, 9(2), 412-419. https://doi.org/10.24925/turjaf.v9i2.412-419.4138
Zhang, M.; Gu, L.; Zheng, P.; Chen, Z.; Dou, X.; Quin, Q.; & Cai, X. (2020). Improvement of cell counting method for Neubauer counting chamber. Journal of Clinical Laboratory Analysis, 34(1). https://doi.org/10.1002/jcla.23024
Zhou, L.; Li, K.; Duan, X.; Hill, D.; Barrow, C.; Dunshea, F.; Martin, G.; & Suleria, H. (2022). Bioactive compounds in microalgae and their potential health benefits. Food Bioscience, 49. https://doi.org/10.1016/j.fbio.2022.101932
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Copyright (c) 2024 Gabriela Fontes Santos; Vivian Marina Gomes Barbosa Lage; Bianca Bomfim Andrade; Kathleen Ramos Deegan; Cristiane de Jesus Barbosa; Suzana Telles da Cunha Lima
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