Bazı Doğal Mantar Türlerinin Antibiyofilm, Antimikrobiyal, Sitotoksik ve Antioksidan Etkilerinin Değerlendirilmesi

Year 2024, Volume: 15 Issue: 2, 60 - 69, 14.10.2024

Hakan Işık , Ceylan Özsoy , Uğur Tutar , Emine Dinçer

https://doi.org/10.30708/mantar.1469051

Abstract

Bu çalışmada Basidiomycota şubesinde yer alan bazı doğal mantar türlerinin (Armillaria mellea (Vahl) P. Kumm., Infundibulicybe geotropa (Bull.) Harmaja, Leucopaxillus gentianeus (Quél.) Kotl. ve Trametes versicolor (L.) Lloyd) etanol ekstraktları, antioksidan, antimikrobiyal, antibiyofilm ve sitotoksik aktiviteleri açısından test edildi. Mantar örnekleri Enterococcus faecalis ve Staphylococcus aureus üzerinde düşük antimikrobiyal aktivite gösterirken, test mikroorganizmaları üzerinde %24.6 ile %80.5 arasında değişen biyofilm önleyici aktivite gösterdi. Antioksidan aktivite çalışmaları sonucunda, A. mellea en yüksek DPPH radikal temizleme kapasitesine (0.105±0.001 mg/mL), T. versicolor ise en yüksek demir (III) iyonu indirgeme gücüne (40.709± 0.003 µg TE/100g) sahip mantar türü olmuştur . En yüksek polifenol içeriği T. versicolor (29,916±0,002 mg GAE/100g) örneklerinde, en düşük ise A. mellea (9,5±0,006 mg GAE/100g) örneklerinde gözlendi. Örneklerin sitotoksik etkileri MCF-7, MDA MB-231 (meme kanseri) ve L929 (fare fibroblast) hücre hatlarında MTT yöntemi kullanılarak test edildi. Sonuç olarak A. mellea ve T. versicolor örneklerinin MCF-7 hücre hattında, A. mellea'nın MDA-MB-231 hücre hattında daha etkili olduğu görüldü.

Keywords

Basidiomycota, biyoaktivite, nutrasötik gıdalar, tıbbi mantarlar

Project Number

ECZ-076

Evaluation of Antibiofilm, Antimicrobial, Cytotoxic and Antioxidant Effects of Some Wild Mushroom Species

Abstract

In this study, ethanol extracts of some wild mushroom species, in the phylum Basidiomycota, (Armillaria mellea (Vahl) P. Kumm., Infundibulicybe geotropa (Bull.) Harmaja, Leucopaxillus gentianeus (Quél.) Kotl. and Trametes versicolor (L.) Lloyd) were tested for their antioxidant, antimicrobial, antibiofilm, and cytotoxic activities. Mushroom samples showed low antimicrobial activity on Enterococcus faecalis and Staphylococcus aureus, while biofilm inhibitory activity on test microorganisms ranged from 24.6% to 80.5%. At the end of the antioxidant activity studies, A. mellea was the mushroom sample having the highest DPPH radical scavenging capacity (0.105±0.001 mg/mL) whereas T. versicolor was the one having the highest iron (III) ion reducing power (40.709±0.003 µg TE/100g). The highest polyphenol content was observed in T. versicolor (29.916±0.002 mg GAE/100g) samples, and the lowest in A. mellea (9.5±0.006 mg GAE/100g) samples. The cytotoxic effects of the samples were tested on MCF-7, MDA-MB-231 (breast cancer) and L929 (mouse fibroblast) cell lines using the MTT method. As a result, it was observed that A. mellea and T. versicolor samples were more effective on the MCF-7 cell line, and A. mellea on MDA-MB-231 cell line.

Keywords

Basidiomycota, bioactivity, nutraceutical foods, medicinal mushrooms

Project Number

ECZ-076

References

• Akagi, J., Baba, H. (2010). PSK may suppress CD57+ T cells to improve survival of advanced gastric cancer patients. International Journal of Clinical Oncology, 15, 145-152.
• Altınsoy, B., Konca, S.F., Aksu, H., Kurt, B., Allı, H. and Şakalar, Ç. (2017). Cytotoxic Activity of Two Extracts from The Mushroom Clitocybe geotropa in MDA-MB-231 Cell Line. Journal of Health Sciences, 26, 13-17.
• Altuner, E.M., Akata, I. (2010). Antimicrobial Activity of Some Macrofungi Extracts. Sakarya Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 14(1), 45-49.
• Alves, M., Ferreira, I.F.R., Dias, J., Teixeira, V., Martins, A. and Pintado, M. (2012). A review on antimicrobial activity of mushroom (basidiomycetes) extracts and isolated compounds. Planta Medica, 78, 1707-1718.
• Aytar, E.C., Akata, I. and Açık, L. (2020). Antioxidant and Antimicrobial Activities of Armillaria mellea and Macrolepiota procera Extracts. Mantar Dergisi, 11(2), 121-128.
• Balouiri, M., Sadiki, M. and Ibnsouda, S.K. (2016). Methods for in vitro evaluating antimicrobial activity: A review. Journal of Pharmaceutical Analysis, 6(2), 71-79.
• Barranco, P.G., Ocanas, L.G., Cabrera, L.V., Mario, C., Carmona, S., Ocanas, F.G., Gomez, X.S. R. and Rangel, R.L. (2010). Evaluation of antioxidant, immunomodulating, cytotoxic and antimicrobial properties of different strains of Basidiomycetes from Northeastern Mexico. Journal of Medicinal Plants Research, 4(17), 1762-1769.
• Barros, L., Ferreira, M.J., Queirós, B., Ferreira, I.C.F.R. and Baptista, P. (2007). Total phenols, ascorbic acid, β-carotene and lycopene in Portuguese wild edible mushrooms and their antioxidant activities. Food Chemistry, 103, 413-419.
• Benzie, I.F.F., Strain, J.J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": The FRAP assay. Analytical Biochemistry, 239, 70-76.
• Blois, M.S. (1958). Antioxidant determinations by the use of a stable free radical. Nature, 181, 1199-1200.
• Chang, R. (1996). Functional Properties of Edible Mushrooms. Nutrition Reviews, 54(11), 91-93.
• Chang, S.T., Miles, P.G. (1992). Mushrooms biology—a new discipline. Mycologist, 6, 64-65.
• Chen, Y.J., Chen, C.C. and Huang, H.L. (2016). Induction of Apoptosis by Armillaria mellea Constituent Armillarikin in Human Hepatocellular Carcinoma. OncoTargets and Therapy, 9, 4773-4783.
• Chauhan, P.S., Kumarasamy, M., Sosnik, A. and Danino, D. (2019). Enhanced Thermostability and Anticancer Activity in Breast Cancer Cells of Laccase Immobilized on Pluronic-stabilized Nanoparticles. ACS Applied Materials & Interfaces, 11, 39436-39448.
• Chugh, R.M., Mittal, P., MP, N., Arora, T., Bhattacharya, T., Chopra, H., Cavalu, S. and Gautam, R.K. (2022). Fungal Mushrooms: A Natural Compound With Therapeutic Applications. Frontiers Pharmacology, 13, 925387. Christensen, G.D., Simpson, W.A., Bisno, A.L., Beachey, E.H. (1982). Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infection and Immunity, 37(1), 318-326.
• Christensen, G.D., Simpson, W.A., Younger, J.J., Baddour, L.M., Barrett, F.F., Melton, D.M. and Beachey, E.H. (1985). Adherence of Coagulase-Negative Staphylococci to Plastic Tissue Culture Plates: A Quantitative Model for the Adherence of Staphylococci to Medical Devices. Journal of Clinical Microbiology, 22(6), 996-1006.
• Clericuzio, M., Mella, M., Vita-Finzi P., Zema, M. and Vidari G. (2004). Cucurbitane Triterpenoids from Leucopaxillus gentianeus. Journal of Natural Products, 67, 1823-1828.
• Cui, J., Chisti, Y. (2003). Polysaccharopeptides of Coriolus versicolor: physiological activity, uses, and production. Biotechnology Advances, 21, 109-122.
• Danışman Kalındemirtaş, F., Kari̇per, İ.A., Hepokur, C. and Erdem Kuruca, S. (2021). Selective Cytotoxicity of Paclitaxel Bonded Silver Nanoparticle on Different Cancer Cells. The Journal of Drug Delivery Science and Technology, 61, 102265.
• De Silva, D.D., Rapior, S., Sudarman, E., Stadler, M., Xu, J., Alias, S.A. and Hyde, K.D. (2013). Bioactive metabolites from macrofungi: Ethnopharmacology, biological activities and chemistry. Fungal Diversity, 62, 1-40.
• Delgado-Tiburcio, E.E., Cadena-Iñiguez, J., Santiago-Osorio, E., Ruiz-Posadas, L.d.M., CastilloJuárez, I., Aguiñiga-Sánchez, I. and Soto-Hernández, M. (2022). Pharmacokinetics and Biological Activity of Cucurbitacins. Pharmaceuticals, 15, 1325.
• Dizeci, N., Onar, O., Karaca, B., Demirtas, N., Coleri Cihan, A. and Yıldırım, Ö. (2021). Comparison of The Chemical Composition and Biological Effects of Clitocybe nebularis and Infundibulicybe geotropa. Mycologia, 113(6), 1156-1168.
• Donnelly, D.M.X., Abe, F., Coveney, D., Fukuda, N. and Prangé, T. (1985). Antibacterial sesquiterpene aryl esters from Armillaria mellea. Journal of Natural Products, 48 (1), 10-16.
• Duvnjak, D., Pantić, M., Pavlović, V., Nedović, V., Lević, S., Matijašević, D., Sknepnek, A. and Nikšić, M. (2016). Advances in batch culture fermented Coriolus versicolor medicinal mushroom for the production of antibacterial compounds. Innov. Food Sci. Emerg. Technol., 34, 1-8.
• Dündar, A., Okumuş, V., Özdemir, S., Çelik, K.S., Boğa, M. and Özçağlı, E. (2016). Determination of cytotoxic, anticholinesterase, antioxidant and antimicrobial activities of some wild mushroom species. Food Science & Technology, 2, 1178060.
• Eraslan, E.C., Çırçırlı, B., Özkan, A. and Akgül, H. (2021). Anticancer Mechanisms of Action of Macrofungus Extracts. Eurasian Journal of Medical and Biological Sciences, 1(2), 58-69.
• Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D.M., Forman D. and Bray, F. (2015). Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. International Journal of Cancer, 136(5), E359-E386.
• Giri, S., Biswas, G., Pradhan, P., Mandal, S.C. and Acharya, K. (2012). Antimicrobial Activities of Basidiocarps Of Wild Edible Mushrooms Of West Bengal, India. International Journal of PharmTech Research, 4(4), 1554-1560.
• Harris, E.D. (1992). Regulation of antioxidant enzymes. The FASEB Journal, 6, 2675-2683.
• Herawati, E., Ramadhan, R., Ariyani, F., Marjenah., Kusuma, I.W., Suwinarti, W., Mardji, D., Amirta, R. and Arung, E.T. (2021). Phytochemical screening and antioxidant activity of wild mushrooms growing in tropical regions. Biodiversitas, 22(11), 4716-4721.
• Ho, C.Y., Kim, C.F., Leung, K.N., Fung, K-P., Tse, T.F., Chan, H. and Lau, C.B.S. (2005). Differential anti- tumor activity of Coriolus versicolor (Yunzhi) extract through p53-and/or Bcl-2-dependent apoptotic pathway in human breast cancer cells. Cancer Biology & Therapy, 4(6), 638-644.
• Jordan, M. (1995). The Encyclopedia of Fungi of Britain and Europe. Frances Lincoln, 384 p., London.
• Kalu, A.U., Chinenye, O.A., Lydia, E.A. and Jude, O.U. (2022). In vitro antimicrobial activity of Armillaria mellea against pathogenic organisms. International Journal of Biotechnology and Microbiology, 4(1), 39-44.
• Kanani, S.H., Pandya, D.J. (2023). The phytochemical screening, total cucurbitacin content, and in vitro anti-breast cancer activity of Leucopaxillus gentianeus mushroom. Future Journal of Pharmaceutical Sciences, 9, 49.
• Kaplan, Ö., Gökşen Tosun, N., Özgür, A., Tayhan, S.E., Bilgin, S., Türkekul, İ. and Gökçe, İ. (2021). Microwave-assisted green synthesis of silver nanoparticles using crude extracts of Boletus edulis and Coriolus versicolor: Characterization, anticancer, antimicrobial and wound healing activities. Journal of Drug Delivery Science and Technology, 64, 102641.
• Kolaylı, S., Şahin, H., Aliyazıcıoğlu, R. and Sesli, E. (2012). Phenolic Components and Antioxidant Activity of Three Edible Wild Mushrooms From Trabzon, Turkey. Chemistry of Natural Compounds, 48(1), 137-140.
• Kosanić, M., Petrović, N. and Stanojković, T. (2020). Bioactive properties of Clitocybe geotropa and Clitocybe nebularis. Journal of Food Measurement and Characterization, 14, 1046-1053.
• Lindequist, U., Niedermeyer, T.H.J. and Jülich, W.Dieter. (2005). The Pharmacological Potential of Mushrooms. Evidence-based Complementary and Alternative Medicine, 2(3), 285-299.
• Lindequist, U., Kim, H.W., Tiralongo, E. and Van Griensven, L. (2014). Medicinal Mushrooms. Evidence-Based Complementary and Alternative Medicine, 2014, 806180.
• Lung, M.Y., Chang, Y.C. (2011). Antioxidant Properties of the Edible Basidiomycete Armillaria mellea in Submerged Cultures. International Journal of Molecular Sciences, 12, 6367-6384.
• Matijašević, D., Pantić, M., Rašković, B., Pavlović, V., Duvnjak, D., Sknepnek, A. and Nikšić, M. (2016). The Antibacterial Activity of Coriolus versicolor Methanol Extract and Its Effect on Ultrastructural Changes of Staphylococcus aureus and Salmonella enteritidis. Frontiers in Microbiology, 7, 1226.
• Moser, M. (1983). Keys to Agarics and Boleti. Gustav Fischer Verlag, 535 p., Stuttgart.
• Muszyńska, B., Sułkowska-Ziaja, K., Wołkowska, M. and Ekiert, H. (2011). Chemical, Pharmacological, and Biological Characterization of the Culinary-Medicinal Honey Mushroom, Armillaria mellea (Vahl) P. Kumm. (Agaricomycetideae): A Review. International Journal of Medicinal Mushrooms, 13(2), 167-175.
• Nurgali, K., Jagoe, T.R. and Abalo, R. (2018). Editorial: Adverse Effects of Cancer Chemotherapy: Anything New to Improve Tolerance and Reduce Sequelae? Front Pharmacology, 9, 245.
• Phillips, R. (1981). Mushrooms and Other Fungi of Great Britain & Europe. Pan Books Ltd., 288p., London.
• Pišlar, A., Sabotič, J., Šlenc, J., Brzin, J. and Kos, J. (2016). Cytotoxic L-amino-acid oxidases from Amanita phalloides and Clitocybe geotropa induce caspase-dependent apoptosis. Cell Death Discovery, 2, 16021.
• Popescu, M.L., Costea, T., Nencu, I., Dutu, L.E. and Gîrd, C.E. (2016). Polyphenols Contents and Antioxidant Activity of Some Romanian Wild Mushrooms. Farmacia, 64(2), 231-236.
• Poyraz, B., Güneş, H., Tül, B. and Baş Sermenli, H. (2015). Antibacterial and Antitumor Activity of Crude Methanolic Extracts from Various Macrofungi Species. Research Journal of Biological Sciences, 8(1), 05-10.
• Redfern, J., Kinninmonth, M., Burdass, D. and Verran, J. (2014). Using Soxhlet Ethanol Extraction to Produce and Test Plant Material (Essential Oils) for Their Antimicrobial Properties. Journal of Microbiology & Biology Education, 15(1), 45-46.
• Obuchi, T., Kondoh, H., Watanabe N., Tamai M., Imura S., Jun-Shan Y. and Xiao-Tian L. (1990). Armillaric Acid, A New Antibiotic Produced by Armillaria mellea. Planta Medica, 56(2), 198-20.
• Özgör, E., Ulusoy, M., Çelebier, İ., Yıldız, S.S. and Keskin, N. (2016). Investigation of Antimicrobial Activity of Different Trametes versicolor Extracts on Some Clinical Isolates. Hacettepe J. Biol. & Chem., 43(3), 267-272.
• Sesli, E., Asan, A., Selçuk, F. (edlr). Abacı Günyar, Ö., Akata, I., Akgül, H., Aktaş, S., Alkan, S., Allı, H., Aydoğdu, H., Berikten, D., Demirel, K., Demirel, R., Doğan, H.H., Erdoğdu, M., Ergül, C.C., Eroğlu, G., Giray, G., Halikî Uztan, A., Kabaktepe, Ş., Kadaifçiler, D., Kalyoncu, F., Karaltı, İ., Kaşık, G., Kaya, A., Keleş, A., Kırbağ, S., Kıvanç, M., Ocak, İ., Ökten, S., Özkale, E, Öztürk, C., Sevindik, M., Şen, B., Şen, İ., Türkekul, İ., Ulukapı, M., Uzun, Ya., Uzun, Yu. and Yoltaş, A. (2020). Türkiye Mantarları Listesi (The Checklist of Fungi of Turkey). Ali Nihat Gökyiğit Vakfı Yayını, İstanbul.
• Sevindik, M., Akgul, H., Selamoglu, Z. and Braidy, N. (2020). Antioxidant and Antigenotoxic Potential of Infundibulicybe geotropa Mushroom Collected from Northwestern Turkey. Oxidative Medicine and Cellular Longevity, 2020, 5620484.
• Sevindik, M. (2021). Anticancer, antimicrobial, antioxidant and DNA protective potential of mushroom Leucopaxillus gentianeus (Quél.) Kotl. Indian Journal of Experimental Biology, 59, 310-315.
• Shawkey, A.M., Rabeh, M.A., Abdulall, A.K. and Abdellatif, A.O. (2013). Green nanotechnology: Anticancer activity of silver nanoparticles using Citrullus colocynthis aqueous extracts. Advances in Life Science and Technology, 13, 60-70.
• Singleton, V., Rossi, J.A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16(3): 144-158.
• Sterniša, M., Sabotič, J. and Klančnik, A. (2022). A novel approach using growth curve analysis to distinguish between antimicrobial and anti-biofilm activities against Salmonella. International Journal of Food Microbiology, 364, 109520.
• Sun, X., Sun, Y., Zhang, Q., Zhang, H., Yang, B., Wang, Z., Zhu, W., Li, B., Wang, Q. and Kuang, H. (2014). Screening and comparison of antioxidant activities of polysaccharides from Coriolus versicolor. International Journal of Biological Macromolecules, 69, 12-19.
• Tel, G., Deveci, E., Küçükaydın, S., Özler, M.A., Duru, M.E. and Harmandar, M. (2013). Evaluation of Antioxidant Activity of Armillaria tabescens, Leucopaxillus gentianeus and Suillus granulatus: The mushroom Species from Anatolia. Eurasian Journal of Analytical Chemistry, 8(3), 36-147.
• Waktola, G., Temesgen, T. (2018). Application of Mushroom as Food and Medicine. Adv Biotech & Micro., 11(3), 555817.
• Wang, Y., Xu, B. (2014). Distribution of Antioxidant Activities and Total Phenolic Contents in Acetone, Ethanol, Water and Hot Water Extracts from 20 Edible Mushrooms via Sequential Extraction. Austin Journal of Nutrition and Food Sciences, 2(1), 1009.
• Wardani, Y.K., Kristiani, E.B.E. and Sucahyo, S. (2020). Correlation between antioxidant activity and phenolic compound content and plant growth locations of Celosia argentea Linn. Bioma: Berkala Ilmiah Biologi, 22(2), 136-142.
• Wasser, S.P. (2010). Medical Mushrooms Science: History, Current Status, Future Trends, and Unsolved Problems. International Journal of Medicinal Mushrooms, 12, 1-16.
• Wu, J., Zhou, J., Lang, Y., Yao, L., Xu, H., Shi, H. and Xu, S. (2012). A polysaccharide from Armillaria mellea exhibits strong in vitro anticancer activity via apoptosis-involved mechanisms. International Journal of Biological Macromolecules, 51(4), 663-667.
• Yamaç, M., Bilgili, F. (2006). Antimicrobial Activities of Fruit Bodies and/or Mycelial Cultures of Some Mushroom Isolates. Pharmaceutical Biology, 44(9), 660-667.