Library Subscription: Guest
Begell Digital Portal Begell Digital Library eBooks Journals References & Proceedings Research Collections
International Journal of Medicinal Mushrooms
IF: 1.423 5-Year IF: 1.525 SJR: 0.433 SNIP: 0.661 CiteScore™: 1.38

ISSN Print: 1521-9437
ISSN Online: 1940-4344

International Journal of Medicinal Mushrooms

DOI: 10.1615/IntJMedMushrooms.2019030874
pages 571-582

Antioxidant, Anticancer, Antimicrobial, and Antibiofilm Properties of the Culinary-Medicinal Fairy Ring Mushroom, Marasmius oreades (Agaricomycetes)

Naznoosh Shomali
Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey
Okan Onar
Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey
Basar Karaca
Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey
Nergiz Demirtas
The Ministry of Food, Agriculture and Livestock, Food Control Laboratory, Food Chemical Analysis Laboratory, Ankara, Turkey
Arzu Coleri Cihan
Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey
Ilgaz Akata
Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey
Ozlem Yildirim
Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey

ABSTRACT

This study is based on the phenolic composition and the antioxidant, anticancer, antimicrobial, and antibiofilm activities of the edible mushroom Marasmius oreades from Turkey. The phenolic composition of an M. oreades ethanol extract was measured by using the Folin-Ciocalteu method, aluminium chloride colorimetry, and ultraperformance liquid chromatography. The antioxidant activity was evaluated on the basis of DPPH radical scavenging activity. The effect of the M. oreades ethanol extract was also screened in order to determine glutathione-S-transferase, glutathione peroxidase, catalase, and superoxide dismutase enzyme activities. The antimicrobial activity of the mushroom extract was evaluated by using well diffusion and was based on the minimum inhibitory concentration. In addition, the antibiofilm potential of M. oreades was analyzed against Gram-positive and -negative bacteria. Finally, the anticancer effects of the mushroom extract were tested on colon (HT-29) and breast (MCF-7 and MDA-MB-231) cancer cell lines by using the MTT assay. The results revealed that the total amount of phenolics in the ethanol extract of M. oreades was 10.990 ± 0.0007 mg gallic acid equivalent/100 g, and the total amount of flavonoids was 1.139 ± 0.0052 mg quercetin equivalent/100 g. The ultraperformance liquid chromatography results indicated that the M. oreades ethanol extract contained various phenolic compounds: catechin, ferulic, gallic acid, and vanillic acid. The M. oreades ethanol extract scavenged about 80% of DPPH free radicals. It did not show any effect on the glutathione-S-transferase, glutathione peroxidase, and catalase enzyme activities, but its maximal concentration (10 mg/mL) increased superoxide dismutase activity (8%). The ethanol extract of M. oreades showed a moderate anticancer effect on the HT-29, MCF-7, and MDA-MB-231 cell lines. Although the ethanolic extract of the mushroom did not show sufficient antibacterial activity, it presented a strong antibiofilm effect against all studied pathogenic strains at the tested concentrations.

REFERENCES

  1. Lorenzen K, Anke T. Basidiomycetes as a source for new bioactive natural products. Curr Org Chem. 1998;2:329-64.

  2. Petrova RD, Mahajna J, Reznick AZ, Wasser SP, Denchev CM, Nevo E. Fungal substances as modulators of NF-kappaB activation pathway. Mol Biol Rep. 2007;34:145-54.

  3. Ruimi N, Petrova RD, Agbaria R, Sussan S, Wasser SP, Reznick AZ, Mahajna J. Inhibition of TNFa-induced iNOS expression in HSV-tk transduced 9L glioblastoma cell lines by Marasmius oreades substances through NF-kB- and MAPK-dependent mechanisms. Mol Biol Rep. 2010;37:3801-12.

  4. Winter HC, Mostafapour K, Goldstein IJ. The mushroom Marasmius oreades lectin is a blood group type B agglutinin that recognizes the Gala 1,3Gal and Gala 1,3Galp 1,4GlcNAc porcine xenotransplantation epitopes with high affinity. J Biol Chem. 2002;277:14996-5001.

  5. Wohlschlager T, Butschi A, Zurfluh K, Vonesch SC, auf dem Keller U, Gehrig P, Bleuler-Martinez S, Hengartner MO, Aebi M, Kunzler M. Nematotoxicity of Marasmius oreades agglutinin (MOA) depends on glycolipid binding and cysteine protease activity. J Biol Chem. 2011;286:30337-43.

  6. Juillot S, Cott C, Madl J, Claudinon J, Velden NSJ, Kunzler M, Thuenauer R, Romer W. Uptake of Marasmius oreades ag-glutinin disrupts integrin-dependent cell adhesion. Biochim Biophys Acta. 2016;392-401.

  7. Onar O, Akata I, Celep GS, Yildirim O. Antioxidant activity of extracts from the red-belt conk medicinal mushroom, Fomitopsis pinicola (Agaricomycetes), and its modulatory effects on antioxidant enzymes. Int J Med Mushrooms. 2016;18(6):501-8.

  8. Slinkard K, Singleton VL. Total phenol analyses: automation and comparison with manual methods. J Enol Viticul. 1977;28:49-55.

  9. Chang CC, Yang MH, Wen HM, Chern JC. Estimation of total flavonoid content in propolis by two complementary colori- metric methods. J Food Drug Anal. 2002;10(3):178-82.

  10. Reis FS, Martins A, Barros L, Ferreira ICFR. Antioxidant properties and phenolic profile of the most widely appreciated cultivated mushrooms: a comparative study between in vivo and in vitro samples. Food Chem Toxicol. 2012;50:1201-7.

  11. Sharma OP, Bhat TK. DPPH antioxidant assay revisited. Food Chem. 2009;113:1202-5.

  12. Shomali Moghaddam N, Isgor BS, Isgor YG, Geven F, Yildirim O. The evaluation of inhibitory effects of selected plant extracts on antioxidant enzymes. Fresenius Environ Bull. 2015;24(1):63-70.

  13. Habig WH, Pabst MJ, Jakoby WB. Glutathione-S-transferases the first enzymatic step in mercapturic acid formaion. J Biol Chem. 1974;249:7130-9.

  14. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967;70:158-69.

  15. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121-6.

  16. Geller BL, Winge DR. Subcellular distribution of superoxide dismutases in rat liver. Methods Enzymol. 1984;105:105-14.

  17. Khan N, Hadi N, Afaq F, Syed DN, Kweon MH, Mukhtar H. Pomegranate fruit extract inhibits prosurvival pathways in human A549 lung carcinoma cells and tumor growth in athymic nude mice. Carcinogenesis. 2007;28:163-73.

  18. Silici S, Koc AN. Comparative study of in vitro methods to analyse the antifungal activity of propolis against yeasts isolated from patients with superficial mycoses. Lett Appl Microbiol. 2006;43:318-24.

  19. Cinical Laboratory & Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-ninth edition. CLSI document M07-A9. Wayne, PA. 2012.

  20. Bala N, Aitken EA, Fechner N, Cusack A, Steadman KJ. Evaluation of antibacterial activity of Australian basidiomycetous macrofungi using a high-throughput 96-well plate assay. Pharm Biol. 2011;49(5):492-500.

  21. Sultanbawa Y, Cusack A, Currie M, Davis C. An innovative microplate assay to facilitate the detection of antimicrobial activity in plant extracts. J Rapid Methods Autom Microbiol. 2009;17:519-34.

  22. Stepanovic S , Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods. 2000;40(2):175-9.

  23. Vestby LK, Maretra T, Balance S, Langsrud S, Nesse LL. Survival potential of wild type cellulose deficient Salmonella from the feed industry. BMC Vet Res. 2009;5:43.

  24. Stepanovic S, Cirkovic I, Ranin L, Svabic-Vlahovic M. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol. 2004;38:428-32.

  25. Pennerman KK, Yin G, Bennett JW. Health effects of small volatile compounds from East Asian medicinal mushrooms. Mycobiology. 2015;43(1):9-13.

  26. Wang XM, Zhang J, Wu LH, Zhao YL, Li T, Li JQ, Wang YZ, Liu HG. A mini-review of chemical composition and nutritional value of edible wild-grown mushroom from China. Food Chem. 2014;15(151):279-85.

  27. Falandysz J, Borovicka J. Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl Microbiol Biotechnol. 2013;97(2):477-501.

  28. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telse J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44-84.

  29. Ramesh C, Pattar MG. Antimicrobial properties, antioxidant activity and bioactive compounds from six wild edible mushrooms of western ghats of Karnataka, India. Pharmacognosy Res. 2010;2(2):107-12.

  30. Suay I, Arenal F, Asensio FJ, Basilio A, Cabello MA, Diez MT, Garda JB, del Val AG, Gorrochategui J, Hernandez P, Pelaez F, Vicente MF. Screening of basidiomycetes for antimicrobial activities. Antonie Van Leeuwenhoek. 2000;78(2):129-39.

  31. Queiros B, Barreira JC, Sarmento AC, Ferreira IC. In search of synergistic effects in antioxidant capacity of combined edible mushrooms. Int J Food Sci Nutr. 2009;60(Suppl. 6):160-72.

  32. Anke T, Kupka J, Schramm G, Steglich W. Antibiotics from basidiomycetes. X. Scorodonin, a new antibacterial and antifungal metabolite from Marasmius scorodonius (Fr.) Fr. J Antibiot (Tokyo). 1980;33(5):463-7.

  33. Davies DG, Hodge P. Biosynthesis of the allene (-)-marasin in Marasmius ramealis. Org Biomol Chem. 2005;3(9):1690-3.

  34. Tobe Y, Dai Y, Tohru T, Masashi I, Junichi S, Kiyomi K, Kazuy K, Yoshinobu O. Synthesis of (.+-.)-marasmic acid via 1-ox-aspirohexane rearrangement. J Am Chem Soc. 1990;112:775-9.

  35. Bin L, Wei L, Xiaohong C, Mei J, Mingsheng D. In vitro antibiofilm activity of the melanin from Auricularia auricula, an edible jelly mushroom. Ann Microbiol. 2012;62(4):1523-30.

  36. Alves MJ, Ferreira IC, Martins A, Pintado M. Antimicrobial activity of wild mushroom extracts against clinical isolates resistant to different antibiotics. J Appl Microbiol. 2012;113(2):466-75.

  37. Alves MJ, Ferreira IC, Lourenjo I, Costa E, Martins A, Pintado M. Wild mushroom extracts as inhibitors of bacterial biofilm formation. Pathogens. 2014;3(3):667-79.

  38. Karaca B, Akata I, Cihan AQ. Lentinus edodes, Lactarius delicious ve Ganoderma lucidum'un antibiyofilm ve antimikrobiyal etkinlikleri. Kastamonu Universitesi Orman Fakultesi Dergisi. 2017;17(4):660-8.


Articles with similar content:

Medicinal Mushroom Extracts Possess Differential Antioxidant Activity and Cytotoxicity to Cancer Cells
International Journal of Medicinal Mushrooms, Vol.17, 2015, issue 5
Eglal AbdAllah Ghonimy, Mahomud Mohammed Alassar, Fang-Sheng Wu, Eman Nasr Elbatrawy
Contents and Antioxidant Activities of Polysaccharides in 14 Wild Mushroom Species from the Forest of Northeastern China
International Journal of Medicinal Mushrooms, Vol.17, 2015, issue 12
Guiqiang Wang, Jian-Yong Wu, Lijian Xu, Qinggui Wang
Enhanced Antiproliferative Effects of Aqueous Extracts of Some Medicinal Mushrooms on Colon Cancer Cells
International Journal of Medicinal Mushrooms, Vol.15, 2013, issue 3
Shagun Arora, Jay Balani, Simran Tandon, Shristhi Goyal
Bioactive Compounds, Chemical Composition, and Medicinal Value of the Giant Puffball, Calvatia gigantea (Higher Basidiomycetes), from Turkey
International Journal of Medicinal Mushrooms, Vol.18, 2016, issue 2
Seyda Kivrak, Mansur Harmandar, Ibrahim Kivrak
Antioxidant and Antiproliferative Potential of Fruiting Bodies of the Wild-Growing King Bolete Mushroom, Boletus edulis (Agaricomycetes), from Western Serbia
International Journal of Medicinal Mushrooms, Vol.19, 2017, issue 1
Nebojsa llic, Sonja Kaisarevic, Aleksandra Novakovic, Maja Karaman, Tanja Radusin