Abstract
Due to climate change and economic difficulties, food production and supply in the world is getting harder and harder. The importance of edible mushrooms is increasing day by day due to their consumption as food, nutritional value and health benefits. Many types of mushrooms are cultivated to overcome the difficulties of obtaining them naturally. Among the mushrooms cultivated in the world, the Pleurotus species ranks second after Agaricus spp. The aim of the current research was to determine the antimicrobial, antioxidant, cytotoxic and deoxyribonucleic acid protective effects of Pleurotus pulmonarius (Fr.) Quel. grown on some local cellulosic wastes. The antimicrobial activity and the minimum inhibitory concentration (MIC) tests carried out by the disk diffusion method and macro-broth dilution techniques. Antioxidant activity was ascertained by the radical scavenging capacity method of 2.2-diphenyl-1-picrylhydrazil. Total antioxidant status and total oxidant status of P. pulmonarius extracts were determined with rel assay kits. The DNA protective effect was evaluated using plasmid pBR322 DNA treated with ultraviolet (UV) and H2O2, and also the cytotoxic effects on the human lung cancer cell (A549) and human breast cancer cell (MDA-MB-231) lines were evaluated using the 3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay method. It was observed to be highly active against all pathogen bacteria (except S. mutans) and dermatophytes (Epidermophyton sp. and Trichophyton sp.) (14.0–29.3 mm) compared to the control group (10.0–32.7 mm), but low against Candida tropicalis. It also showed significant antioxidant potential, the highest TAS (1.33 mmol/L) and TOS (6.74 µmol/L) values were obtained in the mixture of Medicago sativa + Populus nigra (MS-PS (1:1)), on Medicago sativa (MS) medium, and also DPPH radical scavenging effect was more effective at 25 mg (68.09%) on MS-PS (1:1) medium. The methanol extract of P. pulmonarius cultured on MS-PS (1:1) at a concentration of 400 μg/ml significantly reduced the percent viability in MDA-MB-231 cell lines (1.41%). However, it was determined that P. pulmonarius did not have a DNA protective effect. As a result, it was observed that P. pulmonarius had strong antimicrobial, antioxidant and cytotoxic activities, but did not have a DNA protective effect.
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References
Menaga, D.; Rahman, P.K.; Rajakumar, S.; Ayyasamy, P.M.: Antioxidant and cytotoxic activities of a novel isomeric molecule (PF5) obtained from methanolic extract of Pleurotus florida mushroom. J. Bioresour. Bioprod. 6, 338–349 (2021)
Smolskaitė, L.; Venskutonis, P.R.; Talou, T.: Comprehensive evaluation of antioxidant and antimicrobial properties of different mushroom species. LWT 60, 462–471 (2015)
Mariga, A.M.; Pei, F.; Yang, W.J.; Zhao, L.Y.; Shao, Y.N.; Mugambi, D.K.; Hu, Q.H.: Immunopotentiation of Pleurotus eryngii (DC. ex Fr.) Quel. J. Ethnopharmacol. 153, 604–614 (2014)
Rexhepi, B.; Reka, A.: Ethnomycological knowledge of some wild medicinal and food mushrooms from Osogovo Mountains (North Macedonia). J. Nat. Sci. Math. 5(9–10), 10–19 (2020)
Calabretti, A.; Mang, S.M.; Becce, A.; Castronuovo, D.; Cardone, L.; Candido, V.; Camele, I.: Comparison of bioactive substances content between commercial and wild-type isolates of Pleurotus eryngii. Sustainability 13, 3777 (2021)
Karaman, M.; Čapelja, E.; Rašeta, M.; Rakić, M.: Diversity, chemistry, and environmental contamination of wild growing medicinal mushroom species as sources of biologically active substances (Antioxidants, Anti-Diabetics, and AChE Inhibitors). In: Arya, A.; Rusevska, K. (Eds.) Biology, Cultivation and Applications of Mushrooms, pp. 203–257. Springer, Singapore (2022)
Melanouri, E.; Dedousi, M.; Diamantopoulou, P.: Cultivating Pleurotus ostreatus and Pleurotus eryngii mushroom strains on agro-industrial residues in solid-state fermentation. Part II: effect on productivity and quality of carposomes. Carbon Resour. Convers. 5(1), 52–60 (2022)
Bellettini, M.B.; Fiorda, F.A.; Maieves, H.A.; Teixeira, G.L.; Ávila, S.; Hornung, P.S.; Ribani, R.H.: Factors affecting mushroom Pleurotus spp. Saudi J. Biol. Sci. 26, 633–646 (2019)
Caldas, L.A.; Zied, D.C.; Sartorelli, P.: Dereplication of extracts from nutraceutical mushrooms Pleurotus using molecular network approach. Food Chem. 370, 131019 (2022)
Mattila, P.; Konko, K.; Eurola, M.; Pihlava, J.; Astola, J.; Vahteristo, L.; Hietaniemi, V.; Kumpulainen, J.; Valtonen, M.; Piironen, V.: Contents of vitamins, mineral elements, and some phenolic compounds in cultivated mushrooms. J. Agric. Food Chem. 49, 2343–2348 (2001)
Wang, H.; Ng, T.B.: Eryngin, a novel antifungal peptide from fruiting bodies of the edible mushroom Pleurotus eryngii. Peptides 25(1), 1–5 (2004)
Valverde, M.E.; Hernández-Pérez, T.; Paredes-López, O.: Edible mushrooms: improving human health and promoting quality life. Int. J. Microbiol. 376387, 1–14 (2015)
Sharma, A.; Sharma, A.; Tripathi, A.: Biological activities of Pleurotus spp. polysaccharides: a review. J. Food Biochem. 45(6), e13748 (2021)
Torres-Martínez, B.M.; Vargas-Sánchez, R.D.; Torrescano-Urrutia, G.R.; Esqueda, M.; Rodríguez-Carpena, J.G.; Fernández-López, J.; Perez-Alvarez, J.A.; Sánchez-Escalante, A.: Pleurotus genus as a potential ingredient for meat products. Foods 11(6), 779 (2022)
López-Hortas, L.; Flórez-Fernández, N.; Torres, M.D.; Domínguez, H.: Update on potential of edible mushrooms: high-value compounds, extraction strategies and bioactive properties. Int. J. Food Sci. Tech. 57(3), 1378–1385 (2022)
Kehrer, J.P.; Klotz, L.O.: Free radicals and related reactive species as mediators of tissue injury and disease: implications for Health. Crit. Rev. Toxicol. 45, 765–798 (2015)
Widel, M.; Krzywon, A.; Gajda, K.; Skonieczna, M.; Rzeszowska-Wolny, J.: Induction of bystander effects by UVA, UVB, and UVC radiation in human fibroblasts and the implication of reactive oxygen species. Free Radic. Biol. Med. 68, 278–287 (2014)
Jayakumar, T.; Thomas, P.A.; Sheu, J.R.; Geraldine, P.: In-vitro and in-vivo antioxidant effects of the oyster mushroom Pleurotus ostreatus. Food Res. Int. 44, 851–861 (2011)
Figueiredo, L.; Régis, W.C.B.: Medicinal mushrooms in adjuvant cancer therapies: an approach to anticancer effects and presumed mechanisms of action. Nutrire 42, 1–10 (2017)
El-Deeb, N.M.; El-Adawi, H.I.; EL-wahab, A.E.A.; Haddad, A.M.; El Enshasy, H.A.; He, Y.W.; Davis, K.R.: Modulation of NKG2D, KIR2DL and cytokine production by Pleurotus ostreatus glucan enhances natural killer cell cytotoxicity toward cancer cells. Front. Cell Dev. Biol. 7, 165 (2019)
Pandey, A.T.; Pandey, I.; Hachenberger, Y.; Krause, B.C.; Haidar, R.; Laux, P.; Singh, A.V.: Emerging paradigm against global antimicrobial resistance via bioprospecting of mushroom into novel nanotherapeutics development. Trends Food Sci. Technol. 106, 333–344 (2020)
Khan, M.A.; Tania, M.: Nutritional and medicinal importance of Pleurotus mushrooms: an overview. Food Rev. Int. 28, 313–329 (2012)
Carrasco-González, J.A.; Serna-Saldívar, S.O.; Gutiérrez-Uribe, J.A.: Nutritional composition and nutraceutical properties of the Pleurotus fruiting bodies: potential use as food ingredient. J. Food Compost. Anal. 58, 69–81 (2017)
Venturella, G.; Ferraro, V.; Cirlincione, F.; Gargano, M.L.: Medicinal mushrooms: bioactive compounds, use, and clinical trials. Int. J. Mol. Sci. 22, 634 (2021)
Koutrotsios, G.; Tagkouli, D.; Bekiaris, G.; Kaliora, A.; Tsiaka, T.; Tsiantas, K.; Chatzipavlidis, I.; Zoumpoulakis, P.; Kalogeropoulos, N.; Zervakis, G.I.: Enhancing the nutritional and functional properties of Pleurotus citrinopileatus mushrooms through the exploitation of winery and olive mill wastes. Food Chem. 370, 131022 (2022)
Dkhil, M.A.; Diab, M.S.M.; Lokman, M.S.; El-Sayed, H.; Aljawdah, H.M.A.; Al-Quraishy, S.; Bauomy, A.A.: Hepato-protective effect of Pleurotus ostreatus extracts in cadmium-intoxicated rats. J. King Saud Univ. Sci. 32, 3432–3436 (2020)
Goswami, B.; Majumdar, S.; Das, A.; Barui, A.; Bhowal, J.: Evaluation of bioactive properties of Pleurotus ostreatus mushroom protein hydrolysate of different degree of hydrolysis. LWT 149(5), 111768 (2021)
Cateni, F.; Gargano, M.L.; Procida, G.; Venturella, G.; Cirlincione, F.; Ferraro, V.: Mycochemicals in wild and cultivated mushrooms: nutrition and health. Phytochem. Rev. 21, 339–383 (2022)
Pandey, A.T.; Pandey, I.; Kerkar, P.; Singh, M.P.: Antimicrobial activity and mycochemical profile of methanol extract from Pleurotus flabellatus. Vegetos 34, 619–629 (2021)
Sánchez, C.: Bioactives from mushroom and their application. In: Puri, M. (Ed.) Food Bioactives, pp. 23–57. Springer International Publishing AG, Cham (2017)
Askarova, S.; Umbayev, B.; Masoud, A.; Kaiyrlykyzy, A.: The links between the gut microbiome, aging, modern lifestyle and Alzheimer’s disease. Front. Cell Infect. Microbiol. 10, 1–12 (2020)
Mwangi, R.W.; Macharia, J.M.; Wagara, I.N.; Bence, R.L.: The antioxidant potential of different edible and medicinal mushrooms. Biomed. Pharmacother. 147, 112621 (2022)
Croan, S.: Conversion of conifer waste into edible and medicinal mushrooms. For. Prod. J. 54(2), 68–76 (2004)
Jonathan, S.; Okorie, A.; Garuba, E.; Babayemi, O.: Bioconversion of sorghum stalk and rice straw into value added ruminant feed using Pleurotus pulmonarius. Nat. Sci. 10(4), 10–16 (2012)
Maftoun, P.; Johari, H.; Soltani, M.; Malik, R.; Othman, N.Z.; El Enshasy, H.A.: The edible mushroom Pleurotus spp.: I. Biodiversity and nutritional values. Int. J. Biotechnol. Wellness Ind. 4(2), 67–83 (2015)
Smiderle, F.; Olsen, L.; Carbonero, E.; Baggio, C.; Freitas, C.; Marcon, R.; Santos, A.; Gorin, P.; Iacomini, M.: Anti-inflammatory and analgesic properties in a rodent model of a (1→3), (1→6)-linked β-glucan isolated from Pleurotus pulmonarius. Eur. J. Pharmacol. 597(1–3), 86–91 (2008)
Lin, P.; Yan, Z.F.; Kook, M.; Li, C.T.; Yi, T.H.: Genetic and chemical diversity of edible mushroom Pleurotus species. BioMed. Res. Int. 2022, 1–13 (2022)
Akyüz, M.; Şule, İ; Kırbağ, S.: Nutrient content of Pleurotus pulmonarius (Fr.) Quel. grown on some local lignocellulosic wastes. KSU J. Agric. Nat. 25, 25–30 (2022)
Amirullah, N.A.; Abidin, N.Z.; Abdullah, N.; Manickam, S.: The ultrasound extract of Pleurotus pulmonarius (Fr.) Quél alleviates metabolic syndromes in hyperlipidaemic Wistar-Kyoto rats fed with a high-fat diet. Biocatal. Agric. Biotechnol. 34, 102019 (2021)
Dawidowicz, L.: Cultivation of oyster mushrooms (Pleurotus spp.) using organic waste: an example with Pleurotus pulmonarius (Fr.) Quel. Folia. Biol. Oecol. 17, 104–110 (2021)
Banjo, N.; Abikoye, E.; Kukoye, A.: Comparison of three nutrient supplements used as additive to sawdust during the cultivation of oyster mushroom (Pleurotus pulmonarius). Niger. J. Microbiol. 18, 335–336 (2004)
Adebayo, G.; Omolara, B.; Toyin, A.: Evaluation of yield of oyster mushroom (P. pulmonarius) grown on cotton waste and cassava peel. Afr. J. Biotechnol. 8(2), 215–218 (2009)
Akinfemi, A.; Ogunwale, O.: Chemical composition and in vitro digestibility of rice straw treated with Pleurotus ostreatus, Pleurotus pulmonarius and Pleurotus tuber-regium. Slovak J. Anim. Sci. 45(1), 14–20 (2012)
Zadrazil, F.: Cultivation of Pleurotus. In: Chang, S.T.; Hayes, W.A. (Eds.) The Biology and Cultivation of Edible Mushrooms, pp. 521–558. Academic Press, New York (1978)
Babu, D.R.; Pandey, M.; Rao, G.N.: Antioxidant and electrochemical properties of cultivated Pleurotus spp. and their sporeless/low sporing mutants. J. Food Sci. Technol. 51(11), 3317–3324 (2014)
Collins, C.M.; Lyne, P.M.: Microbiological methods. In: Collins, C.H.,; Lyne, P.M.; Grange, J.M.; Flkinham, J.O. (Eds.) Mycological Methods, p. 140, 8 ed. London (2004)
European Committee for Antimicrobial Susceptibility Testing (EUCAST): Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin. Microbiol. Infect. Dis. 9, 1–7 (2003)
Erel, O.: A novel automated direct measurement method for total antioxidant capacity using a new generation. More stable ABTS radical cation. Clin. Biochem. 37, 277–285 (2004)
Erel, O.: A new automated colorimetric method for measuring total oxidant status. Clin. Biochem. 38, 1103–1111 (2005)
Cuendet, M.; Hostettmann, K.; Potterat, O.; Dyatmiko, W.: Iridoid glucosides with free radical scavenging properties from Fagraea blumei. Helv. Chim. Acta. 80, 1144–1152 (1997)
Kirby, A.J.; Schmidt, R.J.: The antioxidant activity of Chinese herbs for eczema and of placebo herbs. J. Ethnopharmacol. 56, 103–108 (1997)
Mossman, T.: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65, 55–63 (1983)
Russo, A.; Acquaviva, R.; Campisi, A.; Sorrenti, V.; Di-Giacomo, C.; Virgata, G.: Bioflavonoids as antiradicals. Antioxidants and DNA cleavage protectors. Cell Biol. Toxicol. 16, 91–98 (2000)
Tepe, B.; Degerli, S.; Arslan, S.; Malatyali, E.; Sarikurkcu, C.: Determination of chemical profile, antioxidant, DNA damage protection and antiamobic activities of Teucrium polium and Stachy siberica. Fitoterapia 82, 237–246 (2011)
Chang, S.T.; Wasser, S.P.: The role of culinary-medicinal mushrooms on human welfare with a pyramid model for human health. Int. J. Med. Mushrooms 14, 95–134 (2012)
Patel, S.; Goyal, A.: Recent developments in mushrooms as anti-cancer therapeutics: a review. 3 Biotech. 2, 1–15 (2012)
Alves, M.; Ferreira, I.F.R.; Dias, J.; Teixeira, V.; Martins, A.; Pintado, M.: A review on antimicrobial activity of mushroom (basidiomycetes) extracts and isolated compounds. Planta Med. 78, 1707–1718 (2012)
Parihar, S.; Virani, K.D.; Pithawala, E.A.; Shukla, M.D.; Lahiri, S.K.; Jain, N.K., et al.: Phytochemical screening, total phenolic content, antibacterial and antioxidant activity of wild edible mushroom Pleurotus ostreatus. Int. Res. J. Pharm. 6, 65–69 (2015)
El-Batal, A.I.; Al-Hazmi, N.E.; Mosallam, F.M.; El-Sayyad, G.S.: Biogenic synthesis of copper nanoparticles by natural polysaccharides and Pleurotus ostreatus fermented fenugreek using gamma rays with antioxidant and antimicrobial potential towards some wound pathogens. Microb. Pathog. 118, 159–169 (2018)
Athukorala, Y.; Kim, K.N.; Jeon, Y.J.: Antiproliferative and antioxidant properties of an enzymatic hydrolysate from brown alg, Ecklonia cava. Food Chem. Toxicol. 44, 1065–1074 (2006)
Kosanić, M.; Ranković, B.; Rančić, A.; Stanojković, T.: Evaluation of metal concentration and antioxidant, antimicrobial, and anticancer potentials of two edible mushrooms Lactarius deliciosus and Macrolepiota procera. J. Food Drug. Anal. 24, 477–484 (2016)
Shimada, K.; Fujikawa, K.; Yahara, K.; Nakamura, T.: Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. J. Agric. Food Chem. 40, 945–948 (1992)
Liu, X.; Zhou, B.; Lin, R.; Jia, L.; Deng, P.; Fan, K.; Zhang, J.: Extraction and antioxidant activities of intracellular polysaccharide from Pleurotus sp. mycelium. Int. J. Biol. Macromol. 47, 116–119 (2010)
Dulay, R.M.R.; Miranda, L.A.; Malasaga, J.S.; Kalaw, S.P.; Reyes, R.G.; Hou, C.T.: Antioxidant and antibacterial activities of acetonitrile and hexane extracts of Lentinus tigrinus and Pleurotus djamour. Biocatal. Agric. Biotechnol. 9, 141–144 (2012)
Zhang, Z.; Zhang, Y.; Liu, H.; Wang, J.; Wang, D.; Deng, Z.; Zhong, S.: A water-soluble selenium-enriched polysaccharide produced by Pleurotus ostreatus: Purification, characterization, antioxidant and antitumor activities in vitro. Int. J. Biol. Macromol. 168, 356–370 (2021)
Sudha, G.; Vadivukkarasi, S.; Shree, R.B.I.; Lakshmanan, P.: Antioxidant activity of various extracts from an edible mushroom Pleurotus eous. Food Sci. Biotechnol. 21, 661–668 (2012)
Song, X.; Ren, Z.; Zhang, C.: Antioxidant, anti-inflammatory and renoprotective effects of acidic-hydrolytic polysaccharides by spent mushroom compost (Lentinula edodes) on LPS-induced kidney injury. Int. J. Biol. Macromol. 151, 1267–1276 (2019)
Kim, M.Y.; Seguin, P.; Ahn, J.K.; Kim, J.J.; Chun, S.C.; Kim, E.H.; Seo, S.H.; Kang, E.Y.; Kim, S.L.; Park, Y.J.; Ro, H.M.; Chung, I.M.: Phenolic compound concentration and antioxidant activities of edible and medicinal mushrooms from Korea. J. Agric. Food Chem. 56, 7265–7270 (2008)
Finimundy, T.C.; Gambato, G.; Fontana, R.; Camassola, M.; Salvador, M.; Moura, S.; Hess, J.; Henriques, J.A.P.; Dillon, A.J.P.; Roesch-Ely, M.: Aqueous extracts of Lentinula edodes and Pleurotus sajor-caju exhibit high antioxidant capability and promising in vitro antitumor activity. Nutr. Res. 33, 76–84 (2013)
Gąsecka, M.; Mleczek, M.; Siwulski, M.; Niedzielski, P.: Phenolic composition and antioxidant properties of Pleurotus ostreatus and Pleurotus eryngii enriched with selenium and zinc. Eur. Food Res. Technol. 242, 723–732 (2016)
Vieira, P.A.F.; Gontijo, D.C.; Vieira, B.C.; Fontes, E.A.; de Assunção, L.S.; Leite, J.P.V.; Kasuya, M.C.M.: Antioxidant activities, total phenolics and metal contents in Pleurotus ostreatus mushrooms enriched with iron, zinc or lithium. LWT 54, 421–425 (2013)
Song, F.Q.; Liu, Y.; Kong, X.S.; Chang, W.; Song, G.: Progress on understanding the anticancer mechanisms of medicinal mushroom: Inonotus obliquus. Asian Pac. J. Cancer Prev. 14, 1571–1578 (2013)
Ma, G.; Yang, W.; Fang, Y.; Ma, N.; Pei, F.; Zhao, L.; Hu, Q.: Antioxidant and cytotoxicites of Pleurotus eryngii residue polysaccharides obtained by ultrafiltration. LWT 73, 108–116 (2016)
Khan, A.A.; Gani, A.; Ahmad, M.; Masoodi, F.A.; Amin, F.; Kousar, S.: Mushroom varieties found in the Himalayan regions of India: antioxidant, antimicrobial, and antiproliferative activities. Food Sci. Biotechnol. 25, 1095–1100 (2016)
Sun, H.; Zhu, Z.; Tang, Y.; Ren, Y.; Song, Q.; Tang, Y.; Zhang, Y.: Structural characterization and antitumor activity of a novel Se-polysaccharide from seleniumenriched Cordyceps gunnii. Food Funct. 9, 2744–2754 (2018)
Maity, G.N.; Maity, P.; Choudhuri, I.; Bhattacharyya, N.; Acharya, K.; Dalai, S.; Mondal, S.: Structural studies of a water insoluble β-glucan from Pleurotus djamor and its cytotoxic effect against PA1, ovarian carcinoma cells. Carbohydr. Polym. 222, 114990 (2019)
Elhusseiny, S.M.; El-Mahdy, T.S.; Awad, M.F.; Elleboudy, N.S.; Farag, M.; Aboshanab, K.M.; Yassien, M.A.: Antiviral, cytotoxic, and antioxidant activities of three edible agaricomycetes mushrooms: Pleurotus columbinus, Pleurotus sajor-caju, and Agaricus bisporus. J. Fungi 7, 645 (2021)
Kim, K.C.; Kim, I.G.: Ganoderma lucidum extract protects DNA from strand breakage caused by hydroxyl radical and UV irradiation. Int. J. Mol. Med. 4, 273–280 (1999)
Sa-Ard, P.; Sarnthima, R.; Khammuang, S.; Kanchanarach, W.: Antioxidant, antibacterial and DNA protective activities of protein extracts from Ganoderma lucidum. J. Food Sci. Technol. 52, 2966–2973 (2015)
Akyüz, M.; Karagöz, I.D.; İnci, Ş; Kılıç, H.İ; Kırbağ, S.; Simitçioğlu, B.: Cytotoxicity and DNA protective effects of Terfazia and Picoa species from eastern region of Turkey. Istanbul J. Pharm. 51, 198–203 (2021)
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Akyüz, M., İnci, Ş. & Kırbağ, S. Evaluation of Antimicrobial, Antioxidant, Cytotoxic and DNA Protective Effects of Oyster Mushroom: Pleurotus pulmonarius (Fr.) Quel.. Arab J Sci Eng 48, 7273–7283 (2023). https://doi.org/10.1007/s13369-022-07418-9
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DOI: https://doi.org/10.1007/s13369-022-07418-9