Chemical Compositions and Antioxidant Activities of 16 Wild Edible Mushroom...

[Full title: Chemical Compositions and Antioxidant Activities of 16 Wild Edible Mushroom Species Grown in Anatolia]

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Life International Journal of Pharmacology ISSN 1811-7775 Life science alert ansinet Asian Network for Scientific Information

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International Journal of Pharmacology 8 (2): 134-138. 2012 ISSN 1811-7775 DOI: 10.3923/ijp.2012.131.138 2012 Asian Network for Scientific Information Chemical Compositions and Antioxidant Activities of 16 Wild Edible Mushroom Species Grown in Anatolia 'Ilgaz Akata, Bülent Ergönül and Fatih Kalyoncu 'Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey Department of Food Engineering, Faculty of Engineering, Celal Bayar University, Manisa, Turkey Department of Biology, Faculty of Science and Letters, Celal Bayar University, Muradiya Campus, Manisa, Turkey Abstract: In this study, chemical compositions and antioxidant activities of 16 wild edible mushrooms (Agrocybe cylindracea, Amanita ceciliae, Armillaria mellea, Boletus reticulatus, Cantharellus cibarius, Chlorophyllum rhacodes, Coprinus comatus, Flammulina velutipes var. velutipes, Lactarius deliciosus, Lactarius salmonicolor, Pleurotus ostreatus, Polyporus squamosus, Rhizopogon roseolus, Russula anthracina, Suillus collinitus and Tricholoma myomyces) were investigated. Antioxidant properties of methanol extracts were studied by the 1,1-diphenyl-2-picrylhydrazyl (DPPII) free radical scavenging method. Among the mushroom extract Amanita ceciliae and Fleurotus ostreatus (96.16 %) showed the most potent radical scavenging activities at 1.51 and 2.72 mg mL, respectively. The lowest scavenging activity was exhibited by C. rhacodes (70.16%) at 2.35 mg mL. Key words: Antioxidant activity, chemical content, edible wild mushroom, Anatolia INTRODUCTION The members of fungal kingdom are present almost everywhere. They are important for continuation of life because they are able to biodegrade the substrate (Manzi et al., 2001). Mushrooms have been used as food and food-flavoring material for centuries (Tsai et al., 2007; Shin et al., 2007). Mushrooms are widely distributed all over the world and some of them have been used as drug in ethno-medicine. Many edible mushrooms are reputed to possess due to properties of antioxidant, antimicrobial and anticancer (Tambekar et al., 2006; Aryantha et al., 2010). Oxidation is essential to aerobic organisms for the production of energy to fuel biological processes. However, the oxygen-derived free radicals is involved in the onset of many diseases such as cancer and atherosclerosis as well as in degenerative processes associated with aging (Turkoglu et al., 2007; Thetsrimuang et al., 2011). Almost all aerobic organisms are well protected against free radicals by enzymes such as superoxide dismutase or compounds such as tocopherols and glutathione (Elmastas et al., 2005; Zongo et al., 2010). When the mechanism of antioxidant. protection becomes unbalanced by factors such as agcing and stress, deterioration of physiological functions may occur, resulting in diseases and accelerated ageing. However, antioxidant-containing foods may be used to help the human body to protect against oxidative damage (Cazzi et al., 1997; Okwulehie et al., 2007). Many species of fruits, vegetables, cereals and seeds have been investigated for antioxidant activity (Halliwell and Gutteridge, 2003). Natural antioxidants are being studied for their capacity to protect cells from damage brought on by reactive oxygen species (Niki et al., 1994). Mushrooms accumulate secondary metabolites, including phenolic compounds, terpenes and alkaloids (Buigut, 2002). Mushrooms are appreciated for their chemical and nutritional properties. Mushrooms have also been reported as therapeutic foods that are useful in preventing diseases such as hypertension, hyperglycemia and cancer. These functional characteristics are mainly due to their chemical content (Manzi et al., 2001; Chenghom et al., 2010). Mushrooms are considered as source of proteins, vitamins, lipids. carbohydrates and minerals (Jiskami, 2001). The essential amino acids, water-soluble vitamins and essential minerals are present (Gulein et al., 2002). Will edible mushrooms are becoming more and more important in our diet for their pharmacological properties (Halliwell and Gulleridge, 2003). Although, there are many studies on cultivated and wild mushrooms in the northern hemisphere, there is little information available about antioxidant properties and proximate chemical composition of wild mushrooms collected from different parts of Anatolia. Our objective Corresponding Author: Ilgaz Akata, Department of Biology, Faculty of Science, Ankara University. Muradiya Campus, Ankara, Turkey 134

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Int. J. Pharmacol., 8 (2): 134-138, 2012 was to evaluate the proximate chemical content and antioxidant activities of methanol extracts of fruit bodies of 16 wild mushrooms by free radical scavenging method. MATERIALS AND METHODS Mushrooms: In this study, 16 will edible mushroom species (Agrocybe cylindracea (DC.) Maire, Amanita ceciliae (Berk and Broome) Bas, Armillaria mellea (Vahl.) P. Kumm., Boletus reticulatus Schaeff., Cantharellus cibarius Fr., Chlorophyllum rhacodes (Vittad.) Vellinga. Coprinus comatus (O.F. Müll.) Pers., Flammulina velutipes var. velutipes (Curtis) Singer, Lactarius deliciosus (L.) Gray, Lactarius salmonicolor R. Heim and Leclair, Pleurotus ostreatus (Jacq.) P. Kumm., Polyporus squamosus (Huds.) Fr., Rhizopogon roseolus (Corda) Th. Fr., Russula anthracina Romagn., Suillus collinitus (Fr.) Kuntze and Tricholoma myomyces (Pers.) (JE. Lange) were collected from different parts of Anatolia and were analyzed for their chemical content and antioxidant activities. Origin, fungarium number and families of these macrofungi were given in Table 1. All of the analyzed mushrooms were identified as edible macrofungi belonging to class Basidiomycetes. All mushroom samples were deposited in the Ankara University. Department of Biology, Turkey. Extraction process: A fine dried mushroom sample (1 g) was continuously extracted with methanol in a Soxhlet apparatus for 24 h. The methanolic extract was evaporated to dryness at 15°C and redissolved in methanol and stored at 4°C prior to fiuther use (Barros et al., 2007). Proximate analysis assay: The water amount, and total carbohydrates of mushroom samples were determined according to AOAC (2006). Total protein was determined Table 1: Geographic distribution of edible mushroom species Species A cylindracea A cecilice A. meliea B. reticulatus C. cibarius C. Phacodes C. combus F. velutipes Families Strophariaceae Amanilaccac Physalacriaceae Boletaceae Cantharellaceae Agaricaccac Agaricaceae Physalacriaceae Russulaceae by the Kjeldahl method (AOAC, 2006). Protein was calculated using the general factor of 6.25. The weight of fat extracted from 5 g of mushroom sample was determined to calculate the lipid content. Diethyl ether was used as an extraction solvent where the extraction was performed for 4 h. Two grams of sample, in a porcelain container, was ignited and incinerated in the muffle furnace at about 550°C until a grayish while ash was obtained (AOAC, 2006). Free-radical scavenging assay: The capacity to scavenge the “stable” free radical DPPH was monitored according to the method of Barros et al. (2007). Various concentrations of methanolic extracts from mushrooms (2 mL) were mixed with 2 mL of methanolic solution containing DPPH radicals (6×10 mol). The mixture was shaken vigorously and left to stand for 30 min in the dark (until stable absorption values were obtained). The reduction of the DPPH radical was determined by measuring the absorption at 517 m. The RachionlScavenging Activity (RSA) was calculated as a percentage of DPPII discoloration using the equation: %RSA=A-Ay A-554 *100 where, A, is the absorbance of the solution when the sample extract has been added at a particular level and A is the absorbance of the DPPH solution (Ramkumar et al., 2010). Also, extract amounts of the samples were determined and concentrations were calculated. The assays were carried out in triplicate and the results expressed as mean values standard deviations. Butylated hydroxytoluene (BHT) was used as standard. Coordinate Altitude (rn) Fungarium No. N 39 56-E 32° 49° 860 AKATA 1037 N 40 53-E 39° 507 850 AKATA 3037 N 40° 35-31° 16° 1420 AKATA 2936 N1103-E 33°/11° 1880 AKATA 1091 N 40° 53-E 30° 50° N4109-E 33° 50° 850 AKATA 3011 1580 AKATA 2005 N 39° 56-32°/19° N 39° 56-32°/19° 860 AKATA 2113 860 AKATA 2127 L. deliciosus L. salmonicolor Russulaccac P. ostreatus N40 36-E 31° 17 1340 AKATA 2434 N 40 36-E 31° 17° 1350 AKATA 2413 P. squamosis R roseolus R anthracinaz S. collinitus Tmyomyces Russulaceae Suillaccac Pleurotaceae Polyporaceae N 39° 56-E 32° 49° 860 AKATA 3093 N 39 56-E 32° 19° 860 AKATA 3091 Rhizopogonaceae N40 35-E 31° 15° 1530 AKATA 3024 N4106-E 33° 44° 1400 AKATA 1184 N4104-E 33° 44° 1780 AKATA 1068 Tricholomataceae N4108 - 33° 50° 1200 AKATA 1561 135

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Int. J. Pharmacol., 8 (2): 134-138, 2012 Statistical analysis: The data presented are the averages of the results of three replicates with a standard error of less than 5%. RESULTS AND DISCUSSION Extraction yields and free radical scavenging activity: The yields of methanol extracts of wild mushrooms are given in Table 2. The methanol extracts of fruit bodies were subjected to screening for possible antioxidant. activity by the DPPH free radical scavenging method (Barros et al., 2007). Free radical scavenging values of fruit bodies extracts as percentage are shown in Table 2. Methanol extracts of P. ostreatus and A. mellea showed the strongest radical scavenging effect. (96.16%) at 2.72 and 4.51 mg ml, respectively. This activity was followed by A. cylindracea (95.79%) and C. cibarius (95.61%), respectively (Table 2). The lowest scavenging activity was exhibited by C. rhacodes (70.16%). However, the scavenging effect for BIIT was 98.24% at 3.0 mg mL. In previous studies, the antioxidant activities of methanolic extracts of several commercial and medicinal mushrooms have been reported (Yang et al., 2002, Mau et al., 2004). Those studies claimed that the methanolic extracts of mushroom species showed high antioxidant activity on the lipid peroxidation. Barros et al. (2007) found that methanolic extracts of Leucopaxillus giganteus, Sarcodon imbricatus and Agaricus arvensis scavenged 100.00, 80.00 and 68.30% of DPPH radicals al 5.0 mg T., respectively. Al 1.50 mg ml. 1, the methanolic extracts of Boletus edulis. Xerocomus chrysenteron, Suillus collinitus and Lactarius deterrimus scavenged 94.66, 89.61, 88.27 and 27.73%, respectively (Sarikurkcu et al., 2008). In present study, scavenging activity of S. collinitus was determined Table 2: Extraction yields and antioxidant activity values of wild edible mushrooms Species 95.35±0.10 Extract concentration mig mL) Extraction yields (%) Polyporus squuTKASS 3.46 17.3 RSA (%) 95.35+0.10 Pleurotus ostrealus 2.72 13.6 96.16+0.42 Amanita cecilia 4.65 23.2 Loctorius salmonicolor 2.90 11.5 F. velutipes var. velutipes 115 22.2 Russula anthracina 2.31 11.5 Agrocybe cylindracea 2.82 14.1 Boletus reticulatus 3.17 15.8 Tricholoma myomyces 2.97 11.8 91.1710.31 95.2710.00 90.62±0.73 95.79+0.10 94.83+0.84 81.93±0.112 Cantorellus cibarius 3.34 16.7 95.6410.10 Armillaria mellea 4.51 22.5 96.1610.00 Suilles collinilis 2.91 14.5 Lactarius deliciosus 2.56 12.7 Rhizopogon roseolus 2.61 13.0 71.94+1.04 92.02±0.21 88.11±0.52 Coprinus comatus 5.09 2.5.1 91.610.10 Chlorophyllum rhacodes 2.35 11.7 BHT 3.00 70.46±0.21 98.24 RSA: Radical scavenging activity at 71.94% at 2.91 mg mL. According to Gezer et al. (2006), the scavenging effect of Romaria flava was 73.30%. Gaafar et al. (2010) reported that Pleurotus ostreatus can improve the antioxidant status during ageing and minimize the occurrence of age-associated disorders associated with involvement of free radicals. Total lipids, triglycerides and total cholesterol reduced in rats supplemented with 10% dried P. ostreatus at 6.85%. 34.00% and 19.13%, respectively. Also, some liver enzymes values [Aspartate Amino Transferase (AST), alanine amino transferase (ALT) and Alkaline Phosphatase (AP)] of aging rats decreased at 37.78, 35.57 and 19.55% with 10% dried P. ostreatus (Gaafar et al., 2010). Yang et al. (2007) found that Am-1 which is one of the saccharides of A. mellea has antioxidant property. Am-1 is a glucopyranose (containing glucuronic acid) and mainly linked by SS (1-3) and SS (1-6) glucosidic linkage (Yang et al., 2007). The carbohydrate content of mushrooms represents the bulk of fruiting bodies accounting for 30 to 65% on dry weight basis. The mannitol, also called as mushroom sugar constitutes about 80% of the total free sugars, hence it is dominant. Water soluble polysaccharides of mushrooms are antitumor and antioxidant (Wani et al., 2010). According to Fu and Shieh (2002), F. velutipes has total phenolics al. 0.75 mg g Free radical scavenging is a generally accepted mechanism for phenolic antioxidants to inhibit lipid oxidation. The antioxidative activity of phenolics is generally governed by their chemical structures, the activity increases with increasing the number of hydroxyl groups and their location in the molecules involved. F. velutipes has tyrosine a phenolic amino acid at 7.85% (Ko et al., 1995). Thus, another possibility for the antioxidant activity may be attributed to the presence of small amounts of vitamin C in the mushrooms. F. velutipes has ascorbic acid at 46 mg/100 g dry matter (Fu and Shieh, 2002). Proximate analysis assay: Proximate analysis was carried out on 16 wild edible mushroom species. Results of proximate composition are presented in Table 3. L. salmonicolor had the highest concentration of protein (46.81%) followed by T. myomyces and S. collinitus while A. cylindraced had the least (13.32%). With respect. To moisture content, A. cylindracea had the highest value (10.32%) and C. rhacodes the least value (7.21%). B. reticulatus had the highest carbohydrate (67.18%) and ash was highest in L. deliciosus (15.16%). The ether extract (fat) values are between 1.00% (B. reticulatus) and 13.32% (F. squamosus) (Table 3). The analytical food value as approximate indices of nutritional quality, it would appear that some of these 136

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Int. J. Pharmacol., 8 (2): 134-138, 2012 Table 3: Proximate composition (%) of 16 wild edible mushrooms Species Polyporus squamosus Pleurotus ostrealus 10.31 Ash Fat Moisture Protein Carbolrydrate 7.14 3.98 7.25 3.21 10.32 13.32 65.24 16.96 62.27 Amanita cecilice 10.75 5.91 9.34 31.20 42.81 Loctorius salmonicolor 5.6-1 1.00 8. 18 17.70 $7.18 F. velaipes var. velutipes 10.40 7.33 9.84 22.04 50.40 Russula anthrina 7.71 9.46 7.24 23.66 $1.93 Agrocybe cylindracea Boletus reticulatus 7.25 1.5.29 289 1.50 9.26 18.83 63.16 8.01 36.67 37.14 Tricholoma muomyces Cantharellus cibarius 15.46 3.29 9.03 18.40 5.88 1.35 8.43 46.81 53.83 37.53 11.21 5.97 8.91 22-11 10.49 13.32 9.70 20.33 Lactarius deliciosus 6.58 7.38 7.93 26.57 Rhizopogon roseolus 9.37 1.31 8.96 20.55 Coprinus comoÌUS 14.36 4.90 Chlorophyllum rhacodes 3.37 817 9.59 9.39 38.06 46.77 51.12 46.17 $1.54 56.81 33.10 32.30 Armillaria mellea Stillus colliitus mushrooms fall between most legumes and meat. In earlier studies, Gruen and Wong (1982) indicated that edible. macrofungi were highly nutritional and compared favorably with meat, egg, legumes and milk. Some of the mushrooms are known to possess anticancer and hypocholesterolaemic agents. which implies that mushrooms could hold special attraction for and may be recommended for people with high cholesterol ailments. The protein contents of the mushrooms were close to those reported by Aletor (1995) in which the author obtained for Termitomyces robustus (33.80%), Psathyrella atroumbonata (32.80%) and Schizophyllum commune (27.00%). The author reported 13.90% ash contents for T. robustus. Also, Adejumo and Awosanya. (2005) reported that 36.80% protein content for Termitomyces mummiformis and 22.80% for Russula vesca. In the same study, reported 70.90% carbohydrate content for R. vesca. The protein contents of the mushrooms analyzed in this study were lower than those obtained in the previous study Kalyoncu et al. (2010) 83.40% for Sparassis crispa and 75.56% for Meripilus giganteus. Ash contents of these mushrooms were the same with mushrooms in presented study. In generally, lipid contents of mushrooms are low but may contribute towards palatability. CONCLUSIONS Antioxidants are chemical compounds that protect cells from the damage caused by unstable molecules known as Reactive Oxygen Species (ROS) or free radicals. ROS are powerful oxidants and those chemical entities that contain unpaired electrons. They are capable of randomly damaging cells, viz. lipids, proteins, DNA. sugars and are involved in mutations and cancers (Wani et al., 2010). The antioxidants are an important defense of the body against ROS and mushrooms which are rich sources of antioxidants (Mau et al., 2004). Antioxidant properties of edible mushrooms are related ko low-molecular weight compounds, in particular to the phenolic fractions. Therefore, a wide range of these beneficial phenolic compounds could be natural substrates of oxidative enzymes, such as peroxidases which are present in high levels in mushrooms (Gursoy et al., 2009). On the basis of the results it is suggested that the extract of wild mushroom species evaluated here could be of use as an easily accessible source of antioxidant for the nourishment. However, at present, the active components in the mushroom extract responsible for the observed antioxidant activity are unknown. Therefore, further work could be done on the isolation and purification of the active components from the mushrooms for showing the mode of action of them. As far as our literature survey could ascertain, there is no information about. The mushroom species presented here. From this point of view, this study could be assumed as the first report on these will species and it can be concluded that since these wild mushroom samples have high free radical scavenging activity, they can be used health beneficial antioxidant supplements. REFERENCES AOAC 2006 Official Methods of Analysis. 18th Edn.. Association of Official Analytical Chemists Inc.. Arlington, TX, USA. Adejumo, T.O. and O.B. Awosanya, 2005. Proximate and mineral composition of four edible mushroom species from South Western Nigeria. Afr. J. Biotechnol., 4: 1084-1088. Aletor, V., 1995. Compositional studies on edible tropical species of mushrooms. Food Chem., 5-1: 265-268. Aryantha, I.N.P., S. Kusmaningati, A.B. Sutjiatmo, Y. Sumartini, A. Nursidah and S. Narvikasari, 2010. The effect of Laetiporus sp. (Bull. ex Fr.) bond. et (Polyporaceae) extract. total blood Sing cholesterol. Biotechnology, 9: 312-318. Barros, L., M.J. Ferreira, B. Queiros, IC.FR. Ferreira and P. Baptista, 2007. 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