New Bioactive Molecules with Potential Antioxidant Activity from Various Extracts of Wild Edible Gelam Mushroom (Boletus spp.)
Author(s)
M. H. M. Y. Yuswan1,
Jameel R. Al-Obaidi2,
A. Rahayu1,
S. Sahidan1,
F. Shazrul1,
D. Fauzi1
Affiliation(s)
1 School of Bioscience and Biotechnology, National University of Malaysia, Selangor, Malaysia. 2 Agro-Biotechnology Institute, c/o MARDI Headquarters, Selangor, Malaysia.
1 School of Bioscience and Biotechnology, National University of Malaysia, Selangor, Malaysia. 2 Agro-Biotechnology Institute, c/o MARDI Headquarters, Selangor, Malaysia.
ABSTRACT
Boletus spp. is a wild edible Gelam mushroom, which is only available at coastal area of Bachok, Kelantan. Locals have used this mushroom as a food source and as a traditional medicine. In this study, antioxidants were extracted using Mili-Q water and methanol. Extraction of 1.0 g of Boletus spp. mushroom pileus and stipe by water produced 0.22 ± 0.09 g and 0.3 ± 0.07 g of total aqueous soluble extracts, respectively. Methanol extraction of 1.0 g Boletus spp. mushroom pileus and stipe produced 0.31 ± 0.08 mg and 0.37 ± 0.05 mg of total methanol soluble extracts, respectively. DPPH assay has been used to determine the value of antioxidant efficiency of each extracts. DPPH assay revealed that the EC50 value of pileus aqueous soluble extract and both pileus and stipe methanol soluble extracts were 1.2 mg/ml. The EC50 value of stipe aqueous soluble extracts was 1.4 mg/ml. The EC50 value of ascorbic acid, an antioxidant control was 0.5 mg/ml. Liquid chromatography- DPPH (LC-DPPH) assay combined with Quadrupole Time-of-flight Mass Spectrometry (QTOF-MS) analysis of 3:2 ratio methanol and water extract has detected 43 antioxidant compounds that were involved in the reduction of DPPH. To identify these compounds, SIMCA 3.0 software that consists of PCA, OPLS-DA and s-plot analyses had been used. PCA analysis had shown the antioxidant activity from sample on DPPH as 73.6%. This antioxidant activity confirmed by OPLS-DA analysis had shown the variability between sample and control as 99.6% with 99.3% prediction. S-plot selection had shown ten antioxidant compounds significantly involved in the DPPH assay. Four of these compounds were identified by the METLIN and NIST databases. The antioxidant metabolites were 2,4,6-trimethylacetophenone imine, glutamyl tryptophan, azatadine and lithocholic acid glycine conjugate. In conclusion, this study revealed that Boletus spp. mushroom is rich with natural antioxidants, which are potentially useful for multiple nutritional and health applications.
Boletus spp. is a wild edible Gelam mushroom, which is only available at coastal area of Bachok, Kelantan. Locals have used this mushroom as a food source and as a traditional medicine. In this study, antioxidants were extracted using Mili-Q water and methanol. Extraction of 1.0 g of Boletus spp. mushroom pileus and stipe by water produced 0.22 ± 0.09 g and 0.3 ± 0.07 g of total aqueous soluble extracts, respectively. Methanol extraction of 1.0 g Boletus spp. mushroom pileus and stipe produced 0.31 ± 0.08 mg and 0.37 ± 0.05 mg of total methanol soluble extracts, respectively. DPPH assay has been used to determine the value of antioxidant efficiency of each extracts. DPPH assay revealed that the EC50 value of pileus aqueous soluble extract and both pileus and stipe methanol soluble extracts were 1.2 mg/ml. The EC50 value of stipe aqueous soluble extracts was 1.4 mg/ml. The EC50 value of ascorbic acid, an antioxidant control was 0.5 mg/ml. Liquid chromatography- DPPH (LC-DPPH) assay combined with Quadrupole Time-of-flight Mass Spectrometry (QTOF-MS) analysis of 3:2 ratio methanol and water extract has detected 43 antioxidant compounds that were involved in the reduction of DPPH. To identify these compounds, SIMCA 3.0 software that consists of PCA, OPLS-DA and s-plot analyses had been used. PCA analysis had shown the antioxidant activity from sample on DPPH as 73.6%. This antioxidant activity confirmed by OPLS-DA analysis had shown the variability between sample and control as 99.6% with 99.3% prediction. S-plot selection had shown ten antioxidant compounds significantly involved in the DPPH assay. Four of these compounds were identified by the METLIN and NIST databases. The antioxidant metabolites were 2,4,6-trimethylacetophenone imine, glutamyl tryptophan, azatadine and lithocholic acid glycine conjugate. In conclusion, this study revealed that Boletus spp. mushroom is rich with natural antioxidants, which are potentially useful for multiple nutritional and health applications.
Cite this paper
Yuswan, M. , Al-Obaidi, J. , Rahayu, A. , Sahidan, S. , Shazrul, F. and Fauzi, D. (2015) New Bioactive Molecules with Potential Antioxidant Activity from Various Extracts of Wild Edible Gelam Mushroom (Boletus spp.). Advances in Bioscience and Biotechnology, 6, 320-329. doi: 10.4236/abb.2015.64031.
Yuswan, M. , Al-Obaidi, J. , Rahayu, A. , Sahidan, S. , Shazrul, F. and Fauzi, D. (2015) New Bioactive Molecules with Potential Antioxidant Activity from Various Extracts of Wild Edible Gelam Mushroom (Boletus spp.). Advances in Bioscience and Biotechnology, 6, 320-329. doi: 10.4236/abb.2015.64031.
References
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http://dx.doi.org/10.1016/0891-5849(96)00178-5 [4] Margaill, I., Plotkine, K. and Lerouet, D. (2005) Anti-oxidant Strategies in the Treatment of Stroke. Free Radical Biology and Medicine, 39, 429-443.
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http://dx.doi.org/10.1016/j. foodchem.2005.04.028 [8] Wong, J., Ng, T.B., Cheung, R.F., Ye, X.J., Wang, H.X. and Lam, S.K., et al. (2010) Proteins with Antifungal Properties and Other Medicinal Applications from Plants and Mushrooms. Applied Microbiology and Biotechnology, 87, 1221-1235.
http://dx.doi.org/doi:10.1007/s00253-010-2690-4 [9] Tidke, G. and Rai, M.K. (2006) Biotechnological Potential of Mushrooms: Drugs and Dye Production. International Journal of Medicinal Mushrooms, 8, 351-360.
http://dx.doi.org/doi:10.1615/IntJMedMushr.v8.i4.60 [10] Kawagishi, H. (2003) Functional Mushrooms and Their Active Principles. Food Style, 7, 70-73. [11] Kawagishi, H., Ando, M., Mizuno, T., Yokota, H. and Konishi, S. (1990) A Novel Fatty Acid from the Mushroom Hericium erinaceum. Agricultural and Biological Chemistry, 54, 1329-1331.
http://dx.doi.org/10.1271/bbb1961.54.1329 [12] Bernas, E., Jaworska, G. and Lisiewska, Z. (2006) Edible Mushrooms as a Source of Valuable Nutritive Constituents. Acta Scientiarum Polonorum, Technologia Alimentaria, 5, 5-20. [13] Kirk, P.M., Cannon, P.F., Minter, D.W. and Stalpers, J.A. (2008) Dictionary of the Fungi. 10th Edition, CAB International, Wallingford. [14] Kuka, M. and Cakste, I. (2011) Bioactive Compounds in Latvian Wild Edible Mushroom Boletus edulis. Proceedings of the 6th Baltic Conference on Food Science and Technology, Jelgava, 5-6 May 2011, 116-120. [15] Kasuga, A., Aoyagi, Y. and Sugahara, T. (1995) Antioxidant Activity of Fungus Suihs bovinus (L: Fr.) O. Kuntze. Journal of Food Science, 60, 1113-1115.
http://dx.doi.org/10.1111/j.1365-2621.1995.tb06304.x [16] Singleton, V.L. and Rossi, J.A. (1965) Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents. American Journal of Enology and Viticulture, 16, 144-158. [17] Wong, J.Y. and Chye, F.Y. (2009) Antioxidant Properties of Selected Tropical Wild Edible Mushrooms. Journal of Food Composition and Analysis, 22, 269-277.
http://dx.doi.org/10.1016/j.jfca.2008.11.021 [18] Calderón, A.I., Wright, B.J., Hurst, W.J. and van Breemen, R.B. (2009) Screening Antioxidants Using LC-MS: Case Study with Cocoa. Journal of Agricultural and Food Chemistry, 57, 5693-5699.
http://dx.doi.org/10.1021/jf9014203 [19] Mujic, I., Zekovic, Z., Lepojevic, Z., Vidovic, S. and Zikovic, J. (2010) Antioxidant Properties of Selected Edible Mushroom Species. Journal of Central European Agriculture, 11, 389-392. [20] Gummer, J.A., Krill, C., Du Fall, L., Waters, O.C., Trengove, R., Oliver, R. and Solomon, P. (2012) Metabolomics Protocols for Filamentous Fungi. In: Bolton, M.D. and Thomma, B.P.H.J., Eds., Plant Fungal Pathogens: Methods and Protocols, Humana Press, New York, 237-254.
http://dx.doi.org/10.1007/978-1-61779-501-5_15 [21] Hajji, M., Jarraya, R., Lassoued, I., Masmoudi, O., Damak, M. and Nasri, M. (2010) GC/MS and LC/MS Analysis, and Antioxidant and Antimicrobial Activities of Various Solvent Extracts from Mirabilis jalapa Tubers. Process Biochemistry, 45, 1486-1493.
http://dx.doi.org/10.1016/j.procbio.2010.05.027 [22] Vaclavik, L., Lacina, O., Hajslova, J. and Zweigenbaum, J. (2011) The Use of High Performance Liquid Chromatography—Quadrupole Time-of-Flight Mass Spectrometry Coupled to Advanced Data Mining and Chemometric Tools for Discrimination and Classification of Red Wines According to Their Variety. Analytica Chimica Acta, 685, 45-51.
http://dx.doi.org/10.1016/j.aca.2010.11.018 [23] Cheung, L.M., Cheung, P.C.K. and Ooi, V.E.C. (2003) Antioxidant Activity and Total Phenolics of Edible Mushroom Extracts. Food Chemistry, 81, 249-255.
http://dx.doi.org/10.1016/S0308-8146(02)00419-3 [24] Molyneux, P. (2004) The Use of Stable Free Radical Diphenylpicrylhydrazyl (DPPH) for Estimating Antioxidant Activity. Songklanakarin Journal of Science and Technology, 26, 211-219. [25] Heleno, S.A., Barros, L., Sousa, M.J., Martins, A., Santos-Buelga, C. and Ferreira, I.C.F.R. (2011) Targeted Metabolites Analysis in Wild Boletus Species. LWT—Food Science and Technology, 44, 1343-1348.
http://dx.doi.org/10.1016/j.lwt.2011.01.017 [26] Eriksson, L., Johansson, E., Kettaneh-Wold, N., Trygg, J., Wikstrom, C. and Wold, S. (2006) Multi- and Megavariate Data Analysis, Part 1: Basic Principles and Applications. 2nd Edition, Umetrics AB, Umea, 63-98.
[1] Wu, X.J. and Hansen, C. (2008) Antioxidant Capacity, Phenolic Content, and Polysaccharide Content of Lentinusedodes Grown in Whey Permeate-Based Submerged Culture. Journal of Food Science, 73, M1-M8.
http://dx.doi.org/10.1111/j.1750-3841.2007.00595.x [2] Coyle, J.T. and Puttfarcken, P. (1993) Oxidative Stress, Glutamate and Neurodegenerative Disorders. Science, 262, 689-695.
http://dx.doi.org/10.1126/science.7901908 [3] Kaul, N. and Forman, H.J. (1996) Activation of NFκB by the Respiratory Burst of Macrophages. Free Radical Biology and Medicine, 21, 401-405.
http://dx.doi.org/10.1016/0891-5849(96)00178-5 [4] Margaill, I., Plotkine, K. and Lerouet, D. (2005) Anti-oxidant Strategies in the Treatment of Stroke. Free Radical Biology and Medicine, 39, 429-443.
http://dx.doi.org/10.1016/j.freeradbiomed.2005.05.003 [5] Roberts, J.M. and Hubel, C.A. (1999) Is Oxidative Stress the Link in the Two-Stage Model of Preeclampsia? Lancet, 354, 788-789.
http://dx.doi.org/10.1016/S0140-6736(99)80002-6 [6] Hamid, A.A., Aiyelaagbe, O.O., Usman, L.A., Ameen, O.M. and Lawal, A. (2010) Antioxidants: Its Medicinal and Pharmacological Applications. African Journal of Pure and Applied Chemistry, 4, 142-151. [7] Djeridane, A., Yousfi, M., Nadjemi, B., Boutassouna, D., Stocker, P. and Vidal, N. (2006) Antioxidant Activity of Some Algerian Medicinal Plants Extracts Containing Phenolic Compounds. Food Chemistry, 97, 654-660.
http://dx.doi.org/10.1016/j. foodchem.2005.04.028 [8] Wong, J., Ng, T.B., Cheung, R.F., Ye, X.J., Wang, H.X. and Lam, S.K., et al. (2010) Proteins with Antifungal Properties and Other Medicinal Applications from Plants and Mushrooms. Applied Microbiology and Biotechnology, 87, 1221-1235.
http://dx.doi.org/doi:10.1007/s00253-010-2690-4 [9] Tidke, G. and Rai, M.K. (2006) Biotechnological Potential of Mushrooms: Drugs and Dye Production. International Journal of Medicinal Mushrooms, 8, 351-360.
http://dx.doi.org/doi:10.1615/IntJMedMushr.v8.i4.60 [10] Kawagishi, H. (2003) Functional Mushrooms and Their Active Principles. Food Style, 7, 70-73. [11] Kawagishi, H., Ando, M., Mizuno, T., Yokota, H. and Konishi, S. (1990) A Novel Fatty Acid from the Mushroom Hericium erinaceum. Agricultural and Biological Chemistry, 54, 1329-1331.
http://dx.doi.org/10.1271/bbb1961.54.1329 [12] Bernas, E., Jaworska, G. and Lisiewska, Z. (2006) Edible Mushrooms as a Source of Valuable Nutritive Constituents. Acta Scientiarum Polonorum, Technologia Alimentaria, 5, 5-20. [13] Kirk, P.M., Cannon, P.F., Minter, D.W. and Stalpers, J.A. (2008) Dictionary of the Fungi. 10th Edition, CAB International, Wallingford. [14] Kuka, M. and Cakste, I. (2011) Bioactive Compounds in Latvian Wild Edible Mushroom Boletus edulis. Proceedings of the 6th Baltic Conference on Food Science and Technology, Jelgava, 5-6 May 2011, 116-120. [15] Kasuga, A., Aoyagi, Y. and Sugahara, T. (1995) Antioxidant Activity of Fungus Suihs bovinus (L: Fr.) O. Kuntze. Journal of Food Science, 60, 1113-1115.
http://dx.doi.org/10.1111/j.1365-2621.1995.tb06304.x [16] Singleton, V.L. and Rossi, J.A. (1965) Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents. American Journal of Enology and Viticulture, 16, 144-158. [17] Wong, J.Y. and Chye, F.Y. (2009) Antioxidant Properties of Selected Tropical Wild Edible Mushrooms. Journal of Food Composition and Analysis, 22, 269-277.
http://dx.doi.org/10.1016/j.jfca.2008.11.021 [18] Calderón, A.I., Wright, B.J., Hurst, W.J. and van Breemen, R.B. (2009) Screening Antioxidants Using LC-MS: Case Study with Cocoa. Journal of Agricultural and Food Chemistry, 57, 5693-5699.
http://dx.doi.org/10.1021/jf9014203 [19] Mujic, I., Zekovic, Z., Lepojevic, Z., Vidovic, S. and Zikovic, J. (2010) Antioxidant Properties of Selected Edible Mushroom Species. Journal of Central European Agriculture, 11, 389-392. [20] Gummer, J.A., Krill, C., Du Fall, L., Waters, O.C., Trengove, R., Oliver, R. and Solomon, P. (2012) Metabolomics Protocols for Filamentous Fungi. In: Bolton, M.D. and Thomma, B.P.H.J., Eds., Plant Fungal Pathogens: Methods and Protocols, Humana Press, New York, 237-254.
http://dx.doi.org/10.1007/978-1-61779-501-5_15 [21] Hajji, M., Jarraya, R., Lassoued, I., Masmoudi, O., Damak, M. and Nasri, M. (2010) GC/MS and LC/MS Analysis, and Antioxidant and Antimicrobial Activities of Various Solvent Extracts from Mirabilis jalapa Tubers. Process Biochemistry, 45, 1486-1493.
http://dx.doi.org/10.1016/j.procbio.2010.05.027 [22] Vaclavik, L., Lacina, O., Hajslova, J. and Zweigenbaum, J. (2011) The Use of High Performance Liquid Chromatography—Quadrupole Time-of-Flight Mass Spectrometry Coupled to Advanced Data Mining and Chemometric Tools for Discrimination and Classification of Red Wines According to Their Variety. Analytica Chimica Acta, 685, 45-51.
http://dx.doi.org/10.1016/j.aca.2010.11.018 [23] Cheung, L.M., Cheung, P.C.K. and Ooi, V.E.C. (2003) Antioxidant Activity and Total Phenolics of Edible Mushroom Extracts. Food Chemistry, 81, 249-255.
http://dx.doi.org/10.1016/S0308-8146(02)00419-3 [24] Molyneux, P. (2004) The Use of Stable Free Radical Diphenylpicrylhydrazyl (DPPH) for Estimating Antioxidant Activity. Songklanakarin Journal of Science and Technology, 26, 211-219. [25] Heleno, S.A., Barros, L., Sousa, M.J., Martins, A., Santos-Buelga, C. and Ferreira, I.C.F.R. (2011) Targeted Metabolites Analysis in Wild Boletus Species. LWT—Food Science and Technology, 44, 1343-1348.
http://dx.doi.org/10.1016/j.lwt.2011.01.017 [26] Eriksson, L., Johansson, E., Kettaneh-Wold, N., Trygg, J., Wikstrom, C. and Wold, S. (2006) Multi- and Megavariate Data Analysis, Part 1: Basic Principles and Applications. 2nd Edition, Umetrics AB, Umea, 63-98.