In vitro study of antioxidant and antimicrobial activities of soybean tempeh and split gill fungus (Schizophyllum commune) as plant-based diets

Main Article Content

Yodsenee, K.
Suthirawut, S.
Pilasombut, K.
Urairong, H.
Rumjuankiat, K.

Abstract

Plant-based diets that reduce or eliminate animal product intake are known to ameliorate the incidence and clinical course of several illnesses. Soybean tempeh and split gill edible fungus (Schizophyllum commune) have long been consumed as plant-based diet choices. Total phenolic content (TPC), antioxidant and antimicrobial activities of soybean tempeh and S. commune extracts were investigated using water for extraction. The aqueous extract of fresh S. commune had the highest TPC at 1191.81 mg GAE/100g. Three methods were evaluated antioxidant activity as the diphenyl picrylhydrazyl radical scavenging test (DPPH), radical cation decolorization assay (ABTS) and reducing power. The IC50 values of fresh S. commune using DPPH and ABTS+ assays were 0.2812% and 0.5761%, respectively whereas the reducing power assay gave EC50 value at 0.3606%. Crude extracts of fresh tempeh and fresh S. commune exhibited antimicrobial activity against Staphylococcus aureus TISTR 746 at concentrations of 25 and 50 mg/ml, respectively. Two times the minimum inhibitory concentration (MIC) of fresh tempeh and fresh S. commune effectively reduced viable cells of S. aureus TISTR 746 of 5 log CFU/ml at 12 h. Both fresh tempeh and S. commune extracts showed promise as natural antioxidants for utilization as plant-based food

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How to Cite
Yodsenee, K., Suthirawut, S., Pilasombut, K., Urairong, H., & Rumjuankiat, K. (2022). In vitro study of antioxidant and antimicrobial activities of soybean tempeh and split gill fungus (Schizophyllum commune) as plant-based diets. International Journal of Agricultural Technology, 18(3), 1339–1354. retrieved from https://li04.tci-thaijo.org/index.php/IJAT/article/view/7348
Section
Original Study

References

Abdullah, N., Ismail, S. M., Aminudin, N., Shuib, A. S. and Lau, B. F. (2012). Evaluation of selected culinary-medicinal mushrooms for antioxidant and ace inhibitory activities. Evidence-Based Complementary and Alternative Medicine, 464238.

Abu, F., Mat Taib, C. N., Mohd Moklas, M. A. and Mohd Akhir, S. (2017). Antioxidant properties of crude extract, partition extract, and fermented medium of Dendrobium sabin flower. Evidence-Based Complementary and Alternative Medicine, 2907219.

Ahnan-Winarno, A. D., Cordeiro, L., Winarno, F. G., Gibbons, J. and H. Xiao. (2021). Tempeh: A semicentennial review on its health benefits, fermentation, safety, processing, sustainability, and affordability. Comprehensive Reviews in Food Science and Food Safety, 20:1717-1767.

Amarowicz, R. and Pegg, R. B. (2019). Natural antioxidants of plant origin. Advances in Food and Nutrition Research, 90:1-81.

Angiolella, L., Sacchetti, G. and Efferth, T. (2018). Antimicrobial and antioxidant activities of natural compounds. Evidence-Based Complementary and Alternative Medicine, 1945179.

Appiah, T., Boakye, Y. D. and Agyare, C. (2017). Antimicrobial activities and time-kill kinetics of extracts of selected ghanaian mushrooms. Evidence-based complementary and alternative medicine, 4534350:1-15.

Basso, V., Schiavenin, C., Mendonça, S., de Siqueira, F. G., Salvador, M. and Camassola, M. (2020). Chemical features and antioxidant profile by Schizophyllum commune produced on different agroindustrial wastes and byproducts of biodiesel production. Food Chemistry, 329:127089.

Cempaka, L., Eliza, N., Ardiansyah, D. Handoko, D. and Astuti, R. M. (2018). Proximate composition total phenolic content and sensory analysis of rice bran tempeh. Makara Journal of Science, 22:89-94.

Charoenteeraboon, J., Ngamkitidechaku, C., Soonthornchareonnon, N., Jaijoy, K. and Sireeratawong, S. (2010). Antioxidant activities of the standardized water extract from fruit of Phyllanthus emblica Linn. Songklanakarin Jounal Science and Technology, 32:599-604.

Corrin, T. and Papadopoulos, A. (2017). Understanding the attitudes and perceptions of vegetarian and plant-based diets to shape future health promotion programs. Appetite, 109:40-47.

Dulay, R. M. R., Vicente, J. J. A., Cruz, A. D., Gagarin, J. M., Fernando, W., Kalaw, S. P. and Reyes, R. G. (2016). Antioxidant activity and total phenolic content of Volvariella volvacea and Schizophyllum commune mycelia cultured in indigenous liquid media. Mycosphere, 7:131-138.

Emsen, B., Kocabas, A., Kaya, A., Cinar, S., Aasim, M. and Said, G. (2017). In vitro cytotoxicity, antibacterial and antioxidant properties of various extracts from Schizophyllum Commune Fr. Fresenius Environmental Bulletin, 26:1144-1153.

Farhadi, F., Khameneh, B., Iranshahi, M. and Iranshahy, M. (2019). Antibacterial activity of flavonoids and their structure–activity relationship: An update review. Phytotherapy Research, 33:13-40.

Ferreira, I. C., Barros, L. and Abreu, R. M. (2009). Antioxidants in wild mushrooms. Current Medicinal Chemistry, 16:1543-1560.

García, S. C., Carreño Ruiz, S. D. and Hernández, R. G. (2018). Fruit body production of Schizophyllum commune. In book: Updates on Tropical Mushrooms, 95-104.

Grajek and Olejnik (2010). The Influence of Food Processing and Home Cooking on the Antioxidant Stability in Foods. Functional Food Product Development (Smith, J., and Charter, E. /Functional Food Product Development), 178-205.

Gunawan-Puteri, M. D. P. T., Hassanein, T. R., Prabawati, E. K., Wijaya, C. H. and Mutukumira, A. N. (2015). Sensory characteristics of seasoning powders from overripe tempeh, a solid-state fermented soybean. Procedia Chemistry, 14:263-269.

Hashim, N., Woon Tai, C. W. T., Xin Wen, H. X. W., Ismail, A. and Kong, K. W. (2018). Comparative evaluation of antioxidant properties and isoflavones of tempeh fermented in two different wrapping materials. Current Research in Nutrition and Food Science Journal, 6:307-317.

He, J., Evans, N. M., Liu, H. and Shao, S. (2020). A review of research on plant-based meat alternatives: Driving forces, history, manufacturing, and consumer attitudes. Comprehensive Reviews in Food Science and Food Safety, 19:2639-2656.

Hever, J. and Cronise, R. J. (2017). Plant-based nutrition for healthcare professionals: implementing diet as a primary modality in the prevention and treatment of chronic disease. Journal of Geriatric Cardiology, 14:355-368.

Hidalgo, G. I. and Almajano, M. P. (2017). Red fruits: extraction of antioxidants, phenolic content, and radical scavenging determination: a review. Antioxidants (Basel), 6(1).

Hwang, I. G., Shin, Y. J. Lee, S. Lee, J. and Yoo, S. M. (2012). Effects of different cooking methods on the antioxidant properties of red pepper (Capsicum annuum L.). Preventive Nutrition and Food Science, 17:286-292.

Hwang, E. S. (2019). Effect of cooking method on antioxidant compound contents in cauliflower. Preventive Nutrition and Food Science Journal, 24:210-216.

Imtiaj, A., Jayasinghe, C., Lee, G. W., Kim, H. Y., Shim, M. J., Rho, H. S., Lee, H. S., Hur, H., Lee, M. W., Lee, U. Y. and Lee, T. S. (2008). Physicochemical requirement for the vegetative growth of Schizophyllum commune collected from different ecological origins. Mycobiology, 36:34-39.

Ito, M., Ito, T., Aoki, H., Nishioka, K., Shiokawa, T., Tada, H., Takeuchi, Y., Takeyasu, N., Yamamoto, T. and Takashiba, S. (2020). Isolation and identification of the antimicrobial substance included in tempeh using Rhizopus stolonifer NBRC 30816 for fermentation. International Journal of Food Microbiology, 325:108645.

Jabri, A., Kumar, A., Verghese, E., Alameh, A., Kumar, A., Khan, M. S. and Kalra, A. (2021). Meta-analysis of effect of vegetarian diet on ischemic heart disease and all-cause mortality. American Journal of Preventive Cardiology, 7:100182.

Johannesen, C. O., Dale, H. F., Jensen, C. and Lied, G. A. (2020). Effects of plant-based diets on outcomes related to glucose metabolism: a systematic review. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, 13:2811-2822.

Khatua, S., Paul, S. and Acharya, K. (2013). Mushroom as the potential source of new generation of antioxidant: a review. Research Journal of Pharmacy and Technology, 6:496-505.

Kobus-Cisowska, J., Szczepaniak, O., Szymanowska-Powałowska, D., Piechocka, J., Szulc, P. and Dziedziński, M. (2020). Antioxidant potential of various solvent extract from Morus alba fruits and its major polyphenols composition. Ciência Rural, Santa Maria, 50: e20190371.

Kuligowski, M., Pawłowska, K., Jasińska-Kuligowska, I. and Nowak, J. (2013). Evaluation of bean and soy tempeh infuence on intestinal bacteria and estimation of antibacterial properties of bean tempeh. Polish Journal of Microbiology, 62:189-194.

Kuligowski, M., Pawłowska, K., Jasińska-Kuligowska, I. and Nowak, J. (2017). Isoflavone composition, polyphenols content and antioxidative activity of soybean seeds during tempeh fermentation. Journal of Food, 15:27-33.

Lešková, E., Kubíková, J., Kováciková, E., Košická, M., Porubská, J. and Holcíková, K. (2006). Vitamin losses: Retention during heat treatment and continual changes expressed by mathematical models. Journal of Food Composition and Analysis, 19:252-276.

Li, D. (2014). Effect of the vegetarian diet on non-communicable diseases. Journal of the Science of Food and Agriculture, 94:169-173.

Liu, K. (2008). Food use of whole soybeans "soybeans: chemistry, production, processing, and utilization. Johnson, L. A., White, P. J. and Galloway, R. eds. AOCS Press, Urbana, IL, 441-481.

Liu, X., Frydenvang, K., Liu, H., Zhai, L., Chen, M., Olsen, C. E. and Christensen, S. B. (2015). Iminolactones from Schizophyllum commune. Journal of Natural Products, 78:1165-1168.

Lourenço, S. C., Moldão-Martins, M. and Alves, A. D. (2019). Antioxidants of natural plant origins: from sources to food industry applications. Molecules, 24:4132.

Mani, V. and Ming, L. C. (2017). Tempeh and other fermented soybean products rich in isoflavones, 453-474.

Marsh, K., Zeuschner, C. and Saunders, A. (2011). Health Implications of a vegetarian diet: a review. American Journal of Lifestyle Medicine, 6:250-267.

Matilla-Cuenca, L., Gil, C., Cuesta, S., Rapún-Araiz, B., Žiemytė, M., Mira, A., Lasa, I. and Valle, J. (2020). Antibiofilm activity of flavonoids on staphylococcal biofilms through targeting BAP amyloids. Scientific Reports, 10:18968.

Mayakrishnan, V., Abdullah, N., Abidin, M. H. Z., Fadzil, N. H. M., Johari, N. M. K., Aminudin N., and Abidin, N. Z. (2013). Investigation of the antioxidative potential of various solvent fractions from fruiting bodies of Schizophyllum commune (Fr.) mushrooms and characterization of phytoconstituents. Journal of Agricultural Science, 5:58-68.

McMacken, M. and Shah., S. (2017). A plant-based diet for the prevention and treatment of type 2 diabetes. Journal of Geriatric Cardiology, 14:342-354.

Meng, G. E., Tian, Y. C., Yang, Y. and Shi, J. (2016). Evaluation of DPPH free radical scavenging activity of various extracts of ligularia fischeri in vitro: a case study of shaanxi region. The Indian Journal of Pharmaceutical Sciences, 78:436-442.

Mickymaray, S., Alfaiz, F. A. and Paramasivam, A. (2020). Efficacy and mechanisms of flavonoids against the emerging opportunistic nontuberculous Mycobacteria. Antibiotics, 9:450.

Mirfat, A. H. S., Noorlidah, A. and Vikineswary, S. (2014). Antimicrobial activities of split gill mushroom Schizophyllum commune Fr. American Journal of Research Communication, 2:113-124.

Molina-Montes, E., Salamanca-Fernandez, E., Garcia-Villanova, B. and Sanchez, M. J. (2020). The impact of plant-based dietary patterns on cancer-related outcomes: a rapid review and meta-analysis. Nutrients, 12.

Noviana, A., Dieny, F. F., Rustanti1, N., Anjani, G., and Afifah, D. N. (2017). Antimicrobial activity of tempeh gembus hydrolysate. IOP Conference Series Earth and Environmental Science, 116:012044.

Nils-Gerrit Wunsch. (2020). Meat substitutes market in the U.S. - Statistics and Facts. Statista Dossier on The U.S. Meat Substitutes Market 62.

Özcan, Ö. and Ertan, F. (2018). Beta-glucan content, antioxidant, and antimicrobial activities of some edible mushroom species. Food Science and Technology, 6:47-55.

Pandey, K. B. and Rizvi, S. I. (2009). Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Medicine and Cellular Longevity, 2:270-278.

Puket, S. R. N., Sangkaew, T., Chanapan, P. and Techoei, S. (2019). Biological activity of β-gulcans from edible mushroom, Schizophyllum commune in Thailand. International Journal of Applied Pharmaceutics, 11:110-112.

Ranilla, L. G., Genovese, M. I. and Lajolo, F. M. (2009). Effect of different cooking conditions on phenolic compounds and antioxidant capacity of some selected Brazilian bean (Phaseolus vulgaris L.) Cultivars. Journal of Agricultural and Food Chemistry, 57:5734-5742.

Reyes, R. G., Grassel, W. and Rau, U. (2009). Coconut water as a novel culture medium for the biotechnological production of Schizophyllum. Journal of Nature Studies, 7:1-6.

Sabaté, J. and Soret. S. (2014). Sustainability of plant-based diets: back to the future. The American Journal of Clinical Nutrition, 100:476S-482S.

Sanjukta, S. and Rai, A. K. (2016). Production of bioactive peptides during soybean fermentation and their potential health benefits. Trends in Food Science and Technology, 50:1-10.

Sardarodiyan, M. and Mohamadi Sani, A. (2016). Natural antioxidants: sources, extraction, and application in food systems. Nutrition and Food Science, 46:363-373.

Sathiaseelan, A., Shit, C. S. and Chai, T. T. (2018). Anti-biofilm activity of fermented soybean tempeh extracts and fractions against oral primary colonizer bacteria. International Conference on Drug Discovery and Development, 1-12.

Shaffique, S., Kang, S. M., Kim, A. Y., Imran, M., Aaqil Khan, M. and Lee, I. J. (2021). Current knowledge of medicinal mushrooms related to anti-oxidant properties. Sustainability, 13:7948.

Shahidi, F. and Ambigaipalan, P. (2015). Phenolics and polyphenolics in foods, beverages, and spices: Antioxidant activity and health effects – A review. Journal of Functional Foods, 18:820-897.

Sihite, N. W., Rusmarilin, H., Suryanto, D. and Sihombing, D. R. (2018). Utilization of jasmine flower extract as antimicrobial in tempeh sausage. IOP Conference Series: Earth and Environmental Science, 205:012037.

Siritrakulsak, P. and Simla, S. (2015). Effects of conventional cooking method on antioxidant content in moonflower. Khon Kaen Agriculture Journal, 43:875-880.

Slima, S. B., Ktari, N., Trabelsi, I., Moussa, H., Makni, I. and Salah, R. B. (2018). Purification characterization and antioxidant properties of a novel polysaccharide extracted from Sorghum bicolor (L.) seeds in sausage. International Journal of Biological Macromolecules, 106:168-178.

Srichanun, M., Lerssutthichawal, T., Nganwisuthiphan, T. and Chirapongsatonkul, N. (2018). Possibility of split mushroom Schizophyllum commune by product extracts as antimicrobial and antioxidant agent for aquaculture. International Journal of Agricultural Technology, 14:1969-1976.

Syamsuri, R., Dewayani, W., Septianti, E. and Maintang. (2020). Chemical characteristic and sensory of tempeh sausage on different soybean varieties and cooking methods variation. IOP Conference Series: Earth and Environmental Science, 575:012012.

Taufik, D., Verain, M. C. D., Bouwman, E. P., and Reinders, M. J. (2019). Determinants of real-life behavioural interventions to stimulate more plant-based and less animal-based diets: A systematic review. Trends in Food Science and Technology, 93:281-303.

Tonstad, S., Butler, T., Yan, R. and Fraser, G. E. (2009). Type of vegetarian diet, body weight, and prevalence of type 2 diabetes. Diabetes Care, 32:791.

Tran, E., Dale, H. F., Jensen, C. and Lied, G. A. (2020). Effects of plant-based diets on weight status: a systematic review. diabetes, metabolic syndrome, and obesity: Targets and Therapy, 13:3433-3448.

Vijayalakshmi, M. and Ruckmani, K. (2016). Ferric reducing antioxidant power assay in plant extract. Bangladesh Journal of Pharmacology, 11:570-572.

Wild, F., Czerny, M., Janssen, A. M., Kole, A., Zunabovic, M., and Domig, K. J. (2014). The evolution of a plant-based alternative to meat. Agro FOOD Industry Hi Tech, 25:45-49.

Xu, X., Liu, A., Hu, S., Ares, I., Martinez-Larranaga, M. R., Wang, X. and Martinez, M. A. (2021). Synthetic phenolic antioxidants: Metabolism, hazards, and mechanism of action. Food Chemistry, 353:129488.

Yim, H. S., Chye, F. Y., Rao, V., Low, J. Y., Matanjun, P., How, S. E., and Ho, C. W. (2013). Optimization of extraction time and temperature on antioxidant activity of Schizophyllum commune aqueous extract using response surface methodology. Journal of Food Science and Technology, 50:275-283.