Evaluation of Nutrient Contents, Antioxidant and Antimicrobial Activities of Two Edible Mushrooms Fermented with Lactobacillus fermentum

Main Article Content

Clement Olusola Ogidi*
Racheal Bukola Agbaje

Abstract

In this study, the edible mushrooms; Termitomyces robustus and Pleurotus ostreatus were fermented with lactic acid bacterium. The proximate composition, minerals, amino acids and fatty acids of unfermented and lacto-fermented mushrooms (mushrooms fermented with Lactobacillus fermentum) were revealed. The free radical scavenging and antimicrobial activities of ethanolic extracts from the mushrooms were carried out. The protein content of P. ostreatus and T. robustus fermented with L. fermentum increased (p<0.05) up to 17.7±1.9% and 10.4±0.4%, respectively. The crude fiber (7.8±0.0%) and total carbohydrates (76.6±7.9%) in lacto-fermented T. robustus as well as crude fiber (9.0±0.6%) and total carbohydrates (67.3±8.4%) in lacto-fermented P. ostreatus were reduced (p<0.05) when compared to unfermented mushroom samples. Lacto-fermented P. ostreatus had the highest valine content of 11.1±0.2 mg/100 g mushroom, while palmitic acid was found to be the most abundant saturated fatty acids (SFA) with 23.0±2.1 % in lacto-fermented T. robustus. The phenolic content of the studied mushrooms ranged from 5.6±0.0-7.8±0.0 mg GAE/g extract, while flavonoid was within 3.1±0.0 - 4.9±0.1 mg QE/g extract. The scavenging activity of the unfermented and lacto-fermented mushrooms against DPPH ranged from 62.8±6.8% to 91.3±10.2%. The extracts from lacto-fermented mushrooms showed better zones of inhibition ranging from 5.0±0.0 mm to 12.5±0.7 mm against tested isolates. The research suggests that the probiotic fermentation of mushrooms is a food processing method that can be adopted to enhance nutritional and functional properties of edible mushrooms.


 


Keywords: fermentation; preservatıon; lactic acid; fatty acid; amino acid


*Corresponding author: Tel.: (+234)7033830019 


                                             E-mail: clementogidi@yahoo.com

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References

Chang, S.-T. and Miles, P.G., 2008. Mushrooms: Cultivation, Nutritional Value, Medicinal Effect, and Environmental Impact. 2nd ed. Boca Raton: CRC Press.

Miller, A.M., Mills, K., Wong, T., Drescher, G., Lee, S.M., Sirimuangmoon, C., Schaefer, S., Langstaff, S., Minor, B. and Guinard, J.-X., 2014. Flavor-enhancing properties of mushrooms in meat-based dishes in which sodium has been reduced and meat has been partially substituted with mushrooms. Journal of Food Science, 79(9), S1795-S1804.

Feeney, M.J., Miller, A.M. and Roupas, P., 2014. Mushrooms-biologically distinct and nutritionally unique. Exploring a “Third Food Kingdom”. Nutrition Today, 49(6), 301-307.

Xue, Z., Hao, J., Yu, W. and Kou, X. 2017. Effects of processing and storage preservation technologies on nutritional quality and biological activities of edible fungi: a review. Journal of Food Process Engineering, 40(3), https://doi.org/10.1111/jfpe.12437

Diamantopoulou, P.A. and Philippoussis, A.N., 2015. Cultivated mushrooms: preservation and processing. In: Y.H. Hui and E. Özgül Evranuz, eds. Handbook of Vegetable Preservation and Processing. Boca Raton: CRC Press, pp. 495-526.

Zhang, K., Pu, Y.-Y. and Sun, D.-W., 2018. Recent advances in quality preservation of postharvest mushrooms (Agaricus bisporus): A review. Trends Food Science and Technology, 78, 72-82.

Zheng, H.-G., Chen, J.-C. and Ahmad, I., 2018. Preservation of king oyster mushroom by the use of different fermentation processes. Journal of Food Processing and Preservation, 42(1), https://doi.org/10.1111/jfpp.13396

Jabłonska-Rys, E., Sławnska, A. and Szwajgier, D., 2016. Effect of lactic acid fermentation on antioxidant properties and phenolic acid contents of oyster (Pleurotus ostreatus) and chanterelle (Cantharellus cibarius) mushrooms. Food Science and Biotechnology, 25(2), 439-444.

Liu, Y., Xie, X-X., Ibrahim, S.A., Khaskheli, S.G., Yang, H., Wang, Y-F. and Huang, W., 2016. Characterization of Lactobacillus pentosus as a starter culture for the fermentation of edible oyster mushrooms (Pleurotus spp.). LWT - Food Science and Technology, 68, 21-26.

Ogidi, C.O., Oyetayo, V.O., Akinyele, B.J., De Carvalho, C.A. and Kasuya, M.C.M., 2018. Food value and safety status of raw (unfermented) and fermented higher basidiomycetes, Lenzites quercina (L) P. Karsten. Preventive Nutrition and Food Science, 23(3), 228-234.

Jabłonska-Rys, E., Skrzypczak, K., Sławnska, A., Radzki, W. and Gustaw, W., 2019. Lactic acid fermentation of edible mushrooms: tradition, technology, current state of research: a review. Comprehensive Reviews in Food Science and Food Safety, 18(3), 655-669.

Lu, H., Lou, H., Hu, J., Liu, Z. and Chen, Q. 2020. Macrofungi: a review of cultivation strategies, bioactivity, and application of mushrooms. Comprehensive Reviews in Food Science and Food Safety, 19(5), 2333-2356.

Singh, V.P., 2018. Recent approaches in food bio-preservation - a review. Open Veterinary Journal, 8(1), 104-111.

Rhee, S.J., Lee, J.-E. and Lee, C.-H., 2011. Importance of lactic acid bacteria in Asian fermented foods. Microbial Cell Factories, 10, https://doi.org/10.1186/1475-2859-10-S1-S5

Petrova, P. and Petrov, K. 2020. Lactic acid fermentation of cereals and pseudocereals: ancient nutritional biotechnologies with modern applications. Nutrients, 12(4), 1118, https://doi.org/10.3390/nu12041118

Cheesbrough, M., 2006. District Laboratory Practices in Tropical Countries Part 2. 2nd ed. Cambridge: Cambridge University Press.

Cowan, S.T., Feltham, R.K.A., Steel, K.J. and Barrow, G.I., 1993. Cowan and Steel’s Manual for the Identification of Medical Bacteria. 3rd ed. Cambridge: Cambridge University Press.

AOAC, 2012. Official Methods of Analysis, 19th ed. Washington D.C.: Association of Official Analytical Chemists.

Spackman, D.H., Stein, W.H. and Moore, S., 1958. Automatic recording apparatus for use in the chromatography of amino acids. Analytical Chemistry, 30(7), 1190-1206.

Stojković, D., Reis, F.S., Barros, L., Glamočlija, J., Ćirić, A., van Griensven, L.J.I.D., Soković, M. and Ferreira, I.C.F.R., 2013. Nutrients and non-nutrients composition and bioactivity of wild and cultivated Coprinus comatus (O.F. Müll.) Pers. Food and Chemical Toxicology, 59, 289-296.

Singleton, V.L., Orthofer, R. and Lamuela-Raventos, R.M., 1999. [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-cioalteau reagents. Methods in Enzymology, 299, 152-178.

Meda, A., Lamien, C.E., Romito, M., Milligo, J. and Nacoulma, O.G., 2005. Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey as well as their radical scavenging activity. Food Chemistry, 91(3), 571-577.

Oyaizu, M., 1986. Studies on product of browning reaction. Antioxidative activities of products of browning reaction prepared from glucosamine. The Japanese Journal of Nutrition and Dietetics, 44(6), 307-315.

Gyamfi, M.A., Yonamine, M. and Aaniya, Y., 1999. Free-radical scavenging action of medicinal herbs from Ghana: Thonningia sanguine on experimentally-induced liver injuries. General Pharmacology, 32(6), 661-667.

Halliwell, B., Gutteridge, J.M.C. and Aruoma, O.I., 1987. The deoxyribose method: A simple ‘test-tube’ assay for determination of rate constants for reactions of hydroxyl radicals. Analytical Biochemistry, 165(1), 215-219.

Jagetia, G.C. and Baliga, M.S., 2004. The evaluation of nitric oxide scavenging activity of certain Indian medicinal plants in vitro: a preliminary study. Journal of Medicinal Food, 7(3), 343-348.

Achi, O.K. and Asamudo, N.U., 2019. Cereal-based fermented foods of Africa as functional foods. In: J.M. Mérillon, K. Ramawat, eds. Bioactive Molecules in Food. Cham: Springer, pp.1527-1558.

Rollán, G.C., Gerez, C.L. and LeBlanc, J.G., 2019. Lactic fermentation as a strategy to improve the nutritional and functional values of pseudocereals. Frontiers in Nutrition, 6, 98, https://doi.org/10.3389/fnut.2019.00098

Adebiyi, A.O., Tedela, P.O. and Atolagbe, T.T., 2016. Proximate and mineral composition of an edible mushroom, Termitomyces robustus (Beeli) Heim in Kwara State, Nigeria. American Journal of Food and Nutrition, 6(3), 65-68.

Khetarpaul, N. and Chauhan, B.M., 1989. Effect of fermentation on protein, fat, minerals and thiamine content of pearl millet. Plant Foods for Human Nutrition, 39, 169-177.

Institute of Medicine, 2005. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. Washington, DC: The National Academies Press.

Liang, J., Han, B.-Z., Nout, M.J.R. and Hamer, R.J., 2008. Effects of soaking, germination and fermentation on phytic acid, total and in vitro soluble zinc in brown rice. Food Chemistry, 110(4), 821-828.

Guillamón, E., García-Lafuente, A., Lozano, M., D ́Arrigo, M., Rostagno, M.A., Villares, A. and Martinez, J.A., 2010. Edible mushrooms: role in the prevention of cardiovascular diseases. Fitoterapia, 81(7), 715-723.

Eggleston, G., Finley, J.W., deMan, J.M., 2018. Carbohydrates. In: J.M. deMan, J.W. Finley, W.J. Hurst and C.Y. Lee, eds. Principles of Food Chemistry. Cham: Springer, pp. 165-229.

Day, C.N. and Morawicki R.O., 2018. Effects of fermentation by yeast and amylolytic lactic acid bacteria on grain sorghum protein content and digestibility. Journal of Food Quality, 2018, https://doi.org/10.1155/2018/3964392

Nkhata, S.G., Ayua, E., Kamau, E.H. and Shingiro, J.B., 2018. Fermentation and germination improve nutritional value of cereals and legumes through activation of endogenous enzymes. Food Science and Nutrition, 6(8), 2446-2458.

Falandysz, J. and Borovička, J., 2013. Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Applied Microbiology and Biotechnology, 97(2), 477-501.

Siwulski, M., Mleczek, M., Rzymski, P., Budka, A., Jasińska, A., Niedzielski, P., Kalač, P., Gąsecka, M., Budzyńska, S. and Mikołajczak P., 2017. Screening the multi-element content of Pleurotus mushroom species using Inductively Coupled Plasma Optical Emission Spectrometer (ICP-OES). Food Analytical and Methods, 10, 487-496.

Keen, C.L., Uriu-Adams, J.Y., Ensuma, J.L. and Gershwin, M.E., 2004. Trace elements/ minerals and immunity. In: M.E. Gershin, P. Nestel and C.L. Keen, eds. Handbook of Nutrition and Immunity. Totowa: Humana Press, pp. 117-140.

Hess, J.M., Wang Q., Kraft, C. and Slavin, J.L., 2017. Impact of Agaricus bisporus mushroom consumption on satiety and food intake. Appetite, 117, 179-185.

Bach, F., Helm, C.V., Bellettini, M.B., Maciel, G.M., Windson, C. and Haminiuk, I., 2017. Edible mushrooms: a potential source of essential amino acids, glucans and minerals International Journal of Food Science and Technology, 52 (11), 2382-2392.

Akabanda, F., Owusu-Kwarteng, J., Tano-Debrah, K., Parkouda, C. and Jespersen, L., 2014. The use of lactic acid bacteria starter culture in the production of Nunu, a spontaneously fermented milk product in Ghana, International Journal of Food Science, 2014, https://doi.org/10.1155/2014/721067

Novik, G., Meerovskaya O. and Savich, V., 2017. Waste Degradation and Utilization by Lactic Acid Bacteria: Use of Lactic Acid Bacteria in Production of Food Additives, Bioenergy and Biogas. [online] Available at: https://www.intechopen.com/books/food-additives/waste-degradation-and-utilization-by-lactic-acid-bacteria-use-of-lactic-acid-bacteria-in-production-

Barros, L., Cruz, T., Baptista, P., Estevinho, L.M. and Ferreira, I.C.F.R., 2008. Wild and commercial mushrooms as source of nutrients and nutraceuticals. Food and Chemical Toxicology, 46(8), 2742-2747.

Ribeiro, B., de Pinho, P.G., Andrade, P.B., Baptista, P. and Valentao, P., 2009. Fatty acid composition of wild edible mushrooms species: a comparative study, Microchemical Journal, 93(1), 29-35.

Sande, D., de Oliveira, G.P., Moura, M.A.F.E., Martins, B.A., Lima, M.T.N.S. and Takahashi, J.A., 2019. Edible mushrooms as a ubiquitous source of essential fatty acids. Food Research International, 125, https://doi.org/10.1016/j.foodres.2019.108524

National Research Council (US) Committee on Diet and Health, 1989. Diet and Health: Implications for Reducing Chronic Disease Risk. Washington (DC): National Academies Press (US).

Skąpska, S., Owczarek, L., Jasińska, U., Hasińska, A., Danielczuk, J. and Sokołowska, B., 2008. Changes in the antioxidant capacity of edible mushrooms during lactic acid fermentation. ŻYWNOŚĆ Nauka Technologia Jakość, 4(59), 243-250.

Ogidi, C.O., Oyetayo, V.O. and Akinyele B.J., 2018. Estimation of total phenolic, flavonoid content and free radical scavenging activity of a wild macrofungus, Lenzites quercina (L.) P. Karsten. Current Research in Environmental and Applied Mycology, 8(4), 425-437.

Huynh, N.T., Van Camp, J., Smagghe, G. and Raes, K., 2014. Improved release and metabolism of flavonoids by steered fermentation processes: a review. International Journal of Molecular Sciences, 15(11), 19369-19388.

Jabłonska-Rys, E., Sławinska, A., Radzki, W. and Gustaw, W., 2016. Evaluation of the potential use of probiotic strain Lactobacillus plantarum 299v in lactic fermentation of button mushroom fruiting bodies. Acta Scientiarum Polonorum, Technologia Alimentaria, 15(4), 399-407.

Gupta, S., Summuna, B., Gupta, M. and Annepu, S.K., 2019. Edible mushrooms: cultivation, bioactive molecules, and health benefits. In: J.M. Mérillon and K. Ramawat, eds. Bioactive Molecules in Food. Reference Series in Phytochemistry. Cham: Springer, pp. 1815-1847.

Shen, H‐S., Shao, S., Chen, J‐C. and Zhou T., 2017. Antimicrobials from mushrooms for assuring food safety. Comprehensive Reviews in Food Science and Food Safety, 16 (2), 316-329.

Pancheniak, E.F., Maziero, M.T., Rodriguez-León, J.A., Parada, J.L., Spier, M.R. and Soccol C.R., 2012. Molecular characterisation and biomass and metabolite production of Lactobacillus reuteri LPB P01-001: a potential probiotic. Brazilian Journal of Microbiology, 43(1), 135-147.

da Costa, R.J., Voloski, F.L.S., Mondadori, R.G., Duval, E.H. and Fiorentini, A.M., 2019. Preservation of meat products with bacteriocins produced by lactic acid bacteria isolated from meat, Journal of Food Quality, 2019, https://doi.org/10.1155/2019/4726510.

Bintsis, T., 2018. Lactic acid bacteria: their applications in foods. Journal of Bacteriology and Mycology, 6(2), 89-94.

Debabandya, M., Manoj, K.T., Sumedha, D. and Sadvatha, R.H., 2017. Sorghum fermentation for nutritional improvement. Advances in Food Science and Engineering, 1(4), 175-195.