Nutritional and antioxidant changes in lentils and quinoa through fungal solid-state fermentation with Pleurotus ostreatus

Abstract

Solid-state fermentation (SSF) may be a suitable bioprocess to produce protein-vegetal ingredients with increased nutritional and functional value. This study assessed changes in phenol content, antinutrient content, biomass production and protein production resulting from the metabolic activity of Pleurotus ostreatus, an edible fungus, in lentils and quinoa over 14 days of SSF. The impact of particle size on these parameters was also assessed because the process was conducted in both seeds and flours. Fungus biomass increased during fermentation, reaching 30.0 ± 1.4 mg/g dry basis and 32 ± 3 mg/g dry basis in lentil grain and flour and 52.01 ± 1.08 mg/g dry basis and 45 ± 2 mg/g dry basis in quinoa seeds and flour after 14 days of SSF. Total protein content also increased by 20% to 25% during fermentation, in all cases except lentil flour. However, the soluble protein fraction remained constant. Regarding phytic acid, SSF had a positive impact, with a progressive decrease being higher in flours than in seeds. Regarding antioxidant properties, autoclaving of the substrates promoted the release of polyphenols, together with antioxidant activity (ABTS, DPPH and FRAP), in all substrates. However, these parameters drastically decreased as fermentation progressed. These results provide scientific knowledge for producing lentil- or quinoa-based ingredients with low antinutrient content enriched with protein fungal biomass.

Keywords

Seeds / Flour / Protein / Polyphenols / Antinutrients

References

[1] Aguilera Y, Dueñas M, Estrella I, . Evaluation of phenolic profile and antioxidant properties of pardina lentil as affected by industrial dehydration. J Agric Food Chem, 2010, 58: 10101-10108.

[2] Aidoo KE, Hendry R, Wood BJB. Estimation of fungal growth in a solid state fermentation system. Eur J Appl Microbiol Biotechnol, 1981, 12: 6-9.

[3] AOAC. Official methods of analysis of AOAC International, 2000, Arlington: Association of Official Analysis Chemists International.

[4] Asensio-Grau A, Calvo-Lerma J, Heredia A, Andrés A. Enhancing the nutritional profile and digestibility of lentil flour by solid state fermentation with Pleurotus ostreatus. Food Funct, 2020, 11: 7905-7912.

[5] Atlı B, Yamaç M, Yıldız Z, Şőlener M. Solid state fermentation optimization of Pleurotus ostreatus for lovastatin production. Pharm Chem J, 2019, 53: 858-864.

[6] Becerra-Tomás N, Papandreou C, Salas-Salvadó J. Legume consumption and cardiometabolic health. Adv Nutr, 2019, 10: S437-S450.

[7] Bei Q, Liu Y, Wang L, . Improving free, conjugated, and bound phenolic fractions in fermented oats (Avena sativa L.) with Monascus anka and their antioxidant activity. J Funct Foods, 2017, 32: 185-194.

[8] Bohn T, Davidsson L, Walczyk T, Hurrell RF. Phytic acid added to white-wheat bread inhibits fractional apparent magnesium absorption in humans. Am J Clin Nutr, 2004, 79: 418-423.

[9] Bouchenak M, Lamri-Senhadji M. Nutritional quality of legumes, and their role in cardiometabolic risk prevention: a review. J Med Food, 2013, 16: 185-198.

[10] Brejnholt SM, Dionisio G, Glitsoe V, . The degradation of phytate by microbial and wheat phytases is dependent on the phytate matrix and the phytase origin. J Sci Food Agric, 2011, 91: 1398-1405.

[11] Briante R, Febbraio F, Nucci R. Antioxidant properties of low molecular weight phenols present in the Mediterranean diet. J Agric Food Chem, 2003, 51: 6975-6981.

[12] Bryngelsson S, Dimberg LH, Kamal-Eldin A. Effects of commercial processing on levels of antioxidants in oats (Avena sativa L.). J Agric Food Chem, 2002, 50: 1890-1896.

[13] Cai S, Wang O, Wu W, . Comparative study of the effects of solid-state fermentation with three filamentous fungi on the total phenolics content (TPC), flavonoids, and antioxidant activities of subfractions from oats (Avena sativa L.). J Agric Food Chem, 2012, 60: 507-513.

[14] Castro-Alba V, Lazarte CE, Perez-Rea D, . Fermentation of pseudocereals quinoa, canihua, and amaranth to improve mineral accessibility through degradation of phytate. J Sci Food Agric, 2019, 99: 5239-5248.

[15] Chang CH, Lin HY, Chang CY, Liu YC. Comparisons on the antioxidant properties of fresh, freeze-dried and hot-air-dried tomatoes. J Food Eng, 2006, 77: 478-485.

[16] Clemente A, Jimenez-Lopez JC. Introduction to the special issue: legumes as food ingredient: characterization, processing, and applications. Foods, 2020, 9: 1525.

[17] Couto SR, Sanromán MÁ. Application of solid-state fermentation to food industry—a review. J Food Eng, 2006, 76: 291-302.

[18] Devi J, Sanwal SK, Koley TK, . Variations in the total phenolics and antioxidant activities among garden pea (Pisum sativum L.) genotypes differing for maturity duration, seed and flower traits and their association with the yield. Sci Hortic, 2019, 244: 141-150.

[19] Dhull SB, Punia S, Kidwai MK, . Solid-state fermentation of lentil (Lens culinaris L.) with Aspergillusawamori: effect on phenolic compounds, mineral content, and their bioavailability. Legume Sci, 2020, 2: e37.

[20] Ergun SO, Urek RO. Production of ligninolytic enzymes by solid state fermentation using Pleurotus ostreatus. Ann Agrarian Sci, 2017, 15: 273-277.

[21] Espinosa-Páez E, Alanis-Guzmán MG, Hernández-Luna CE, . Increasing antioxidant activity and protein digestibility in Phaseolus vulgaris and Avena sativa by fermentation with the Pleurotus ostreatus Fungus. Molecules, 2017, 22: 2275.

[22] Febles CI, Arias A, Hardisson A, . Phytic acid level in wheat flours. J Cereal Sci, 2002, 36: 19-23.

[23] Fukumoto LR, Mazza G. Assessing antioxidant and prooxidant activities of phenolic compounds. J Agric Food Chem, 2000, 48: 3597-3604.

[24] Gallego M, Arnal M, Barat JM, Talens P. Effect of cooking on protein digestion and antioxidant activity of different legume pastes. Foods, 2020, 10: 47.

[25] Garrido-Galand S, Asensio-Grau A, Calvo-Lerma J, . The potential of fermentation on nutritional and technological improvement of cereal and legume flours: a review. Food Res Int, 2021, 145: 110398.

[26] Gebru YA, Sbhatu DB. Effects of fungi-mediated solid-state fermentation on phenolic contents and antioxidant activity of brown and white teff (Eragrostis tef (Zucc.) Trotter) grains. J Food Qual, 2020

[27] Gupta S, Lee JJL, Chen WN. Analysis of improved nutritional composition of potential functional food (Okara) after probiotic solid-state fermentation. J Agric Food Chem, 2018, 66: 5373-5381.

[28] Guttieri MJ, Peterson KM, Souza EJ. Milling and baking quality of low phytic acid wheat. Crop Sci, 2006, 46: 2403-2408.

[29] Haug W, Lantzsch H-J. Sensitive method for the rapid determination of phytate in cereals and cereal products. J Sci Food Agric, 1983, 34: 1423-1426.

[30] Hídvégi M, Lásztity R. Phytic acid content of cereals and legumes and interaction with proteins. Periodica Polytech Chem Eng, 2002, 46: 59-64.

[31] Hurrell RF, Reddy MB, Juillerat M-A, Cook JD. Degradation of phytic acid in cereal porridges improves iron absorption by human subjects. Am J Clin Nutr, 2003, 77: 1213-1219.

[32] Karimi S, Ferreira JA, Taherzadeh MJ (2021) The application of fungal biomass as feed. In: Encyclopedia of mycology. Elsevier, pp 601–612

[33] Khazaei H, Subedi M, Nickerson M, . Seed protein of lentils: current status, progress, and food applications. Foods, 2019, 8: 391.

[34] Liang J, Han BZ, Nout MJR, Hamer RJ. Effects of soaking, germination and fermentation on phytic acid, total and in vitro soluble zinc in brown rice. Food Chem, 2008, 110: 821-828.

[35] Limón RI, Peñas E, Torino MI, . Fermentation enhances the content of bioactive compounds in kidney bean extracts. Food Chem, 2015, 172: 343-352.

[36] Liu X, Kokare C. Brahmachari G, Demain AL, Adro JL. Microbial enzymes of use in industry. Biotechnology of microbial enzymes, 2017, Amsterdam: Elsevier Inc, 267-298.

[37] Madapathage Dona A. Enhancing antioxidant activity and extractability of bioactive compounds of wheat bran using thermal treatments, 2011, Winnipeg: University of Manitoba.

[38] Magro AEA, Silva LC, Rasera GB, . Solid-state fermentation as an efficient strategy for the biotransformation of lentils: enhancing their antioxidant and antidiabetic potentials. Bioresources and Bioprocessing, 2019, 6: 1-9.

[39] Marathe SA, Rajalakshmi V, Jamdar SN, Sharma A. Comparative study on antioxidant activity of different varieties of commonly consumed legumes in India. Food Chem Toxicol, 2011, 49: 2005-2012.

[40] Michael HW, Bultosa G, Pant LM. Nutritional contents of three edible oyster mushrooms grown on two substrates at Haramaya, Ethiopia, and sensory properties of boiled mushroom and mushroom sauce. Int J Food Sci Technol, 2011, 46: 732-738.

[41] Mora-Uzeta C, Cuevas-Rodríguez E, López-Cervantes J, . Improvement nutritional/antioxidant properties of underutilized legume tepary bean (Phaseolus acutifolius) by solid state fermentation. Agrociencia, 2019, 53: 987-1003.

[42] Motta C, Castanheira I, Gonzales GB, . Impact of cooking methods and malting on amino acids content in amaranth, buckwheat and quinoa. J Food Compos Anal, 2019, 76: 58-65.

[43] Muñoz-Llandes C, Guzmán-Ortiz F, Román-Guitiérrez A, et al (2019) Effect of germination on antinutritional compounds of grains and seeds. Types Process Effects, pp 83–99

[44] Muzquiz M, Varela A, Burbano C, . Bioactive compounds in legumes: pronutritive and antinutritive actions. Implications for nutrition and health. Phytochem Rev, 2012, 11: 227-244.

[45] Nemecek T, von Richthofen JS, Dubois G, . Environmental impacts of introducing grain legumes into European crop rotations. Eur J Agron, 2008, 28: 380-393.

[46] Nkhata SG, Ayua E, Kamau EH, Shingiro JB. Fermentation and germination improve nutritional value of cereals and legumes through activation of endogenous enzymes. Food Sci Nutr, 2018, 6: 2446-2458.

[47] Olukomaiya OO, Adiamo OQ, Fernando WC, . Effect of solid-state fermentation on proximate composition, anti-nutritional factor, microbiological and functional properties of lupin flour. Food Chem, 2020, 315: 126238.

[48] Pandey A. Solid-state fermentation. Biochem Eng J, 2003, 13: 81-84.

[49] Peng W, Tao Z, Ji Chun T. Phytic acid contents of wheat flours from different mill streams. Agric Sci China, 2010, 9: 1684-1688.

[50] Raghavarao KSMS, Ranganathan TV, Karanth NG. Some engineering aspects of solid-state fermentation. Biochem Eng J, 2003, 13: 127-135.

[51] Rocchetti G, Miragoli F, Zacconi C, . Impact of cooking and fermentation by lactic acid bacteria on phenolic profile of quinoa and buckwheat seeds. Food Res Int, 2019, 119: 886-894.

[52] Rodrigues Da Luz JM, Dias Nunes M, Albino Paes S, . Lignocellulolytic enzyme production of Pleurotus ostreatus growth in agroindustrial wastes. Braz J Microbiol, 2012, 43: 1508-1515.

[53] Romano A, Ferranti P (2019) Sustainable crops for food security: quinoa (Chenopodium quinoa Willd.). In: Encyclopedia of food security and sustainability, pp 399–402. https://doi.org/10.1016/B978-0-08-100596-5.22573-0

[54] Samtiya M, Aluko RE, Dhewa T. Plant food anti-nutritional factors and their reduction strategies: an overview. Food Prod Process Nutr, 2020, 2: 1-14.

[55] Sánchez-Navarro V, Zornoza R, Faz Á, Fernández JA. A comparative greenhouse gas emissions study of legume and non-legume crops grown using organic and conventional fertilizers. Sci Hortic, 2020, 260: 108902.

[56] Şanlier N, Başar Gökcen B, Ceyhun Sezgin A. Health benefits of fermented foods. Crit Rev Food Sci Nutr, 2019, 59: 506-527.

[57] Sarwar-Gilani G, Wu Xiao C, Cockell KA. Impact of antinutritional factors in food proteins on the digestibility of protein and the bioavailability of amino acids and on protein quality. Br J Nutr, 2012, 108: S315-S332.

[58] Schlemmer U, Frølich W, Prieto RM, Grases F. Phytate in foods and significance for humans: food sources, intake, processing, bioavailability, protective role and analysis. Mol Nutr Food Res, 2009, 53: S330-S375.

[59] Shi L, Mu K, Arntfield SD, Nickerson MT. Changes in levels of enzyme inhibitors during soaking and cooking for pulses available in Canada. J Food Sci Technol, 2017, 54: 1014-1022.

[60] Thaipong K, Boonprakob U, Crosby K, . Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extracts. J Food Compos Anal, 2006, 19: 669-675.

[61] Tomaselli Scotti C, Vergoignan C, Feron G, Durand A. Glucosamine measurement as indirect method for biomass estimation of Cunninghamella elegans grown in solid state cultivation conditions. Biochem Eng J, 2001, 7: 1-5.

[62] Torino MI, Limón RI, Martínez-Villaluenga C, . Antioxidant and antihypertensive properties of liquid and solid state fermented lentils. Food Chem, 2013, 136: 1030-1037.

[63] Villaño D, Fernández-Pachón MS, Troncoso AM, García-Parrilla MC. Comparison of antioxidant activity of wine phenolic compounds and metabolites in vitro. Anal Chim Acta, 2005, 538: 391-398.

[64] Xiao Y, Xing G, Rui X, . Enhancement of the antioxidant capacity of chickpeas by solid state fermentation with Cordyceps militaris SN-18. J Funct Foods, 2014, 10: 210-222.

[65] Xu L-N, Guo S, Zhang S. Effects of solid-state fermentation with three higher fungi on the total phenol contents and antioxidant properties of diverse cereal grains. FEMS Microbiol Lett, 2018, 365: fny163.

[66] Zhai FH, Wang Q, Han JR. Nutritional components and antioxidant properties of seven kinds of cereals fermented by the basidiomycete Agaricus blazei. J Cereal Sci, 2015, 65: 202-208.

Funding

Ministerio de Ciencia, Innovación y Universidades(PID2019-107723RB-C22)