Solid-state fermentation as an efficient strategy for the biotransformation of lentils: enhancing their antioxidant and antidiabetic potentials

Abstract

Background

Fermentation is a classic industrial process that can be applied as an efficient strategy to increase the release of bioactive compounds with antioxidant and antidiabetic activities.

Methods

This work reported the effects of solid-state fermentation (SSF) performed using strains of Aspergillus oryzae and Aspergillus niger on the antioxidant (DPPH, ABTS and FRAP) and in vitro antidiabetic (inhibition of α-amylase and α-glucosidase activities) potential of lentils.

Results

The results showed that the profiles of the biological activities of the extracts obtained from the fermented samples varied greatly with respect to both the microorganism involved and the fermentation time. The extracts obtained from the fermented lentils by A. oryzae after 72 h and by A. niger after 48 h using the FRAP assay showed the most remarkable changes in the antioxidant activity, increasing by 107 and 81%, respectively, compared to the nonfermented lentils. The lentil extracts produced by fermentation with A. niger after 48 h were able to inhibit the α-glucosidase activity by up to 90%, while a maximal inhibition of amylase (~ 75%) was achieved by the lentil extract obtained after 24 h of fermentation with A. oryzae. The content of the total phenolic compounds (TPCs) and the identification of them in lentil extracts correlated well with the improvement of the biological activities.

Conclusion

These results suggested that SSF was feasible to obtain extracts of fermented lentils with improved antioxidant and antidiabetic properties. Additionally, these results indicated that the proper choice of microorganism is crucial to direct the process for the production of compounds with specific biological activities.

Keywords

Lentils / Solid-state fermentation / Antioxidant compounds / Antidiabetic potential

References

[1] Agil R, Gaget A, Gliwa J, Avis TJ, Willmore WG, Hosseinian F. Lentils enhance probiotic growth in yogurt and provide added benefit of antioxidant protection. LWT Food Sci Technol, 2013, 50: 45-49.

[2] Aguilar CN, Aguilera-Carbo A, Robledo A, Ventura J, Belmares R, Martinez D, Rodríguez-Herrera R, Contreras J. Production of antioxidant nutraceuticals by solid-state cultures of pomegranate (Punica granatum) peel and creosote bush (Larrea tridentata) leaves. Food Technol Biotechnol, 2008, 46: 218-222.

[3] Al-Duais M, Müller L, Böhm V, Jetschke G. Antioxidant capacity and total phenolics of Cyphostemma digitatum before and after processing: use of different assays. Eur Food Res Technol, 2009, 228: 813-821.

[4] Apostolidis E, Kwon YI, Ghaedian R, Shetty K. Fermentation of milk and soymilk by Lactobacillus bulgaricus and Lactobacillus acidophilus enhances functionality for potential dietary management of hyperglycemia and hypertension. Food Biotechnol, 2007, 21: 217-236.

[5] Ayyash M, Johnson SK, Liu S, Mesmari N, Dahmani S, Al Dhaheri AS, Kizhakkayil J. In vitro investigation of bioactivities of solid-state fermented lupin, quinoa and wheat using Lactobacillus spp. Food Chem, 2019, 275: 50-58.

[6] Bautista-Expósito S, Peñas E, Silván JM, Frias J, Martínez-Villaluenga C. pH-controlled fermentation in mild alkaline conditions enhances bioactive compounds and functional features of lentil to ameliorate metabolic disturbances. Food Chem, 2018, 248: 262-271.

[7] Bautista-Expósito S, Peñas E, Dueñas M, Silván JM, Frias J, Martínez-Villaluenga C. Individual contributions of Savinase and Lactobacillus plantarum to lentil functionalization during alkaline pH-controlled fermentation. Food Chem, 2018, 257: 341-349.

[8] Benzie IFF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem, 1996, 239: 70-76.

[9] Bier MCJ, Medeiros ABP, Kimpe ND, Soccol CR. Evaluation of antioxidant activity of the fermented product from the biotransformation of R-(+)-limonene in solid-state fermentation of orange waste by Diaporthe sp. Biotechnol Res Innov, 2019, 3: 168-176.

[10] Campos-Vega R, Loarca-Piña G, Oomah BD. Minor components of pulses and their potential impact on human health. Food Res Int, 2010, 43: 461-482.

[11] de Camargo AC, Vieira TMFS, Regitano-D’Arce MAB, Calori-Domingues MA, Canniatti-Brazaca SG. Gamma radiation effects on peanut skin antioxidants. Int J Mol Sci, 2012, 13: 3073-3084.

[12] de Castro RJS, Sato HH. Synergistic effects of agroindustrial wastes on simultaneous production of protease and α-amylase under solid state fermentation using a simplex centroid mixture design. Ind Crops Prod, 2013, 49: 813-821.

[13] de Castro RJS, Ohara A, Nishide TG, Bagagli MP, Dias FFG, Sato HH. A versatile system based on substrate formulation using agroindustrial wastes for protease production by Aspergillus niger under solid state fermentation. Biocatal Agric Biotechnol, 2015, 4: 678-684.

[14] Dey TB, Kuhad RC. Upgrading the antioxidant potential of cereals by their fungal fermentation under solid-state cultivation conditions. Lett Appl Microbiol, 2014, 59: 493-499.

[15] Dey TB, Chakraborty S, Jain KK, Sharma A, Kuhad RC. Antioxidant phenolics and their microbial production by submerged and solid state fermentation process: a review. Trends Food Sci Technol, 2016, 53: 60-74.

[16] Dulf FV, Vodnar DC, Socaciu C. Effects of solid-state fermentation with two filamentous fungi on the total phenolic contents, flavonoids, antioxidant activities and lipid fractions of plum fruit (Prunus domestica L.) by-products. Food Chem, 2016, 209: 27-36.

[17] Ekanayake LJ, Thavarajah D, Vial E, Schatz B, McGe R, Thavarajah P. Selenium fertilization on lentil (Lens culinaris Medikus) grain yield, seed selenium concentration, and antioxidant activity. Field Crop Res, 2015, 177: 9-14.

[18] Frias J, Miranda ML, Doblado R, Vidal-Valverde C. Effect of germination and fermentation on the antioxidant vitamin content and antioxidant capacity of Lupinus albus L. var Multolupa. Food Chem, 2005, 92: 211-220.

[19] Fujita A, Sarkar D, Genovese MI, Shetty K. Improving anti-hyperglycemic and anti-hypertensive properties of camu-camu (Myriciaria dubia Mc. Vaugh) using lactic acid bacterial fermentation. Process Biochem, 2017, 59: 133-140.

[20] García-Mora P, Martín-Martínez M, Bonache MA, González-Múniz R, Peñas E, Frias J, Martinez-Villaluenga C. Identification, functional gastrointestinal stability and molecular docking studies of lentil peptides with dual antioxidant and angiotensin I converting enzyme inhibitory activities. Food Chem, 2017, 221: 464-472.

[21] Gunenc A, Yeung MH, Lavergne C, Bertinato J, Hosseinian F. Enhancements of antioxidant activity and mineral solubility of germinated wrinkled lentils during fermentation in kefir. J Funct Foods, 2017, 32: 72-79.

[22] Handa CL, de Lima FS, Guelfi MFG, Fernandes MS, Georgetti SR, Ida EI. Parameters of the fermentation of soybean flour by Monascus purpureus or Aspergillus oryzae on the production of bioactive compounds and antioxidant activity. Food Chem, 2019, 271: 274-283.

[23] Hillis W, Swain T. The phenolic constituents of Prunus domestica. Sci Food Agric, 1959, 10: 63-68.

[24] Ibrahim MA, Koorbanally NA, Islam MS. Antioxidative activity and inhibition of key enzymes linked to type-2 diabetes (α-Glucosidase and α-Amylase) by Khaya senegalensis. Acta Pharm, 2014, 64: 311-324.

[25] Joshi M, Timilsena Y, Adhikari B. Global production, processing and utilization of lentil: a review. J Integr Agric, 2017, 16: 2898-2913.

[26] Kaprasob R, Kerdchoechuen O, Laohakunjit N, Sarkar D, Shetty K. Fermentation-based biotransformation of bioactive phenolics and volatile compounds from cashew apple juice by select lactic acid bacteria. Process Biochem, 2017, 59: 141-149.

[27] Limón RI, Peñas E, Torino MI, Martínez-Villaluenga C, Dueñas M, Frias J. Fermentation enhances the content of bioactive compounds in kidney bean extracts. Food Chem, 2015, 172: 343-352.

[28] Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem, 1959, 31: 426-428.

[29] Mirali M, Purves RW, Vandenberg A. Phenolic profiling of green lentil (Lens culinaris Medic.) seeds subjected to long-term storage. Eur Food Res Technol, 2016, 242: 2161-2170.

[30] Ohara A, dos Santos JG, Angelotti JAF, Barbosa PPM, Dias FFG, Bagagli MP, Sato HH, de Castro RJS. A multicomponent system based on a blend of agroindustrial wastes for the simultaneous production of industrially applicable enzymes by solid-state fermentation. Food Sci Technol, 2018, 38: 131-137.

[31] Oseguera-Toledo ME, de Mejia EG, Amaya-Llano SL. Hard-to-cook bean (Phaseolus vulgaris L.) proteins hydrolyzed by alcalase and bromelain produced bioactive peptide fractions that inhibit targets of type-2 diabetes and oxidative stress. Food Res Int, 2015, 76: 839-851.

[32] Sheih IC, Fang TJ, Wu TK, Chen RY. Effects of fermentation on antioxidant properties and phytochemical composition of soy germ. J Sci Food Agric, 2014, 94: 3163-3170.

[33] Simsek S, El SN, Kilinc AK, Karakaya S. Vegetable and fermented vegetable juices containing germinated seeds and sprouts of lentil and cowpea. Food Chem, 2014, 156: 289-295.

[34] Siva N, Thavarajah P, Thavarajah D. The impact of processing and cooking on prebiotic carbohydrates in lentil. J Food Compos Anal, 2018, 70: 72-77.

[35] Toldrá F, Reig M, Aristoy MC, Mora L. Generation of bioactive peptides during food processing. Food Chem, 2018, 267: 395-404.

[36] Torino MI, Limón RI, Martínez-Villaluenga C, Mäkinen S, Pihlanto A, Vidal-Valverde C, Frias J. Antioxidant and antihypertensive properties of liquid and solid state fermented lentils. Food Chem, 2013, 136: 1030-1037.

[37] Vaz-Patto MC, Amarowicz R, Aryee ANA, Boye JI, Chung H, Martín-Cabrejas MA, Domoney C. Achievements and challenges in improving the nutritional quality of food legumes. CRC Crit Rev Plant Sci, 2015, 34: 105-143.

[38] Wiriyaphan C, Chitsomboon B, Yongsawadigul J. Antioxidant activity of protein hydrolysates derived from threadfin bream surimi byproducts. Food Chem, 2012, 132: 104-111.

[39] Xavier JA, Valentim IB, Camatari FOS, de Almeida AMM, Goulart HF, Ferro JNS, Barreto EO, Cavalcanti BC, Bottoli CBG, Goulart MOF. Polyphenol profile by UHPLC-MS/MS, anti-glycation, antioxidant and cytotoxic activities of several samples of propolis from the northeastern semi-arid region of Brazil. Pharm Biol, 2017, 55: 1884-1893.

Funding

Fundação de Amparo à Pesquisa do Estado de São Paulo(2017/02000-9)

Fundo de Apoio ao Ensino, à Pesquisa e Extensão, Universidade Estadual de Campinas