Biocompatible natural deep eutectic solvent-based extraction and cellulolytic enzyme-mediated transformation of Pueraria mirifica isoflavones: a sustainable approach for increasing health-bioactive constituents

Fonthip Makkliang , Boondaree Siriwarin , Gorawit Yusakul , Suppalak Phaisan , Attapon Sakdamas , Natthapon Chuphol , Waraporn Putalun , Seiichi Sakamoto

Bioresources and Bioprocessing ›› 2021, Vol. 8 ›› Issue (1) : 76

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Bioresources and Bioprocessing ›› 2021, Vol. 8 ›› Issue (1) : 76 DOI: 10.1186/s40643-021-00428-9
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Biocompatible natural deep eutectic solvent-based extraction and cellulolytic enzyme-mediated transformation of Pueraria mirifica isoflavones: a sustainable approach for increasing health-bioactive constituents

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Abstract

The presence of specific gut microflora limits the biotransformation of Pueraria mirifica isoflavone (PMI) glycosides into absorbable aglycones, thus limiting their health benefits. Cellulolytic enzyme-assisted extraction (CAE) potentially solves this issue; however, solvent extraction requires recovery of the hydrophobic products. Here, we established the simultaneous transformation and extraction of PMIs using cellulolytic enzymes and natural deep eutectic solvents (NADESs). The NADES compositions were optimized to allow the use of NADESs as CAE media, and the extraction parameters were optimized using response surface methodology (RSM). The optimal conditions were 14.7% (v/v) choline chloride:propylene glycol (1:2 mol ratio, ChCl:PG) at 56.1 °C for the cellulolytic enzyme (262 mU/mL) reaction in which daidzin and genistin were extracted and wholly transformed to their aglycones daidzein and genistein. The extraction of PMIs using ChCl:PG is more efficient than that using conventional solvents; additionally, biocompatible ChCl:PG enhances cellulolytic enzyme activity, catalyzing the transformation of PMIs into compounds with higher estrogenicity and absorbability.

Keywords

Biotransformation / Cellulolytic enzymes / Isoflavonoid / Natural deep eutectic solvent / Pueraria mirifica

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Fonthip Makkliang, Boondaree Siriwarin, Gorawit Yusakul, Suppalak Phaisan, Attapon Sakdamas, Natthapon Chuphol, Waraporn Putalun, Seiichi Sakamoto. Biocompatible natural deep eutectic solvent-based extraction and cellulolytic enzyme-mediated transformation of Pueraria mirifica isoflavones: a sustainable approach for increasing health-bioactive constituents. Bioresources and Bioprocessing, 2021, 8(1): 76 DOI:10.1186/s40643-021-00428-9

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References

[1]

Arboleya S, Watkins C, Stanton C, Ross RP. Gut Bifidobacteria populations in human health and aging. Front Microbiol, 2016, 7: 1204.

[2]

Bajkacz S, Adamek J. Evaluation of new natural deep eutectic solvents for the extraction of isoflavones from soy products. Talanta, 2017, 168: 329-335.

[3]

Braune A, Blaut M. Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes, 2016, 7(3): 216-234.

[4]

Chen H, Hayn M, Esterbauer H. Purification and characterization of two extracellular beta-glucosidases from Trichoderma reesei. Biochim Biophys Acta, 1992, 1121(1–2): 54-60.

[5]

Chen KI, Yao Y, Chen HJ, Lo YC, Yu RC, Cheng KC. Hydrolysis of isoflavone in black soy milk using cellulose bead as enzyme immobilizer. J Food Drug Anal, 2016, 24(4): 788-795.

[6]

Cheng QB, Zhang LW. Highly efficient enzymatic preparation of daidzein in deep eutectic solvents. Molecules, 2017, 22(1): 186.

[7]

Daily JW, Ko BS, Ryuk J, Liu M, Zhang W, Park S. Equol decreases hot flashes in postmenopausal women: a systematic review and meta-analysis of randomized clinical trials. J Med Food, 2019, 22(2): 127-139.

[8]

de Oliveira SF, Lemos TC, Sandora D, Monteiro M, Perrone D. Fermentation of soybean meal improves isoflavone metabolism after soy biscuit consumption by adults. J Sci Food Agric, 2020, 100(7): 2991-2998.

[9]

Fernandez MLA, Boiteux J, Espino M, Gomez FJV, Silva MF. Natural deep eutectic solvents-mediated extractions: the way forward for sustainable analytical developments. Anal Chim Acta, 2018, 1038: 1-10.

[10]

Gajardo-Parra NF, Cotroneo-Figueroa VP, Aravena P, Vesovic V, Canales RI. Viscosity of choline chloride-based deep eutectic solvents: experiments and modeling. J Chem Eng Data, 2020, 65(11): 5581-5592.

[11]

González-Rivera J, Husanu E, Mero A, Ferrari C, Duce C, Tinè MR, D'Andrea F, Pomelli CS, Guazzelli L. Insights into microwave heating response and thermal decomposition behavior of deep eutectic solvents. J Mol Liq, 2020

[12]

Izumi T, Piskula MK, Osawa S, Obata A, Tobe K, Saito M, Kataoka S, Kubota Y, Kikuchi M. Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J Nutr, 2000, 130(7): 1695-1699.

[13]

Khodaverdian S, Dabirmanesh B, Heydari A, Dashtban-Moghadam E, Khajeh K, Ghazi F. Activity, stability and structure of laccase in betaine based natural deep eutectic solvents. Int J Biol Macromol, 2018, 107(Pt B): 2574-2579.

[14]

Kongkaew C, Scholfield NC, Dhippayom T, Dilokthornsakul P, Saokaew S, Chaiyakunapruk N. Efficacy and safety of Pueraria candollei var. mirifica (Airy Shaw & Suvat.) Niyomdham for menopausal women: a systematic review of clinical trials and the way forward. J Ethnopharmacol, 2018, 216: 162-174.

[15]

Lee CH, Yang L, Xu JZ, Yeung SYV, Huang Y, Chen ZY. Relative antioxidant activity of soybean isoflavones and their glycosides. Food Chem, 2005, 90(4): 735-741.

[16]

Liu S. Liu S. Enzymes. Bioprocess engineering, 2017, Amsterdam: Elsevier.

[17]

Mansur AR, Song NE, Jang HW, Lim TG, Yoo M, Nam TG. Optimizing the ultrasound-assisted deep eutectic solvent extraction of flavonoids in common buckwheat sprouts. Food Chem, 2019, 293: 438-445.

[18]

Mayo B, Vazquez L, Florez AB. Equol: a bacterial metabolite from the daidzein isoflavone and its presumed beneficial health effects. Nutrients, 2019, 11(9): 2231.

[19]

Nakamura K, Zhu S, Komatsu K, Hattori M, Iwashima M. Deglycosylation of the isoflavone c-glucoside puerarin by a combination of two recombinant bacterial enzymes and 3-oxo-glucose. Appl Environ Microbiol, 2020, 86(14): e00607-00620.

[20]

Newton KM, Reed SD, Uchiyama S, Qu C, Ueno T, Iwashita S, Gunderson G, Fuller S, Lampe JW. A cross-sectional study of equol producer status and self-reported vasomotor symptoms. Menopause, 2015, 22(5): 489-495.

[21]

Nirmala FS, Lee H, Kim JS, Jung CH, Ha TY, Jang YJ, Ahn J. Fermentation improves the preventive effect of soybean against bone loss in senescence-accelerated mouse prone 6. J Food Sci, 2019, 84(2): 349-357.

[22]

Okabe Y, Shimazu T, Tanimoto H. Higher bioavailability of isoflavones after a single ingestion of aglycone-rich fermented soybeans compared with glucoside-rich non-fermented soybeans in Japanese postmenopausal women. J Sci Food Agric, 2011, 91(4): 658-663.

[23]

Peerakam N, Sirisa-Ard P, Huy NQ, On TV, Long PT, Intharuksa A. Isoflavonoids and phytoestrogens from Pueraria candollei var. mirifica related with appropriate ratios of ethanol extraction. Asian J Chem, 2018, 30(9): 2086-2090.

[24]

Peterson G, Barnes S. Genistein inhibition of the growth of human breast cancer cells: independence from estrogen receptors and the multi-drug resistance gene. Biochem Biophys Res Commun, 1991, 179(1): 661-667.

[25]

Phaisan S, Makkliang F, Putalun W, Sakamoto S, Yusakul G. Development of a colorless Centella asiatica (L.) Urb. extract using a natural deep eutectic solvent (NADES) and microwave-assisted extraction (MAE) optimized by response surface methodology. RSC Adv, 2021, 11(15): 8741-8750.

[26]

Pyo Y-H, Lee T-C, Lee Y-C. Enrichment of bioactive isoflavones in soymilk fermented with β-glucosidase-producing lactic acid bacteria. Food Res Int, 2005, 38(5): 551-559.

[27]

Qadir R, Anwar F, Batool F, Mushtaq M, Jabbar A. Enzyme-assisted extraction of Momordica balsamina L. fruit phenolics: process optimized by response surface methodology. J Food Meas Charact, 2018, 13(1): 697-706.

[28]

Setchell KD, Brown NM, Zimmer-Nechemias L, Brashear WT, Wolfe BE, Kirschner AS, Heubi JE. Evidence for lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Am J Clin Nutr, 2002, 76(2): 447-453.

[29]

Setchell KD, Brown NM, Summer S, King EC, Heubi JE, Cole S, Guy T, Hokin B. Dietary factors influence production of the soy isoflavone metabolite S−(−)equol in healthy adults. J Nutr, 2013, 143(12): 1950-1958.

[30]

Singh J, Kundu D, Das M, Banerjee R. Kuddus M. Enzymatic processing of juice from fruits/vegetables: an emerging trend and cutting edge research in food biotechnology. Enzymes in food biotechnology, 2019, Cambridge: Academic Press, 419-432.

[31]

Uribe S, Sampedro JG. Measuring solution viscosity and its effect on enzyme activity. Biol Proced Online, 2003, 5(1): 108-115.

[32]

Utkina EA, Antoshina SV, Selishcheva AA, Sorokoumova GM, Rogozhkina EA, Shvets VI. Isoflavones daidzein and genistein: Preparation by acid hydrolysis of their glycosides and the effect on phospholipid peroxidation. Russ J Bioorganic Chem, 2004, 30(4): 385-390.

[33]

Wang S, Yang Z, Peng N, Zhou J, Yong X, Yuan H, Zheng T. Optimization of ionic liquids-based microwave-assisted hydrolysis of puerarin and daidzein derivatives from Radix Puerariae Lobatae extract. Food Chem, 2018, 256: 149-155.

[34]

Wang C, Liu X, Zhang M, Shao H, Zhang M, Wang X, Wang Q, Bao Z, Fan X, Li H. Efficient enzyme-assisted extraction and conversion of polydatin to resveratrol from polygonum cuspidatum using thermostable cellulase and immobilized beta-glucosidase. Front Microbiol, 2019, 10(445): 445.

[35]

Xu HN, Zhang YX, He CH. Ultrasonically assisted extraction of isoflavones from stem of Pueraria lobata (Willd.) Ohwi and its mathematical model. Chin J Chem Eng, 2007, 15(6): 861-867.

[36]

Xu WJ, Huang YK, Li F, Wang DD, Yin MN, Wang M, Xia ZN. Improving β-glucosidase biocatalysis with deep eutectic solvents based on choline chloride. Biochem Eng J, 2018, 138: 37-46.

[37]

Yusakul G, Juengsanguanpornsuk W, Sritularak B, Phaisan S, Juengwatanatrakul T, Putalun W. (+)-7-O-Methylisomiroestrol, a new chromene phytoestrogen from the Pueraria candollei var. mirifica root. Nat Prod Res, 2020

[38]

Yusakul G, Kitisripanya T, Juengwatanatrakul T, Sakamoto S, Tanaka H, Putalun W. Enzyme linked immunosorbent assay for total potent estrogenic miroestrol and deoxymiroestrol of Pueraria candollei, a Thai herb for menopause remedy. J Nat Med, 2018, 72(3): 641-650.

[39]

Zhang XG, Lu Y, Wang WN, Liu ZY, Liu JW, Chen XQ. A novel enzyme-assisted approach for efficient extraction of Z-ligustilide from Angelica sinensis plants. Sci Rep, 2017, 7(1): 9783.

[40]

Zuorro A, Lavecchia R, Gonzalez-Delgado AD, Garcia-Martinez JB, L'Abbate P. Optimization of enzyme-assisted extraction of flavonoids from corn husks. Processes, 2019, 7(11): 804.

Funding

Walailak University (TH)(WU-IRG-63-005)

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