Abstract
The study investigated an integrated bioprocessing of raw and by-products from sugarcane and dairy industries for production of non-digestible prebiotic and functional ingredients. The low-priced feedstock, whey, molasses, table sugar, jaggery, etc., were subjected to transglucosylation reactions catalyzed by dextransucrase from Leuconostoc mesenteroides MTCC 10508. HPLC analysis approximated production of about 11–14 g L−1 trisaccharide i.e. 2-α-d-glucopyranosyl-lactose (4-galactosyl-kojibiose) from the feedstock prepared from table sugar, jaggery, cane molasses and liquid whey, containing about 30 g L−1 sucrose and lactose each. The trisaccharide was hydrolysed into the prebiotic disaccharide, kojibiose, by employing recombinant β-galactosidase from Escherichia coli. The enzyme β-galactosidase achieved about 90% conversion of 2-α-d-glucopyranosyl-lactose into kojibiose. The d-fructose generated by catalytic reactions of dextransucrase was targeted for catalytic transformation into rare sugar, d-allulose (or d-psicose), by treating the samples with Smt3-d-psicose 3-epimerase. The catalytic reactions resulted in the conversion of ~ 25% d-fructose to d-allulose. These bioactive compounds are known to exert a plethora of benefits to human health, and therefore, are preferred ingredients for making functional foods.
Similar content being viewed by others
References
Singh A, Lal UR, Mukhtar HM, Singh PS, Shah G, Dhawan RK (2015) Phytochemical profile of sugarcane and its potential health aspects. Pharmacogn Rev 9:45–54
Chen ZY, Jiao R, Ma KY (2008) Cholesterol-lowering nutraceuticals and functional foods. J Agric Food Chem 56:8761–8773
Garcia JM, Narvaez PC, Heredia FJ, Orjuela A, Osorio C (2017) Physicochemical and sensory (aroma and colour) characterisation of a non-centrifugal cane sugar (“panela”) beverage. Food Chem 228:7–13
Liu YP, Zheng P, Sun ZH, Ni Y, Dong JJ, Zhu LL (2008) Economical succinic acid production from cane molasses by Actinobacillus succinogenes. Bioresour Technol 99:1736–1742
Hirabayashi K, Kondo N, Toyota H, Hayashi S (2017) Production of the functional trisaccharide 1-kestose from cane sugar molasses using Aspergillus japonicus β-fructofuranosidase. Curr Microbiol 74:145–148
Kaur P, Satyanarayana T (2005) Production of cell-bound phytase by Pichia anomala in an economical cane molasses medium: optimization using statistical tools. Process Biochem 40:3095–3102
Mironczuk AM, Rakicka M, Biegalska A, Rymowicz W, Dobrowolski A (2015) A two-stage fermentation process of erythritol production by yeast Y. lipolytica from molasses and glycerol. Bioresour Technol 198:445–455
Xia J, Xu J, Hu L, Liu X (2016) Enhanced poly(l-malic acid) production from pretreated cane molasses by Aureobasidium pullulans in fed-batch fermentation. Prep Biochem Biotechnol 46:798–802
Dai JY, Zhao P, Cheng XL, Xiu ZL (2015) Enhanced production of 2,3-butanediol from sugarcane molasses. Appl Biochem Biotechnol 175:3014–3024
Xu K, Xu P (2014) Efficient production of l-lactic acid using co-feeding strategy based on cane molasses/glucose carbon sources. Bioresour Technol 153:23–29
Ikram-Ul H, Ali S, Qadeer MA, Iqbal J (2004) Citric acid production by selected mutants of Aspergillus niger from cane molasses. Bioresour Technol 93:125 – 30
Zhang YY, Bu YF, Liu JZ (2015) Production of l-ornithine from sucrose and molasses by recombinant Corynebacterium glutamicum. Folia Microbiol (Praha) 60:393–398
Yan D, Lu Y, Chen YF, Wu Q (2011) Waste molasses alone displaces glucose-based medium for microalgal fermentation towards cost-saving biodiesel production. Bioresour Technol 102:6487–6493
Gong Y, Liu J, Jiang M, Liang Z, Jin H, Hu X, Wan X, Hu C (2015) Improvement of omega-3 docosahexaenoic acid production by marine Crypthecodinium cohnii dinoflagellate using rapeseed meal hydrolysate and waste molasses as feedstock. PLoS One 10:e0125368
Liu J, Huang J, Jiang Y, Chen F (2012) Molasses-based growth and production of oil and astaxanthin by Chlorella zofingiensis. Bioresour Technol 107:393–398
Wisuthiphaet N, Napathorn SC (2016) Optimisation of the use of products from the cane sugar industry for poly (3-hydroxybutyrate) production by Azohydromonas lata DSM 1123 in fed-batch cultivation. Process Biochem 51:352–361
Xia J, Xu Z, Xu H, Liang J, Li S, Feng X (2014) Economical production of poly(epsilon-l-lysine) and poly(l-diaminopropionic acid) using cane molasses and hydrolysate of streptomyces cells by Streptomyces albulus PD-1. Bioresour Technol 164:241–247
Sadeghiyan-Rizi T, Fooladi J, Momhed Heravi M, Sadrai S (2014) Optimization of l-tryptophan biosynthesis from l-serine of processed iranian beet and cane molasses and indole by induced Escherichia coli ATCC 11303 cells. Jundishapur J Microbiol 7:e10589
Sharma M, Patel SN, Lata K, Singh U, Krishania M, Sangwan RS, Singh SP (2016) A novel approach of integrated bioprocessing of cane molasses for production of prebiotic and functional bioproducts. Bioresour Technol 219:311–318
Patel SN, Sharma M, Lata K, Singh U, Kumar V, Sangwan RS, Singh SP (2016) Improved operational stability of d-psicose 3-epimerase by a novel protein engineering strategy, and d-psicose production from fruit and vegetable residues. Bioresour Technol 216:121–127
Cazetta ML, Celligoi MA, Buzato JB, Scarmino IS (2007) Fermentation of molasses by Zymomonas mobilis: effects of temperature and sugar concentration on ethanol production. Bioresour Technol 98:2824–2828
Broderick GA, Radloff WJ (2004) Effect of molasses supplementation on the production of lactating dairy cows fed diets based on alfalfa and corn silage. J Dairy Sci 87:2997–3009
Panesar PS, Kennedy JF (2011) Biotechnological approaches for the value addition of whey. Crit Rev Biotechnol 32:327–348
Panesar PS, Kennedy JF, Knill CJ, Kosseva MR (2007) Applicability of pectate-entrapped Lactobacillus casei cells for l(+) lactic acid production from whey. Appl Microbiol Biotechnol 74:35–42
Marangoni C, Furigo A, Glaucia A (2002) Production of poly (3-hydroxybutyrate-co-3-hydroxyvalerate) by Ralstonia eutropha in whey and inverted sugar with propionic acid feeding. Process Biochem 38:137–141
Corzo-Martinez M, Luscher A, de Las Rivas B, Munoz R, Moreno FJ (2015) Valorization of cheese and tofu whey through enzymatic synthesis of lactosucrose. PLoS One 10:e0139035
Qureshi N, Friedl A, Maddox IS (2014) Butanol production from concentrated lactose/whey permeate: use of pervaporation membrane to recover and concentrate product. Appl Microbiol Biotechnol 98:9859–9867
Alonso S, Rendueles M, Diaz M (2013) Feeding strategies for enhanced lactobionic acid production from whey by Pseudomonas taetrolens. Bioresour Technol 134:134–142
Foda MI, Lopez-Leiva M (2000) Continuous production of oligosaccharides from whey using a membrane reactor. Process Biochem 35:581–587
Silveira ST, Martinez-Maqueda D, Recio I, Hernandez-Ledesma B (2013) Dipeptidyl peptidase-IV inhibitory peptides generated by tryptic hydrolysis of a whey protein concentrate rich in β-lactoglobulin. Food Chem 141:1072–1077
Smithers GW (2008) Whey and whey proteins—from ‘gutter-to-gold’. Int Dairy J 18:695–704
Rastall RA, Gibson GR (2015) Recent developments in prebiotics to selectively impact beneficial microbes and promote intestinal health. Curr Opin Biotechnol 32:42–46
Slavin J (2013) Fiber and prebiotics: mechanisms and health benefits. Nutrients 5:1417–1435
Lehmann S, Hiller J, van Bergenhenegouwen J, Knippels LMJ, Garssen J, Traidl-Hoffmann C (2015) In vitro evidence for immune-modulatory properties of non-digestible oligosaccharides: direct effect on human monocyte derived dendritic cells. PLoS One 10:e0132304
Mussatto SI, Mancilha IM (2007) Non-digestible oligosaccharides: a review. Carbohyd polym 68:587–597
Nauta AJ, Garssen J (2013) Evidence-based benefits of specific mixtures of non-digestible oligosaccharides on the immune system. Carbohyd polym 93:263–265
Van Loo J, Cummings J, Delzenne N, Englyst H, Franck A, Hopkins M, Kok N, Macfarlane G, Newton D, Quigley M (1999) Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94-1095). Br J Nutr 8:121–132
Laparra JM, Diez-Municio M, Javier Moreno FHerrero M (2015) Kojibiose ameliorates arachidic acid-induced metabolic alterations in hyperglycaemic rats. Br J Nutr 114:1395–1402
Laparra JM, Diez-Municio M, Herrero M, Moreno FJ (2014) Structural differences of prebiotic oligosaccharides influence their capability to enhance iron absorption in deficient rats. Food Funct 5:2430–2437
Lee BH, Rose DR, Lin AH, Quezada-Calvillo R, Nichols BL, Hamaker BR (2016) Contribution of the individual small intestinal α-glucosidases to digestion of unusual α-linked glycemic disaccharides. J Agric Food Chem 64:6487–6494
Diez-Municio M, Montilla A, Jimeno ML, Corzo A, Olano N, Moreno FJ (2012) Synthesis and characterization of a potential prebiotic trisaccharide from cheese whey permeate and sucrose by Leuconostoc mesenteroides dextransucrase. J Agric Food Chem 60:1945–1953
Diez-Municio M, Montilla A, Moreno FJ, Herrero M (2014) A sustainable biotechnological process for the efficient synthesis of kojibiose. Green Chem 16:2219–2226
Purama RK, Goyal A (2008) Purified dextransucrase from Leuconostoc mesenteroides NRRL B640 exists as single homogeneous protein: analysis by nondenaturing native PAGE. Internet J Microbiol 6:1
Liu Z, Zhao C, Deng Y, Huang Y, Liu B (2015) Characterization of a thermostable recombinant β-galactosidase from a thermophilic anaerobic bacterial consortium YTY-70. Biotechnol Biotechnol Equip 29(3):547554
Naessens M, Cerdobbel A, Soetaert W, Vandamme EJ (2005) Leuconostoc dextransucrase and dextran: production, properties and applications. J Chem Technol Biotech 80:845–860
Smith TJ, Foegeding EA, Drake MA (2016) Flavor and functional characteristics of whey protein isolates from different whey sources. J Food Sci 4:849–857
Rahiman F, Pool EJ (2016) The effect of sugar cane molasses on the immune and male reproductive systems using in vitro and in vivo methods. Iran J Basic Med Sci 19:1125
Sharma M, Patel SN, Sangwan RS, Singh SP (2017) Biotransformation of banana pseudostem extract into a functional juice containing value added biomolecules of potential health benefits. Indian J Exp Biol 55:453–462
Vedamuthu ER (1994) The dairy Leuconostoc: use in dairy products. J Dairy Sci 77:2725–2737
Ogier JC, Casalta E, Farrokh C, Saihi A (2008) Safety assessment of dairy microorganisms: the Leuconostoc genus. Int J Food Microbiol 126:286–290
Shah HS, Patel CM, Parikh SC (2013) Production of invertase from bacteria by using waste jaggery. Microbes 3:19–23
Song Y, Nguyen QA, Wi SG, Yang J, Bae HJ (2017) Strategy for dual production of bioethanol and d-psicose as value-added products from cruciferous vegetable residue. Bioresour Technol 223:34–39
Stahel P, Kim JJ, Xiao C, Cant JP (2017) Of the milk sugars, galactose, but not prebiotic galacto-oligosaccharide, improves insulin sensitivity in male Sprague-Dawley rats. PLoS One 12:e0172260
He W, Mu W, Jiang B, Yan X, Zhang T (2016) Food-grade expression of d-psicose 3-epimerase with tandem repeat genes in Bacillus subtilis. J Agric Food Chem 64:5701–5707
Patel SN, Singh V, Sharma M, Sangwan RS, Singhal NK, Singh SP (2018) Development of a thermo-stable and recyclable magnetic nanobiocatalyst for bioprocessing of fruit processing residues and d-allulose synthesis. Bioresour Technol 247:633
Acknowledgements
The authors acknowledge the Department of Biotechnology (DBT), Government of India for facilitating the present work at Center of Innovative and Applied Bioprocessing (CIAB), Mohali, India. KL acknowledges Science and Engineering Research Board (SERB) for providing N-PDF fellowship (PDF/2016/000408). SPS acknowledges ECR/2016/001228 grant. The thematic disclosures herein are covered in Indian patent file no. 201711006155.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lata, K., Sharma, M., Patel, S.N. et al. An integrated bio-process for production of functional biomolecules utilizing raw and by-products from dairy and sugarcane industries. Bioprocess Biosyst Eng 41, 1121–1131 (2018). https://doi.org/10.1007/s00449-018-1941-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00449-018-1941-0