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In vitro prebiotic potential, digestibility and biocompatibility properties of laminari-oligosaccharides produced from curdlan by β-1,3-endoglucanase from Clostridium thermocellum

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Abstract

Curdlan or laminarin, a β-1,3-glucan was hydrolysed by β-1,3-endoglucanase (CtLam81A) from Clostridium thermocellum to produce laminari-oligosaccharides. TLC analysis of hydrolysed curdlan showed the presence of laminari-oligosaccharides of the degree of polymerization, DP2-DP7. This mixture of laminari-oligosaccharides displayed prebiotic properties. Laminari-oligosaccharides showed an increase in the growth of probiotic bacteria such as Lactobacillus plantarum DM5 and Lactobacillus acidophilus, while they did not promote the growth of non-probiotic bacteria (Escherichia coli and Enterobacter aerogenes). Laminari-oligosaccharides showed higher prebiotic activity score of 0.92 ± 0.01 and 0.64 ± 0.08 for L. plantarum DM5 and L. acidophilus NRRL B-4496, respectively, similar to those shown by inulin. Laminari-oligosaccharides showed higher resistance or low digestibility against α-amylase, artificial gastric juice and intestinal fluid than inulin indicating their bioavailability to the probiotic bacteria present in the gastrointestinal tract of human. The probiotic bacteria consumed laminaribiose and laminariotriose more readily than higher laminari-oligosaccharides as carbon source for their growth. The in vitro cytotoxicity assay of laminari-oligosaccharides (1 mg/ml) on human embryonic kidney (HEK 293) cells showed that the cell viability was not affected even after 72 h indicating their biocompatible nature. All the results amply indicated that laminari-oligosaccharides can serve as potential prebiotic additives for functional food products.

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References

  • Akramiene D, Kondrotas A, Didziapetriene J, Kevelaitis E (2006) Effects of beta-glucans on the immune system. Medicina (Kaunas, Lithuania) 43:597–606

    Article  Google Scholar 

  • Al-Sheraji SH, Ismail A, Manap MY, Mustafa S, Yusof RM, Hassan FA (2012) Fermentation and non-digestibility of Mangifera pajang fibrous pulp and its polysaccharides. J Funct Foods 4:933–940

    Article  CAS  Google Scholar 

  • Asadi M, Fayazi S, Adarvishi S, Alavinejad P, Latifi M, Soleimani A (2016) The effect of benson relaxation on quality of life of patients with irritable bowel syndrome. Jundishapur J Chron Dis Care 5(4):e31068

    Google Scholar 

  • Baruah R, Maina NH, Katina K, Juvonen R, Goyal A (2017) Functional food applications of dextran from Weissella cibaria RBA12 from pummelo (Citrus maxima). Int J Food Microbiol 242:124–131

    Article  CAS  PubMed  Google Scholar 

  • Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72:3593–3599

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chakraborty S, Rani A, Goyal A (2018) Pectic oligosaccharides produced from pectin extracted from waste peels of Citrus limetta using recombinant endo-pectate lyase (PL1B) inhibit colon cancer cells. Trends Carbo Res 10:25–34

    CAS  Google Scholar 

  • Chapla D, Pandit P, Shah A (2012) Production of xylooligosaccharides from corncob xylan by fungal xylanase and their utilization by probiotics. Bioresour Technol 115:215–221

    Article  CAS  PubMed  Google Scholar 

  • Das D, Goyal A (2014) Potential probiotic attributes and antagonistic activity of an indigenous isolate Lactobacillus plantarum DM5 from an ethnic fermented beverage “Marcha” of North Eastern Himalayas. Int J Food Sci Nutr 65:335–344

    Article  PubMed  Google Scholar 

  • Das D, Baruah R, Goyal A (2014) A food additive with prebiotic properties of an α-d-glucan from Lactobacillus plantarum DM5. Int J Biol Macromol 69:20–26

    Article  CAS  PubMed  Google Scholar 

  • Delzenne NM, Neyrinck AM, Bäckhed F, Cani PD (2011) Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7:639

    Article  CAS  PubMed  Google Scholar 

  • Devillé C, Gharbi M, Dandrifosse G, Peulen O (2007) Study on the effects of laminarin, a polysaccharide from seaweed, on gut characteristics. J Sci Food Agric 87:1717–1725

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Fernandez MF, Boris S, Barbes C (2003) Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract. J Appl Microbiol 94:449–455

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Yin H, Wang W, Wang M, Zhang H, Zhao X, Du Y (2011) β-1, 3-Glucan with different degree of polymerization induced different defense responses in tobacco. Carbohydr Polym 86:774–782

    Article  CAS  Google Scholar 

  • Ghosh A, Verma AK, Tingirikari JR, Shukla R, Goyal A (2015) Recovery and purification of oligosaccharides from copra meal by recombinant endo-β-mannanase and deciphering molecular mechanism involved and its role as potent therapeutic agent. Mol Biotechnol 57:111–127

    Article  CAS  PubMed  Google Scholar 

  • Huebner J, Wehling RL, Hutkins RW (2007) Functional activity of commercial prebiotics. Int Dairy J 17:770–775

    Article  CAS  Google Scholar 

  • Jacobs DM, Gaudier E, Van Duynhoven J, Vaughan EE (2009) Non-digestible food ingredients, colonic microbiota and the impact on gut health and immunity: arole for metabolomics. Curr Drug Metab 10:41–54

    Article  CAS  PubMed  Google Scholar 

  • Jamois F, Ferrières V, Guégan JP, Yvin JC, Plusquellec D, Vetvicka V (2005) Glucan-like synthetic oligosaccharides: iterative synthesis of linear oligo-β-(1, 3)-glucans and immunostimulatory effects. Glycobiology 15:393–407

    Article  CAS  PubMed  Google Scholar 

  • Kerry RG, Patra JK, Gouda S, Park Y, Shin H-S, Das G (2018) Benefaction of probiotics for human health: A review. J Food Drug Analysis 26:927–939

    Article  CAS  Google Scholar 

  • Khangwal I, Shukla P (2019) Potential prebiotics and their transmission mechanisms: Recent approaches. J Food Drug Anal 27:649–656

    Article  PubMed  Google Scholar 

  • Kimura I, Inoue D, Maeda T, Hara T, Ichimura A, Miyauchi S, Tsujimoto G (2011) Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc Natl Aacd Sci 108:8030–8035

    Article  CAS  Google Scholar 

  • Klarzynski O, Plesse B, Yvin JCM, Kopp M, Kloareg B, Fritig B (2000) Linear β-1, 3 glucans are elicitors of defense responses in tobacco. Plant Physiol 124:1027–1038

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Korakli M, Gänzle MG, Vogel RF (2002) Metabolism by bifidobacteria and lactic acid bacteria of polysaccharides from wheat and rye, and exopolysaccharides produced by Lactobacillus sanfranciscensis. J Appl Microbiol 92:958–965

    Article  CAS  PubMed  Google Scholar 

  • Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F (2016) From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165:1332–1345

    Article  CAS  PubMed  Google Scholar 

  • Kothari D, Goyal A (2015) Gentio-oligosaccharides from Leuconostoc mesenteroides NRRL B-1426 dextransucrase as prebiotics and as a supplement for functional foods with anti-cancer properties. Food Funct 6:604–611

    Article  CAS  PubMed  Google Scholar 

  • Kuda T, Yano T, Matsuda N, Nishizawa M (2005) Inhibitory effects of laminarin and low molecular alginate against the putrefactive compounds produced by intestinal microflora in vitro and in rats. Food Chem 91:745–749

    Article  CAS  Google Scholar 

  • Kumar M, Nagpal R, Kumar R, Hemalatha R, Verma V, Kumar A, Yadav H (2012) Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp Diabetes Res. https://doi.org/10.1155/2012/902917

    Article  PubMed Central  PubMed  Google Scholar 

  • Kumar K, Correia MA, Pires VM, Dhillon A, Sharma K, Rajulapati V, Goyal A (2018) Novel insights into the degradation of β-1, 3-glucans by the cellulosome of Clostridium thermocellum revealed by structure and function studies of a family 81 glycoside hydrolase. Int J Biol Macromol 117:890–901

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Arai CT, Ibrahim D, Kosugi A, Prawitwong P, Lan D, Mori Y (2014) Purification and characterization of a thermostable laminarinase from Penicillium rolfsii c3–2 (1) IBRL. BioResources 9:1072–1084

    Google Scholar 

  • Mano MCR, Neri-Numa IA, da Silva JB, Paulino BN, Pessoa MG, Pastore GM (2018) Oligosaccharide biotechnology: an approach of prebiotic revolution on the industry. Appl Microbiol Biotechnol 102:17–37

    Article  CAS  PubMed  Google Scholar 

  • Miyanishi N, Iwamoto Y, Watanabe E, Odaz T (2003) Induction of TNF-α production from human peripheral blood monocytes with β-1, 3-glucan oligomer prepared from laminarin with β-1, 3-glucanase from Bacillus clausii NM-1. J Biosci Bioeng 95(2):192–195

    Article  CAS  PubMed  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  CAS  PubMed  Google Scholar 

  • Mueller M, Reiner J, Fleischhacker L, Viernstein H, Loeppert R, Praznik W (2016) Growth of selected probiotic strains with fructans from different sources relating to degree of polymerization and structure. J Funct Foods 24:264–275

    Article  CAS  Google Scholar 

  • Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    CAS  Google Scholar 

  • O’Doherty JV, McDonnell P, Figat S (2010) The effect of dietary laminarin and fucoidan in the diet of the weanling piglet on performance and selected faecal microbial populations. Livest Sci 134:208–210

    Article  Google Scholar 

  • Pandey KR, Naik SR, Vakil BV (2015) Probiotics, prebiotics and synbiotics-a review. J Food Sci Technol 52:7577–7587

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roberfroid M, Gibson G, Hoyles L, McCartney A, Rastall R, Rowland I (2010) Prebiotic effects: metabolic and health benefits. Br J Nutr 104:S1–S63

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Liu J, Yan Q, You X, Yang S, Jiang Z (2018) In vitro digestibility and prebiotic potential of curdlan (1→3)-β-D-glucan oligosaccharides in Lactobacillus species. Carbohydr Polym 188:17–26

    Article  CAS  PubMed  Google Scholar 

  • Shimizu J, Tsuchisashi N, Kudoh K, Wada M, Tarika T, Innami S (2001) Dietary curdlan increases proliferation of bifidobacteria in the cecum of rats. Biosci Biotechnol Biochem 65:466–469

    Article  CAS  PubMed  Google Scholar 

  • Somogyi M (1945) Determination of blood sugar. J Biol Chem 160:69–73

    CAS  Google Scholar 

  • Spicer EJ, Goldenthal EI, Ikeda T (1999) A toxicological assessment of curdlan. Food Chem Toxicol 37:455–479

    Article  CAS  PubMed  Google Scholar 

  • Swennen K, Courtin CM, Delcour JA (2006) Non-digestible oligosaccharides with prebiotic properties. Crit Rev Food Sci Nutr 46(6):459–471

    Article  CAS  PubMed  Google Scholar 

  • Volman JJ, Ramakers JD, Plat J (2008) Dietary modulation of immune function by β-glucans. Physiol Behav 94:276–284

    Article  CAS  PubMed  Google Scholar 

  • Tingirikari JMR, Kothari D, Goyal A (2014) Superior prebiotic and physicochemical properties of novel dextran from Weissella cibaria JAG8 for potential food applications. Food funct 5:2324–2330

    Article  CAS  PubMed  Google Scholar 

  • Wichienchot S, Prasertsan P, Hongpattarakere T, Gibson GR, Rastall RA (2006) In vitro fermentation of mixed linkage gluco-oligosaccharides produced by Gluconobacter oxydans NCIMB 4943 by the human colonic microflora. Curr Issues Intest Microbiol 7:7–12

    CAS  PubMed  Google Scholar 

  • Wichienchot S, Jatupornpipat M, Rastall RA (2010) Oligosaccharides of Pitaya (dragon fruit) flesh and their prebiotic properties. Food Chem 120:850–857

    Article  CAS  Google Scholar 

  • Wong JMW, de Souza R, Kendall CWC, Emam A, Jenkins DJA (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40:235–243

    Article  CAS  PubMed  Google Scholar 

  • Xiao M, Jiang MF, Wu K, Yang H, Ni XW, Yan WL (2017) Investigation on curdlan dissociation by heating in water. Food Hydrocoll 70:57–64

    Article  CAS  Google Scholar 

  • Xu LX, Zhang JF (2016) Bacterial glucans: Production, properties, and applications. Appl Microbiol Biotechnol 100:9023–9036

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Hu H, Wang L, Liu F, Pan S (2018) Preparation and prebiotic potential of pectin oligosaccharides obtained from citrus peel pectin. Food Chem 244:232–237

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to Departmental Central Instrument Facility, Biosciences and Bioengineering, IIT Guwahati for providing the cell culture facility.

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Authors and Affiliations

  1. Carbohydrate Enzyme Biotechnology Laboratory, Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati, Guwahati, Assam, 781039, India

    Krishan Kumar, Vikky Rajulapati & Arun Goyal

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  1. Krishan Kumar
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  2. Vikky Rajulapati
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  3. Arun Goyal
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Contributions

AG conceived the idea and designed the objectives. KK performed the prebiotic evaluation of laminarioligosaccharides and VR performed in vitro biocompatibility study. AG, KK and VR wrote the paper.

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Correspondence to Arun Goyal.

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Kumar, K., Rajulapati, V. & Goyal, A. In vitro prebiotic potential, digestibility and biocompatibility properties of laminari-oligosaccharides produced from curdlan by β-1,3-endoglucanase from Clostridium thermocellum. 3 Biotech 10, 241 (2020). https://doi.org/10.1007/s13205-020-02234-0

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