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Properties of recombinant 4-α-glucanotransferase from Bifidobacterium longum subsp. longum JCM 1217 and its application

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Abstract

To determine the physiochemical properties of the 4-α-glucanotransferase from Bifidobacterium sp., the bllj_0114 gene encoding 4-α-glucanotransferase was cloned from Bifidobacterium longum subsp. longum JCM 1217 and expressed in Escherichia coli. The amino acid sequence alignment indicated that the recombinant protein, named BL-αGTase, belongs to the glycoside hydrolase (GH) family 77. BL-αGTase was purified using nickel-nitrilotriacetic acid affinity chromatography and characterized using various substrates. The enzyme catalyzed the disproportionation activity, which transfers a glucosyl unit from oligosaccharides to acceptor molecules, and had the highest activity at 40 °C and pH 6.0. In the presence of 5 mM metal ions, in particular Cu2+, Zn2+, and Fe2+, BL-αGTase activity was reduced. To determine whether BL-αGTase can be used to generate thermoreversible gels, potato starch was treated with BL-αGTase for various reaction times. The BL-αGTase-treated starches showed sol–gel reversibility and melted at 59.6–75.7 °C.

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References

  • Arboleya S, Watkins C, Stanton C, Ross RP. Gut Bifidobacteria populations in human health and aging. Front. Microbiol. 7: 1-9 (2016)

    Article  CAS  Google Scholar 

  • Bhuiyan S, Kitaoka M, Hayashi K. A cycloamylose-forming hyperthermostable 4-α-glucanotransferase of Aquifex aeolicus expressed in Escherichia coli. J. Mol. Catal. B-Enzym 22: 45-53 (2003)

    Article  CAS  Google Scholar 

  • Do VH, Mun S, Kim YL, Rho SJ, Park KH, Kim YR. Novel formulation of low-fat spread using rice starch modified by 4-alpha-glucanotransferase. Food Chem. 208: 132-141 (2016)

    Article  CAS  Google Scholar 

  • Godany A, Vidova B, Janecek S. The unique glycoside hydrolase family 77 amylomaltase from Borrelia burgdorferi with only catalytic triad conserved. FEMS Microbiol. Lett. 284: 84-91 (2008)

    Article  CAS  Google Scholar 

  • Imamura H, Fushinobu S, Yamamoto M, Kumasaka T, Jeon BS, Wakagi T, Matsuzawa H. Crystal structures of 4-alpha-glucanotransferase from Thermococcus litoralis and its complex with an inhibitor. J. Biol. Chem. 278: 19378-19386 (2003)

    Article  CAS  Google Scholar 

  • Janer C, Arigoni F, Lee BH, Pelaez C, Requena T. Enzymatic ability of Bifidobacterium animalis subsp. lactis to hydrolyze milk proteins: identification and characterization of endopeptidase O. Appl. Environ. Microb. 71: 8460-8465 (2005)

  • Kaper T, Talik B, Ettema TJ, Bos H, van der Maarel MJ, Dijkhuizen L. Amylomaltase of Pyrobaculum aerophilum IM2 produces thermoreversible starch gels. Appl. Environ. Microb. 71: 5098-5106 (2005)

    Article  CAS  Google Scholar 

  • Kaper T, van der Maarel MJ, Euverink GJ, Dijkhuizen L. Exploring and exploiting starch-modifying amylomaltases from thermophiles. Biochem. Soc. Trans. 32: 279-282 (2004)

    Article  CAS  Google Scholar 

  • Kim MS, Jang JH, Kim YW. Overproduction of a thermostable 4-alpha-glucanotransferase by codon optimization at N-terminus region. J. Sci. Food Agr. 93: 2683-2690 (2013)

    Article  CAS  Google Scholar 

  • Kim NR, Jeong DW, Ko DS, Shim JH. Characterization of novel thermophilic alpha-glucosidase from Bifidobacterium longum. Int. J. Biol. Macromol. 99: 594-599 (2017)

    Article  CAS  Google Scholar 

  • Kuchtová A, Janeček Š. In silico analysis of family GH77 with focus on amylomaltases from Borreliae and disproportionating enzymes DPE2 from plants and bacteria. Biochim. Biophys. Acta 1854: 1260-1268 (2015)

    Article  Google Scholar 

  • Kwak JY, Kim MG, Kim YW, Ban HS, Won MS, Park JT, Park KH. Properties of a glycogen like polysaccharide produced by a mutant of Escherichia coli lacking glycogen synthase and maltodextrin phosphorylase. Carbohyd. Polym. 136: 649-655 (2016)

    Article  CAS  Google Scholar 

  • Lee HS, Auh JH, Yoon HG, Kim MJ, Park JH, Hong SS, Kang MH, Kim TJ, Moon TW, Kim JW, Park KH. Cooperative action of alpha-glucanotransferase and maltogenic amylase for an improved process of isomaltooligosaccharide (IMO) production. J. Agric. Food Chem. 50: 2812-2817 (2002)

    Article  CAS  Google Scholar 

  • Lee JH, O’Sullivan DJ. Genomic insights into bifidobacteria. MMBR 74: 378-416 (2010)

    CAS  PubMed  Google Scholar 

  • Lee KY, Kim YR, Park KH, Lee HG. Rheological and gelation properties of rice starch modified with 4-alpha-glucanotransferase. Int. J. Biol. Macromol. 42: 298-304 (2008a)

    Article  CAS  Google Scholar 

  • Lee SH, Choi SJ, Shin SI, Park KH. Structural and rheological properties of sweet potato starch modified with 4-α-Glucanotransferase from Thermus aquaticus. Food Sci. Biotechnol. 17: 705-712 (2008b)

    CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42: D490-D495 (2014)

    Article  CAS  Google Scholar 

  • Machovič M, Janeček S. The invariant residues in the α-amylase family: just the catalytic triad. Biologia 58: 1127-1132 (2003)

    Google Scholar 

  • Mua J, Jackson, D. Relationships between functional attributes andmolecular structures of amylose and amylopectin fractions from corn starch. J. Agr. Food Chem. 45: 3848-3854 (1997)

    Article  CAS  Google Scholar 

  • Nguyen DHD, Park SH, Tran PL, Kim JW, Le QT, Boos W, Park JT. Characterization of the transglycosylation reaction of 4-alpha-glucanotransferase (MalQ) and its role in glycogen breakdown in Escherichia coli. J. Microbiol. Biotechnol. 29: 357-366 (2019)

    Article  Google Scholar 

  • Palmer TN, Ryman BE, Whelan WJ. The action pattern of amylomaltase from Escherichia coli. Eur. J. Biochem. 69: 105-115 (1976)

    Article  CAS  Google Scholar 

  • Park JH, Kim HJ, Kim YH, Cha HJ, Kim YW, Kim TJ, Kim YR, Park KH. The action mode of Thermus aquaticus YT-1 4-α-glucanotransferase and its chimeric enzymes introduced with starch-binding domain on amylose and amylopectin. Carbohydr. polym. 67: 164-173 (2007)

    Article  CAS  Google Scholar 

  • Takaha T, Yanase M, Okada S, Smith SM. Disproportionating enzyme (4-alpha-glucanotransferase; EC 2.4.1.25) of potato. purification, molecular cloning, and potential role in starch metabolism. J. Biol. Chem. 268: 1391-1396 (1993)

  • Takaha T, Yanase M, Takata H, Okada S, Smith SM. Potato D-enzyme catalyzes the cyclization of amylose to produce cycloamylose, a novel cyclic glucan. J. Biol. Chem. 271: 2902-2908 (1996)

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30: 2725-2729 (2013)

  • Tang SY, Yang SJ, Cha H, Woo EJ, Park C, Park KH. Contribution of W229 to the transglycosylation activity of 4-alpha-glucanotransferase from Pyrococcus furiosus. Biochim. Biophys. Acta 1764: 1633-1638 (2006)

    Article  CAS  Google Scholar 

  • Terada Y, Fujii K, Takaha T, Okada S. Thermus aquaticus ATCC 33923 amylomaltase gene cloning and expression and enzyme characterization: Production of cycloamylose. Appl. Environ. Microbiol. 65: 910-915 (1999)

    Article  CAS  Google Scholar 

  • Tomsic M, Prossnigg F, Glatter O. A thermoreversible double gel: characterization of a methylcellulose and kappa-carrageenan mixed system in water by SAXS, DSC and rheology. J. Colloid Interf. Sci. 322: 41-50 (2008)

    Article  CAS  Google Scholar 

  • van der Maarel MJ, Leemhuis H. Starch modification with microbial alpha-glucanotransferase enzymes. Carbohydr. Polym. 93: 116-121 (2013)

    Article  Google Scholar 

  • Wang H, Lee IS, Braun C, Enck P. Effect of probiotics on central nervous system functions in animals and humans: A systematic review. J. Neurogastroenterol. Motil. 22: 589-605 (2016)

    Article  Google Scholar 

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Acknowledgements

This study was supported by Hallym Research Fund (HRF-201905-005).

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  1. Department of Food Science and Nutrition, and The Korean Institute of Nutrition, Hallym University, Chuncheon, 24252, Republic of Korea

    Da-Woon Jeong, Hyun-Mo Jeong, Yu-Jeong Shin, Seung-Hye Woo & Jae-Hoon Shim

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  1. Da-Woon Jeong
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  2. Hyun-Mo Jeong
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  3. Yu-Jeong Shin
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  5. Jae-Hoon Shim
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Jeong, DW., Jeong, HM., Shin, YJ. et al. Properties of recombinant 4-α-glucanotransferase from Bifidobacterium longum subsp. longum JCM 1217 and its application. Food Sci Biotechnol 29, 667–674 (2020). https://doi.org/10.1007/s10068-019-00707-4

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  • DOI: https://doi.org/10.1007/s10068-019-00707-4

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