Glucansucrase (mutant) enzymes from Lactobacillus reuteri 180 efficiently transglucosylate Stevia component rebaudioside A, resulting in a superior taste

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Te Poele, Evelien M ^a,e   Devlamynck, Tim ^a,b   Jäger, Manuel ^c   Gerwig, Gerrit J ^a,d   Van De Walle, Davy ^b   Dewettinck, Koen ^b   Hirsch, Anna K H ^c   Kamerling, Johannis P ^a,d   Soetaert, Wim ^b   Dijkhuizen, Lubbert ^a,e  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

^e CarbExplore Research BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNANSUCRASE; GLYCOSYLTRANSFERASE; KAURANE DERIVATIVE; MUTANT PROTEIN; REBAUDIOSIDE A; SUCROSE; SWEETENING AGENT;

CHEMISTRY; ENZYMOLOGY; GENETICS; GLYCOSYLATION; LACTOBACILLUS REUTERI; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; MISSENSE MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; TASTE;

DITERPENES, KAURANE; GLYCOSYLATION; GLYCOSYLTRANSFERASES; LACTOBACILLUS REUTERI; MAGNETIC RESONANCE SPECTROSCOPY; MUTANT PROTEINS; MUTATION, MISSENSE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUCROSE; SWEETENING AGENTS; TASTE;

EID: 85041090800     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-19622-5     Document Type: Article

References (49)

1. Hellfritsch, C., Brockhoff, A., Stähler, F., Meyerhof, W. & Hofmann, T. Human psychometric and taste receptor responses to steviol glycosides. J. Agric. Food Chem. 60, 6782-6793 (2012).
2. Geuns, J. M. C. Stevioside. Phytochemistry 64, 913-921 (2003).
3. Goyal, S. K., Samsher & Goyal, R. K. Stevia (Stevia rebaudiana) a bio-sweetener: a review. Int. J. Food Sci. Nutr. 61, 1-10 (2010).
4. Puri, M., Sharma, D. & Tiwari, A. K. Downstream processing of stevioside and its potential applications. Biotechnol. Adv. 29, 781-791 (2011).
5. DuBois, G. E. & Prakash, I. Non-caloric sweeteners, sweetness modulators, and sweetener enhancers. Annu. Rev. Food Sci. Technol. 3, 353-380 (2012).
6. Yadav, S. K. & Guleria, P. Steviol glycosides from Stevia: biosynthesis pathway review and their application in foods and medicine. Crit. Rev. Food Sci. Nutr. 52, 988-998 (2012).
7. Brandle, J. E., Starratt, A. N. & Gijzen, M. Stevia rebaudiana: Its agricultural, biological, and chemical properties. Can. J. Plant Sci. 78, 527-536 (1998).
8. Ceunen, S. & Geuns, J. M. C. Steviol glycosides: chemical diversity, metabolism, and function. J. Nat. Prod. 76, 1201-1228 (2013).
9. Commission Regulation (EU) No 1131/2011. Off. J. Eur. Union L295, 205-211 (2011).
10. Risso, D. et al. Genetic signature of differential sensitivity to stevioside in the Italian population. Genes Nutr. 9, 401 (2014).
11. Wolwer-Rieck, U. The leaves of Stevia rebaudiana (Bertoni), their constituents and the analyses thereof: a review. J. Agric. Food Chem. 60, 886-895 (2012).
12. Darise, M. et al. Enzymic transglucosylation of rubusoside and the structure-sweetness relationship of steviol-bisglycosides. Agric. Biol. Chem. 48, 2483-2488 (1984).
13. Li, X. et al. Human receptors for sweet and umami taste. Proc. Natl. Acad. Sci. USA 99, 4692-4696 (2002).
14. Nelson, G. et al. Mammalian sweet taste receptors. Cell 106, 381-390 (2001).
15. Gerwig, G. J., te Poele, E. M., Dijkhuizen, L. & Kamerling, J. P. Stevia glycosides: chemical and enzymatic modifications of their carbohydrate moieties to improve the sweet-tasting quality. Adv. Carbohydr. Chem. Biochem. 73, 1-72 (2016).
16. Abelyan, V. A., Balayan, A. M., Ghochikyan, V. T. & Markosyan, A. A. Transglycosylation of stevioside by cyclodextrin glucanotransferases of various groups of microorganisms. Appl. Biochem. Microbiol. 40, 129-134 (2004).
17. Fukunaga, Y. et al. Enzymic transglucosylation products of stevioside: separation and sweetness-evaluation. Agric. Biol. Chem. 53, 1603-1607 (1989).
18. Ohtani, K. et al. Further study on the 1,4-α-transglucosylation of rubusoside, a sweet steviol-bisglucoside from Rubus suavissimus. Agric. Biol. Chem. 55, 449-453 (1991).
19. Ohtani, K. et al. Solubilization of steviolbioside and steviolmonoside with γ-cyclodextrin and its application to selective syntheses of better sweet glycosides from stevioside and rubusoside. Chem. Pharm. Bull. (Tokyo) 39, 3172-3174 (1991).
20. Lobov, S. V., Kasai, R., Ohtani, K., Tanaka, O. & Yamasaki, K. Enzymic production of sweet stevioside derivatives: transglucosylation by glucosidases. Agric. Biol. Chem. 55, 2959-2965 (1991).
21. Monsan, P., Remaud-Simeon, M. & Andre, I. Transglucosidases as efficient tools for oligosaccharide and glucoconjugate synthesis. Curr. Opin. Microbiol. 13, 293-300 (2010).
22. Leemhuis, H. et al. Glucansucrases: three-dimensional structures, reactions, mechanism, α-glucan analysis and their implications in biotechnology and food applications. J. Biotechnol. 163, 250-272 (2013).
23. Gerwig, G. J., te Poele, E. M., Dijkhuizen, L. & Kamerling, J. P. Structural analysis of rebaudioside A derivatives obtained by Lactobacillus reuteri 180 glucansucrase-catalyzed trans-α-glucosylation. Carbohydr. Res. 440-441, 51-62 (2017).
24. Vujičić-Žagar, A. et al. Crystal structure of a 117 kDa glucansucrase fragment provides insight into evolution and product specificity of GH70 enzymes. Proc. Natl. Acad. Sci. USA 107, 21406-21411 (2010).
25. Meng, X., Pijning, T., Dobruchowska, J. M., Gerwig, G. J. & Dijkhuizen, L. Characterization of the functional roles of amino acid residues in acceptor binding subsite +1 in the active site of the glucansucrase GTF180 enzyme of Lactobacillus reuteri 180. J. Biol. Chem. 290, 30131-30141 (2015).
26. Meng, X. et al. Characterization of the glucansucrase GTF180 W1065 mutant enzymes producing polysaccharides and oligosaccharides with altered linkage composition. Food Chem. 217, 81-90 (2017).
27. van Leeuwen, S. S. et al. Structural characterization of bioengineered α-D-glucans produced by mutant glucansucrase GTF180 enzymes of Lactobacillus reuteri strain 180. Biomacromolecules 10, 580-588 (2009).
28. Prakash, I., DuBois, G. E., Clos, J. F., Wilkens, K. L. & Fosdick, L. E. Development of Rebiana, a natural, non-caloric sweetener. Food Chem. Toxicol. 46, S75-S82 (2008).
29. LeadIT version 2.1.8. (2014). BioSolveIT GmbH. www.biosolveit.de/LeadIT/
30. Upreti, M., Smit, J. P., Hagen, E. J., Smolenskaya, V. N. & Prakash, I. Single crystal growth and structure determination of the natural 'high potency' sweetener Rebaudioside A. Cryst. Growth Des. 12, 990-993 (2012).
31. Kralj, S. et al. Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 150, 3681-3690 (2004).
32. Meng, X. et al. Truncation of domain V of the multidomain glucansucrase GTF180 of Lactobacillus reuteri 180 heavily impairs its polysaccharide-synthesizing ability. Appl. Microbiol. Biotechnol. 99, 5885-5894 (2015).
33. Meng, X., Dobruchowska, J. M., Pijning, T., Gerwig, G. J. & Dijkhuizen, L. Synthesis of new hyperbranched α-glucans from sucrose by Lactobacillus reuteri 180 glucansucrase mutants. J. Agric. Food Chem. 64, 433-442 (2016).
34. Meng, X. et al. Residue Leu940 has a crucial role in the linkage and reaction specificity of the glucansucrase GTF180 of the probiotic bacterium Lactobacillus reuteri 180. J. Biol. Chem. 289, 32773-32782 (2014).
35. van Leeuwen, S. S., Kralj, S., Gerwig, G. J., Dijkhuizen, L. & Kamerling, J. P. Structural analysis of bioengineered α-D-glucan produced by a triple mutant of the glucansucrase GTF180 enzyme from Lactobacillus reuteri strain 180: generation of (α1 → 4) linkages in a native (1 → 3)(1 → 6)-α-D-glucan. Biomacromolecules 9, 2251-2258 (2008).
36. Mayer, R. M., Matthews, M. M., Futerman, C. L., Parnaik, V. K. & Jung, S. M. Dextransucrase: acceptor substrate reactions. Arch. Biochem. Biophys. 208, 278-287 (1981).
37. Van Geel-Schutten, G. H. et al. Biochemical and structural characterization of the glucan and fructan exopolysaccharides synthesized by the Lactobacillus reuteri wild-type strain and by mutant strains. Appl. Environ. Microbiol. 65, 3008-3014 (1999).
38. Box, G. E. P. & Wilson, K. B. On the experimental attainment of optimum conditions. J. Roy. Stat. Soc. Ser. B13, 1-45 (1951).
39. Box, G. E. P. & Behnken, D. W. Some new three level designs for the study of quantitative variables. Technometrics 2, 455-475 (1960).
40. JMPR version 12 (1989-2007). SAS Institute Inc., Cary, NC, www.jmp.com/.
41. SeeSAR version 3.3. (2015) BioSolveIT GmbH. www.biosolveit.de/SeeSAR/.
42. PyMOL version 1.6.x (2013) Schrodinger, L. The PyMOL Molecular Graphics System. www.schrodinger.com/pymol.
43. Damasio, M. H. & Costell, E. Analisis sensorial descriptivo: generacion de descriptores y seleccion de catadores. Rev. Agroquim. Y Tecnol. Aliment. 31, 165-178 (1991).
44. Amerine, M. A., Pangborn, R. M. & Roessler, E. B. Principles of Sensory Evaluation of Food. (Academic Press, 1965).
45. Schiffman, S. S., Sattely-Miller, E. A. & Bishay, I. E. Time to maximum sweetness intensity of binary and ternary blends of sweeteners. Food Qual. Prefer. 18, 405-415 (2007).
46. Jamieson, P. The sugarfree toolbox-bulk ingredients and intense sweeteners. Manuf. Confect. 88, 33-46 (2008).
47. Fujimaru, T., Park, J.-H. & Lim, J. Sensory characteristics and relative sweetness of tagatose and other sweeteners. J. Food Sci. 77, S323-S328 (2012).
48. Tukey, J. W. The problem of multiple comparisons. Princeton University. (1953).
49. Games, P. & Howell, J. Pairwise multiple comparison procedures with unequal N's and/or variances: a Monte Carlo study. J. Educ. Stat. 1, 113-125 (1976).