Biochemical characterization of the Lactobacillus reuteri glycoside hydrolase family 70 GTFB type of 4,6-α-glucanotransferase enzymes that synthesize soluble dietary starch fibers

Applied and Environmental Microbiology

Volumn 81, Issue 20, 2015, Pages 7223-7232

  Bai, Yuxiang ^a,b   van der Kaaij, Rachel Maria ^a   Leemhuis, Hans ^a,c   Pijning, Tjaard ^a   Leeuwen, Sander Sebastiaan van ^a   Jin, Zhengyu ^b   Dijkhuizen, Lubbert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b JIANGNAN UNIVERSITY   (China)

^c AVEBE UA   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; ENZYMES; ESCHERICHIA COLI; HYDROLASES; NUCLEAR MAGNETIC RESONANCE; STARCH; SUGARS;

BIOCHEMICAL CHARACTERIZATION; BIOCHEMICAL PROPERTIES; GLYCOSIDE HYDROLASES; HIGH SUBSTRATE CONCENTRATIONS; LACTOBACILLUS REUTERI; N-TERMINAL TRUNCATION; NUCLEAR MAGNETIC RESONANCE(NMR); SUBSTRATE SPECIFICITY;

BIOCHEMICAL ENGINEERING;

ENZYME ACTIVITY; HYDROLYSIS; MICROBIAL ACTIVITY; NUCLEAR MAGNETIC RESONANCE; POLYSACCHARIDE; PROTEIN; STARCH;

ESCHERICHIA COLI; LACTOBACILLUS REUTERI;

BACTERIAL PROTEIN; GLUCOSYLTRANSFERASE; STARCH;

BIOSYNTHESIS; ENZYMOLOGY; LACTOBACILLUS REUTERI; METABOLISM;

BACTERIAL PROTEINS; GLUCOSYLTRANSFERASES; LACTOBACILLUS REUTERI; STARCH;

EID: 84943327444     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01860-15     Document Type: Article

References (49)

1. Singh N, Singh J, Kaur L, Sodhi NS, Gill BS. 2003. Morphological, thermal and rheological properties of starches from different botanical sources. Food Chem 81:219-231. http://dx.doi.org/10.1016/S0308-8146(02)00416-8.
2. Tester RF, Karkalas J, Qi X. 2004. Starch-composition, fine structure and architecture. J Cereal Sci 39:151-165. http://dx.doi.org/10.1016/j.jcs.2003.12.001.
3. Singh J, Kaur L, McCarthy OJ. 2007. Factors influencing the physicochemical, morphological, thermal and rheological properties of some chemically modified starches for food applications-a review. Food Hydrocolloid 21:1-22. http://dx.doi.org/10.1016/j.foodhyd.2006.02.006.
4. Guzman-Maldonado H, Paredes-Lopez O, Biliaderis CG. 1995. Amylolytic enzymes and products derived from starch-a review. Crit Rev Food Sci 35:373-403. http://dx.doi.org/10.1080/10408399509527706.
5. van der Maarel MJEC, Leemhuis H. 2013. Starch modification with microbial α-glucanotransferase enzymes. Carbohydr Polym 93:116-121. http://dx.doi.org/10.1016/j.carbpol.2012.01.065.
6. van der Maarel MJEC, van der Veen B, Uitdehaag JCM, Leemhuis H, Dijkhuizen L. 2002. Properties and applications of starch-converting enzymes of the α-amylase family. J Biotechnol 94:137-155. http://dx.doi.org/10.1016/S0168-1656(01)00407-2.
7. Ludwig DDS. 2002. The glycemic index-physiological mechanisms relating to obesity, diabetes, and cardiovascular disease. JAMA 287:2414-2423. http://dx.doi.org/10.1001/jama.287.18.2414.
8. Lattimer JM, Haub MD. 2010. Effects of dietary fiber and its components on metabolic health. Nutrients 2:1266-1289. http://dx.doi.org/10.3390/nu2121266.
9. Guraya HS, James C, Champagne ET. 2001. Effect of enzyme concentration and storage temperature on the formation of slowly digestible starch from cooked debranched rice starch. Starke 53:131-139. http://dx.doi.org/10.1002/1521-379X(200104)53:3/4<131::AID-STAR131>3.0.CO;2-M.
10. Shin SI, Kim HJ, Ha HJ, Lee SH, Moon TW. 2005. Effect of hydrothermal treatment on formation and structural characteristics of slowly digestible non-pasted granular sweet potato starch. Starke 57:421-430. http://dx.doi.org/10.1002/star.200400377.
11. Lee BH, Nichols BL, Hamaker BR. 2013. Enzyme-synthesized highly branched maltodextrins have slow glucogenesis at the mucosal α-glucosidase level and are slowly digestible in vivo. PLoS One 2013:e59745. http://dx.doi.org/10.1371/journal.pone.0059745.
12. Kittisuban P, Lee BH, Suphantharika M, Hamaker BR. 2014. Slow glucose release property of enzyme-synthesized highly branched maltodextrins differs among starch sources. Carbohyd Polym 107:182-191. http://dx.doi.org/10.1016/j.carbpol.2014.02.033.
13. Le QT, Lee CK, Kim YW, Lee SJ, Zhang R, Withers SG, Kim YR, Auh JH, Park KH. 2009. Amylolytically-resistant tapioca starch modified by combined treatment of branching enzyme and maltogenic amylase. Carbohyd Polym 75:9-14. http://dx.doi.org/10.1016/j.carbpol.2008.06.001.
14. Lee CK, Le QT, Kim YH, Shim JH, Lee SJ, Park JH, Lee KP, Song SH, Auh JH, Lee SJ, Park KH. 2008. Enzymatic synthesis and properties of highly branched rice starch amylose and amylopectin cluster. J Agric Food Chem 56:126-131. http://dx.doi.org/10.1021/jf072508s.
15. Dobruchowska JM, Gerwig GJ, Kralj S, Grijpstra P, Leemhuis H, Dijkhuizen L, Kamerling JP. 2012. Structural characterization of linear isomalto-/malto-oligomer products synthesized by the novel GTFB 4, 6-α-glucanotransferase enzyme from Lactobacillus reuteri 121. Glycobiology 22:517-528. http://dx.doi.org/10.1093/glycob/cwr167.
16. Kralj S, Grijpstra P, van Leeuwen SS, Leemhuis H, Dobruchowska JM, van der Kaaij RM, Malik A, Oetari A, Kamerling JP, Dijkhuizen L. 2011. 4, 6-α-Glucanotransferase, a novel enzyme that structurally and functionally provides an evolutionary link between glycoside hydrolase enzyme families 13 and 70. Appl Environ Microbiol 77:8154-8163. http://dx.doi.org/10.1128/AEM.05735-11.
17. Leemhuis H, Dobruchowska JM, Ebbelaar M, Faber F, Buwalda PL, van der Maarel MJ, Kamerling JP, Dijkhuizen L. 2014. Isomalto/maltopolysaccharide, a novel soluble dietary fiber made via enzymatic conversion of starch. J Agric Food Chem 62:12034-12044. http://dx.doi.org/10.1021/jf503970a.
18. Leemhuis H, Dijkman WP, Dobruchowska JM, Pijning T, Grijpstra P, Kralj S, Kamerling JP, Dijkhuizen L. 2013. 4, 6-α-Glucanotransferase activity occurs more widespread in Lactobacillus strains and constitutes a separate GH70 subfamily. Appl Microbiol Biotechnol 97:181-193. http://dx.doi.org/10.1007/s00253-012-3943-1.
19. Dijkhuizen L, van der Maarel MJEC, Kamerling JP, Leemhuis H, Kralj S, Dobruchowska JM. November 2010. Gluco-oligosaccharides compris ing (α1→4) and (α1→6) glycosidic bonds, use thereof, and methods for providing them. Patent WO/2010/128859.
20. Bai Y, van der Kaaij RM, Woortman AJJ, Jin Z, Dijkhuizen L. 2015. Characterization of the 4, 6-α-glucanotransferase GTFB enzyme of Lactobacillus reuteri 121 isolated from inclusion bodies. BMC Biotechnol 15:49. http://dx.doi.org/10.1186/s12896-015-0163-7.
21. Palomo M, Pijning T, Booiman T, Dobruchowska JM, van der Vlist J, Kralj S, Planas A, Loos K, Kamerling JP, Dijkstra BW, van der Maarel MJEC, Dijkhuizen L, Leemhuis H. 2011. Thermus thermophilus glycoside hydrolase family 57 branching enzyme crystal structure, mechanism of action, and products formed. J Biol Chem 286:3520-3530. http://dx.doi.org/10.1074/jbc.M110.179515.
22. Cochran B, Lunday D, Miskevich F. 2008. Kinetic analysis of amylase using quantitative Benedict's and iodine starch reagents. J Chem Educ 85:401-403. http://dx.doi.org/10.1021/ed085p401.
23. Green F, Clausen CA, Highley TL. 1989. Adaptation of the Nelson-Somogyi reducing-sugar assay to a microassay using microtiter plates. Anal Biochem 182:197-199. http://dx.doi.org/10.1016/0003-2697(89)90578-2.
24. Kralj S, van Geel-Schutten GH, van der Maarel MJEC, Dijkhuizen L. 2004. Biochemical and molecular characterization of Lactobacillus reuteri 121 reuteransucrase. Microbiology 150:2099-2112. http://dx.doi.org/10.1099/mic.0.27105-0.
25. Monchois V, Arguello-Morales M, Russell RRB. 1999. Isolation of an active catalytic core of Streptococcus downei MFe28 GTF-I glucosyltransferase. J Bacteriol 181:2290-2292.
26. Swistowska AM, Wittrock S, Collisi W, Hofer B. 2008. Heterologous hyper-expression of a glucansucrase-type glycosyltransferase gene. Appl Microbiol Biotechnol 79:255-261. http://dx.doi.org/10.1007/s00253-008-1435-0.
27. Leemhuis H, Pijning T, Dobruchowska JM, van Leeuwen SS, Kralj S, Dijkstra BW, Dijkhuizen L. 2013. Glucansucrases: three-dimensional structures, reactions, mechanism, α-glucan analysis and their implications in biotechnology and food applications. J Biotechnol 163:250-272. http://dx.doi.org/10.1016/j.jbiotec.2012.06.037.
28. Kralj S, van Geel-Schutten GH, Dondorff MMG, Kirsanovs S, van der Maarel MJEC, Dijkhuizen L. 2004. Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 150:3681-3690. http://dx.doi.org/10.1099/mic.0.27321-0.
29. van Leeuwen SS, Leeflang BR, Gerwig GJ, Kamerling JP. 2008. Development of a 1H NMR structural-reporter-group concept for the primary structural characterisation of α-D-glucans. Carbohyd Res 343:1114-1119. http://dx.doi.org/10.1016/j.carres.2008.01.043.
30. Aref HL, Mosbah H, Louati H, Said K, Selmi B. 2011. Partial characterization of a novel amylase activity isolated from Tunisian Ficus carica latex. Pharm Biol 49:1158-1166. http://dx.doi.org/10.3109/13880209.2011.575791.
31. Xiao Z, Storms R, Tsang A. 2006. A quantitative starch-iodine method for measuring α-amylase and glucoamylase activities. Anal Biochem 351: 146-148. http://dx.doi.org/10.1016/j.ab.2006.01.036.
32. Kelly RM, Leemhuis H, Dijkhuizen L. 2007. Conversion of a cyclodextrin glucanotransferase into an α-amylase: assessment of directed evolution strategies. Biochemistry 46:11216-11222. http://dx.doi.org/10.1021/bi701160h.
33. Wang DD, Guo WH, Hu JM, Liu F, Chen LS, Du SW, Tang ZK. 2013. Estimating atomic sizes with Raman spectroscopy. Sci Rep 3:1486. http://dx.doi.org/10.1038/srep01486.
34. Genin AL, Banatskaya MI, Nikitin IV, Skokova IF, Vainshtein EF, Kushnerev MY, Kozlov PV. 1983. Criteria of choice of helix type in crystalline dextrane. Polym Sci 25:1717-1722.
35. Yu XC, Houtman C, Atalla RH. 1996. The complex of amylose and iodine. Carbohyd Res 292:129-141.
36. Jung JH, Jung TY, Seo DH, Yoon SM, Choi HC, Park BC, Park CS, Woo EJ. 2011. Structural and functional analysis of substrate recognition by the 250s loop in amylomaltase from Thermus brockianus. Proteins 79: 633-644. http://dx.doi.org/10.1002/prot.22911.
37. Tang SY, Yang SJ, Cha HJ, Woo EJ, Park C, Park KH. 2006. Contribution of W229 to the transglycosylation activity of 4-α-glucanotransferase from Pyrococcus furiosus. Biochim Biophys Acta 1764:1633-1638. http://dx.doi.org/10.1016/j.bbapap.2006.08.013.
38. Tachibana Y, Takaha T, Fujiwara S, Takagi M, Imanaka T. 2000. Acceptor specificity of 4-α-glucanotransferase from Pyrococcus kodakaraensis KOD1, and synthesis of cycloamylose. J Biosci Bioeng 90:406-409. http://dx.doi.org/10.1016/S1389-1723(01)80009-8.
39. Moulis C, Arcache A, Escalier PC, Rinaudo M, Monsan P, RemaudSimeon M, Potocki-Veronese G. 2006. High-level production and purification of a fully active recombinant dextransucrase from Leuconostoc mesenteroides NRRL B-512F. FEMS Microbiol Lett 261:203-210. http://dx.doi.org/10.1111/j.1574-6968.2006.00347.x.
40. Pijning T, Vujicic-Zagar A, Kralj S, Dijkhuizen L, Dijkstra BW. 2012. Structure of the α-1, 6/α-1, 4-specific glucansucrase GTFA from Lactobacillus reuteri 121. Acta Crystallogr F Struct Biol Commun 68:1448-1454. http://dx.doi.org/10.1107/S1744309112044168.
41. Pijning T, Vujicic-Zagar A, Kralj S, Eeuwema W, Dijkhuizen L, Dijkstra BW. 2008. Biochemical and crystallographic characterization of a glucansucrase from Lactobacillus reuteri 180. Biocatal Biotransformation 26:12-17. http://dx.doi.org/10.1080/10242420701789163.
42. Vujičić-Žagar A, Pijning T, Kralj S, Lopez CA, Eeuwema W, Dijkhuizen L, Dijkstra BW. 2010. Crystal structure of a 117 kDa glucansucrase fragment provides insight into evolution and product specificity of GH70 enzymes. Proc Natl Acad Sci U S A 107:21406-21411. http://dx.doi.org/10.1073/pnas.1007531107.
43. Ito K, Ito S, Shimamura T, Weyand S, Kawarasaki Y, Misaka T, Abe K, Kobayashi T, Cameron AD, Iwata S. 2011. Crystal structure of glucansucrase from the dental caries pathogen Streptococcus mutans. J Mol Biol 408:177-186. http://dx.doi.org/10.1016/j.jmb.2011.02.028.
44. Naessens M, Cerdobbel A, Soetaert W, Vandamme EJ. 2005. Dextran dextrinase and dextran of Gluconobacter oxydans. J Ind Microbiol Biotechnol 32:323-334. http://dx.doi.org/10.1007/s10295-005-0259-5.
45. Naessens M, Vandamme E. 2001. Transglucosylation and hydrolysis activity of Glucanobacter oxydans dextran dextrinase with several donor and acceptor substrates, p 195-203. In Chiellini E, Gil H, Braunegg G, Buchert J, Gatenholm P, van der Zee M (ed), Biorelated polymers: sustainable polymerscience and technology. Kluwer/Plenum, London, United Kingdom.
46. Cech J, Friedecky B. 1972. Determination of α amylase by a modification of photometric iodine starch method. Cas Lek Cesk 111:309-311.
47. Terada Y, Fujii K, Takaha T, Okada S. 1999. Thermus aquaticus ATCC 33923 amylomaltase gene cloning and expression and enzyme characterization: production of cycloamylose. Appl Environ Microbiol 65: 910-915.
48. Kralj S, Stripling E, Sanders P, van Geel-Schutten GH, Dijkhuizen L. 2005. Highly hydrolytic reuteransucrase from probiotic Lactobacillus reuteri strain ATCC 55730. Appl Environ Microbiol 71:3942-3950. http://dx.doi.org/10.1128/AEM.71.7.3942-3950.2005.
49. Kelly RM, Leemhuis H, Rozeboom HJ, van Oosterwijk N, Dijkstra BW, Dijkhuizen L. 2008. Elimination of competing hydrolysis and coupling side reactions of a cyclodextrin glucanotransferase by directed evolution. Biochem J 413:517-525. http://dx.doi.org/10.1042/BJ20080353.