Structure–function relationships of family GH70 glucansucrase and 4,6-α-glucanotransferase enzymes, and their evolutionary relationships with family GH13 enzymes

Cellular and Molecular Life Sciences

Volumn 73, Issue 14, 2016, Pages 2681-2706

  Meng, Xiangfeng ^a   Gangoiti, Joana ^a   Bai, Yuxiang ^a   Pijning, Tjaard ^a   Van Leeuwen, Sander S ^a   Dijkhuizen, Lubbert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

4,6 Glucanotransferase; Evolution; GH13; GH70; Glucansucrase; Structure function

Indexed keywords

4,6 ALPHA GLUCANOTRANSFERASE; ALPHA GLUCAN; GH13 GLUCANSUCRASE; GH70 GLUCANSUCRASE; GLUCAN; GLYCOSYLTRANSFERASE; MALTOSE; OLIGOSACCHARIDE; SUCRASE; UNCLASSIFIED DRUG; 4 ALPHA-GLUCANOTRANSFERASE; ALTERNANSUCRASE; GLYCOGEN DEBRANCHING ENZYME;

BIOCATALYST; CARBOHYDRATE SYNTHESIS; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENE SEQUENCE; LACTIC ACID BACTERIUM; LACTOBACILLUS; LEUCONOSTOC; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN LOCALIZATION; REVIEW; STREPTOCOCCUS; STRUCTURE ACTIVITY RELATION; WEISSELLA; BACTERIUM; BIOCATALYSIS; CHEMISTRY; ENZYMOLOGY; METABOLISM;

BACTERIA; BIOCATALYSIS; EVOLUTION, MOLECULAR; GLYCOGEN DEBRANCHING ENZYME SYSTEM; GLYCOSYLTRANSFERASES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84966264000     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-016-2245-7     Document Type: Review

References (139)

1. Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15(2):67–78. doi:10.1016/j.tifs.2003.09.004
2. Kumari A, Catanzaro R, Marotta F (2011) Clinical importance of lactic acid bacteria: a short review. Acta Biomed 82(3):177–180
3. Galle S, Arendt EK (2014) Exopolysaccharides from sourdough lactic acid bacteria. Crit Rev Food Sci Nutr 54(7):891–901. doi:10.1080/10408398.2011.617474
4. Jolly L, Vincent SJ, Duboc P, Neeser JR (2002) Exploiting expolysaccharides from lactic acid bacteria. Antonie Van Leeuwenhoek 82(1–4):367–374
5. Ryan PM, Ross RP, Fitzgerald GF, Caplice NM, Stanton C (2015) Sugar-coated: exopolysaccharide producing lactic acid bacteria for food and human health applications. Food Funct 6(3):679–693. doi:10.1039/C4fo00529e
6. Welman AD, Maddox IS (2003) Exopolysaccharides from lactic acid bacteria: perspectives and challenges. Trends Biotechnol 21(6):269–274. doi:10.1016/S0167-7799(03)00107-0
7. Torino MI, Font de Valdez G, Mozzi F (2015) Biopolymers from lactic acid bacteria. Novel applications in foods and beverages. Front Microbiol 6:834. doi:10.3389/fmicb.2015.00834
8. Zannini E, Waters DM, Coffey A, Arendt EK (2015) Production, properties, and industrial food application of lactic acid bacteria-derived exopolysaccharides. Appl Microbiol Biotechnol. doi:10.1007/s00253-015-7172-2
9. Bowen WH, Koo H (2011) Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res 45(1):69–86. doi:10.1159/000324598
10. Gibbons RJ (1968) Formation and significance of bacterial polysaccharides in caries etiology. Caries Res 2(2):164–171. doi:10.1159/000259554
11. Laws A, Gu Y, Marshall V (2001) Biosynthesis, characterisation, and design of bacterial exopolysaccharides from lactic acid bacteria. Biotechnol Adv 19(8):597–625. doi:10.1016/S0734-9750(01)00084-2
12. De Vuyst L, Degeest B (1999) Heteropolysaccharides from lactic acid bacteria. FEMS Microbiol Rev 23(2):153–177
13. van Hijum SA, Kralj S, Ozimek LK, Dijkhuizen L, van Geel-Schutten IGH (2006) Structure–function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 70(1):157–176. doi:10.1128/MMBR.70.1.157-176.2006
14. Korakli M, Vogel RF (2006) Structure/function relationship of homopolysaccharide producing glycansucrases and therapeutic potential of their synthesised glycans. Appl Microbiol Biotechnol 71(6):790–803. doi:10.1007/s00253-006-0469-4
15. 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(2):250–272. doi:10.1016/j.jbiotec.2012.06.037
16. Monchois V, Willemot R-M, Monsan P (1999) Glucansucrases: mechanism of action and structure–function relationships. FEMS Microbiol Rev 23(2):131–151. doi:10.1111/j.1574-6976.1999.tb00394.x
17. Gangoiti J, Pijning T, Dijkhuizen L (2015) Biochemical characterization of the Exiguobacterium sibiricum 255-15 GtfC enzyme representing a novel glycoside hydrolase 70 subfamily of 4,6-α-glucanotransferase enzymes. Appl Environ Microbiol. doi:10.1128/AEM.03420-15
18. 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(22):8154–8163. doi:10.1128/AEM.05735-11
19. Monsan P, Bozonnet S, Albenne C, Joucla G, Willemot R-M, Remaud-Siméon M (2001) Homopolysaccharides from lactic acid bacteria. Int Dairy J 11(9):675–685. doi:10.1016/S0958-6946(01)00113-3
20. Naessens M, Cerdobbel A, Soetaert W, Vandamme EJ (2005) Leuconostoc dextransucrase and dextran: production, properties and applications. J Chem Technol Biotechnol 80(8):845–860. doi:10.1002/Jctb.1322
21. Hehre EJ (1941) Production from sucrose of a sero-logically reactive polysaccharide by a sterile bacterial extract. Science 93(2410):237–238. doi:10.1126/science.93.2410.237
22. Hehre EJ, Sugg JY (1942) Serologically reactive polysaccharides produced through the action of bacterial enzymes: Dextran of Leuconostoc mesenteroides from sucrose. J Exp Med 75(3):339–353
23. Bounaix MS, Gabriel V, Morel S, Robert H, Rabier P, Remaud-Siméon M, Gabriel B, Fontagné-Faucher C (2009) Biodiversity of exopolysaccharides produced from sucrose by sourdough lactic acid bacteria. J Agric Food Chem 57(22):10889–10897. doi:10.1021/jf902068t
24. López-Munguia A, Pelenc V, Remaud-Siméon M, Biton J, Michel JM, Lang C, Paul F, Monsan P (1993) Production and purification of alternansucrase, a glucosyltransferase from Leuconostoc mesenteroides NRRL B-1355 for the synthesis of oligoalternans. Enzyme Microb Technol 15(1):77–85. doi:10.1016/0141-0229(93)90120-Q
25. Van Geel-Schutten IGH, Faber EJ, Smit E, Bonting K, Smith MR, Ten Brink B, Kamerling JP, Vliegenthart JFG, Dijkhuizen L (1999) 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(7):3008–3014
26. Hanada N, Kuramitsu HK (1989) Isolation and characterization of the Streptococcus mutans gtfD gene, coding for primer-dependent soluble glucan synthesis. Infect Immun 57(7):2079–2085
27. Ooshima T, Matsumura M, Hoshino T, Kawabata S, Sobue S, Fujiwara T (2001) Contributions of three glucosyltransferases to sucrose-dependent adherence of Streptococcus mutans. J Dent Res 80(7):1672–1677. doi:10.1177/00220345010800071401
28. Passerini D, Vuillemin M, Ufarte L, Morel S, Loux V, Fontagné-Faucher C, Monsan P, Remaud-Siméon M, Moulis C (2015) Inventory of the GH70 enzymes encoded by Leuconostoc citreum NRRL B-1299 - identification of three novel α-transglucosylases. FEBS J 282(11):2115–2130. doi:10.1111/febs.13261
29. Argüello-Morales MA, Remaud-Siméon M, Pizzut S, Sarcabal P, Willemot R-M, Monsan P (2000) Sequence analysis of the gene encoding alternansucrase, a sucrose glucosyltransferase from Leuconostoc mesenteroides NRRL B-1355. FEMS Microbiol Lett 182(1):81–85. doi:10.1111/j.1574-6968.2000.tb08878.x
30. Walker GJ, Cheetham NWH, Taylor C, Pearce BJ, Slodki ME (1990) Productivity of 4 α-d-glucosyltransferases released by Streptococcus sobrinus under defined conditions in continuous culture. Carbohyd Polym 13(4):399–421. doi:10.1016/0144-8617(90)90039-U
31. Kim D, Robyt JF (1994) Production and selection of mutants of Leuconostoc mesenteroides constitutive for glucansucrases. Enzyme Microb Technol 16(8):659–664. doi:10.1016/0141-0229(94)90086-8
32. Kim D, Robyt JF (1995) Dextransucrase constitutive mutants of Leuconostoc mesenteroides B-1299. Enzyme Microb Technol 17(12):1050–1056. doi:10.1016/0141-0229(95)00039-9
33. Kim D, Robyt JF (1995) Production, selection, and characteristics of mutants of Leuconostoc mesenteroides B-742 constitutive for dextransucrases. Enzyme Microb Technol 17(8):689–695. doi:10.1016/0141-0229(94)00021-I
34. Badel S, Bernardi T, Michaud P (2011) New perspectives for Lactobacilli exopolysaccharides. Biotechnol Adv 29(1):54–66. doi:10.1016/j.biotechadv.2010.08.011
35. Bozonnet S, Dols-Laffargue M, Fabre E, Pizzut S, Remaud-Siméon M, Monsan P, Willemot R-M (2002) Molecular characterization of DSR-E, an α-1,2 linkage-synthesizing dextransucrase with two catalytic domains. J Bacteriol 184(20):5753–5761. doi:10.1128/JB.184.20.5753-5761.2002
36. Brison Y, Pijning T, Malbert Y, Fabre E, Mourey L, Morel S, Potocki-Vèronése G, Monsan P, Tranier S, Remaud-Siméon M, Dijkstra BW (2012) Functional and structural characterization of α-(1 → 2) branching sucrase derived from DSR-E glucansucrase. J Biol Chem 287(11):7915–7924. doi:10.1074/jbc.M111.305078
37. Fabre E, Bozonnet S, Arcache A, Willemot R-M, Vignon M, Monsan P, Remaud-Siméon M (2005) Role of the two catalytic domains of DSR-E dextransucrase and their involvement in the formation of highly α-1,2 branched dextran. J Bacteriol 187(1):296–303. doi:10.1128/JB.187.1.296-303.2005
38. Monchois V, Willemot R-M, Remaud-Siméon M, Croux C, Monsan P (1996) Cloning and sequencing of a gene coding for a novel dextransucrase from Leuconostoc mesenteroides NRRL B-1299 synthesizing only α (1 → 6) and α (1 → 3) linkages. Gene 182(1–2):23–32. doi:10.1016/S0378-1119(96)00443-X
39. Monchois V, Remaud-Siméon M, Monsan P, Willemot R-M (1998) Cloning and sequencing of a gene coding for an extracellular dextransucrase (DSRB) from Leuconostoc mesenteroides NRRL B-1299 synthesizing only a α(1 → 6) glucan. FEMS Microbiol Lett 159(2):307–315. doi:10.1111/j.1574-6968.1998.tb12876.x
40. Côté GL, Robyt JF (1982) Isolation and partial characterization of an extracellular glucansucrase from Leuconostoc mesenteroides NRRL B-1355 that synthesizes an alternating (1 → 6)/(1 → 3)-α-d-glucan. Carbohydr Res 101(1):57–74. doi:10.1016/S0008-6215(00)80795-8
41. Vidal RF, Martinez A, Moulis C, Escalier P, Morel S, Remaud-Siméon M, Monsan P (2011) A novel dextransucrase is produced by Leuconostoc citreum strain B/110-1-2: an isolate used for the industrial production of dextran and dextran derivatives. J Ind Microbiol Biotechnol 38(9):1499–1506. doi:10.1007/s10295-010-0936-x
42. Fraga Vidal R, Moulis C, Escalier P, Remaud-Siméon M, Monsan P (2011) Isolation of a gene from Leuconostoc citreum B/110-1-2 encoding a novel dextransucrase enzyme. Curr Microbiol 62(4):1260–1266. doi:10.1007/s00284-010-9851-7
43. Côté GL, Skory CD (2012) Cloning, expression, and characterization of an insoluble glucan-producing glucansucrase from Leuconostoc mesenteroides NRRL B-1118. Appl Microbiol Biotechnol 93(6):2387–2394. doi:10.1007/s00253-011-3562-2
44. Amari M, Valérie G, Robert H, Morel S, Moulis C, Gabriel B, Remaud-Siméon M, Fontagné-Faucher C (2015) Overview of the glucansucrase equipment of Leuconostoc citreum LBAE-E16 and LBAE-C11, two strains isolated from sourdough. FEMS Microbiol Lett 362(1):1–8. doi:10.1093/femsle/fnu024
45. Hamada S, Slade HD (1980) Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol Rev 44(2):331–384
46. Mayhall CW, Butler WT (1976) The carbohydrate composition of experimental salivary pellicles. J Oral Pathol 5(6):358–370. doi:10.1111/j.1600-0714.1976.tb01787.x
47. Emilson CG, Nilsson B, Bowen WH (1984) Carbohydrate composition of dental plaque from primates with irradiation caries. J Oral Pathol 13(3):213–220. doi:10.1111/j.1600-0714.1984.tb01419.x
48. Hata S, Mayanagi H (2003) Acid diffusion through extracellular polysaccharides produced by various mutants of Streptococcus mutans. Arch Oral Biol 48(6):431–438. doi:10.1016/S0003-9969(03)0032-3
49. Shiroza T, Ueda S, Kuramitsu HK (1987) Sequence analysis of the gtfB gene from Streptococcus mutans. J Bacteriol 169(9):4263–4270
50. Ueda S, Shiroza T, Kuramitsu HK (1988) Sequence analysis of the gtfC gene from Streptococcus mutans GS-5. Gene 69(1):101–109. doi:10.1016/0378-1119(88)90382-4
51. Yamashita Y, Bowen WH, Burne RA, Kuramitsu HK (1993) Role of the Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model. Infect Immun 61(9):3811–3817
52. Tsumori H, Kuramitsu H (1997) The role of the Streptococcus mutans glucosyltransferases in the sucrose-dependent attachment to smooth surfaces: essential role of the GtfC enzyme. Oral Microbiol Immunol 12(5):274–280. doi:10.1111/j.1399-302X.1997.tb00391.x
53. Gilmore KS, Russell RRB, Ferretti JJ (1990) Analysis of the Streptococcus downei gtfS gene, which specifies a glucosyltransferase that synthesizes soluble glucans. Infect Immun 58(8):2452–2458
54. Valeur N, Engel P, Carbajal N, Connolly E, Ladefoged K (2004) Colonization and immunomodulation by Lactobacillus reuteri ATCC 55730 in the human gastrointestinal tract. Appl Environ Microbiol 70(2):1176–1181. doi:10.1128/AEM.70.2.1176-1181.2004
55. van Geel-Schutten IGH, Flesch F, ten Brink B, Smith MR, Dijkhuizen L (1998) Screening and characterization of Lactobacillus strains producing large amounts of exopolysaccharides. Appl Microbiol Biotechnol 50(6):697–703. doi:10.1007/s002530051353
56. Kralj S, van Geel-Schutten IGH, van der Maarel MJEC, Dijkhuizen L (2004) Biochemical and molecular characterization of Lactobacillus reuteri 121 reuteransucrase. Microbiology 150(Pt 7):2099–2112. doi:10.1099/mic.0.27105-0
57. Kralj S, van Geel-Schutten IGH, 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(Pt 11):3681–3690. doi:10.1099/mic.0.27321-0
58. Kralj S, van Geel-Schutten IGH, Rahaoui H, Leer RJ, Faber EJ, van der Maarel MJEC, Dijkhuizen L (2002) Molecular characterization of a novel glucosyltransferase from Lactobacillus reuteri strain 121 synthesizing a unique, highly branched glucan with α-(1 → 4) and α-(1 → 6) glucosidic bonds. Appl Environ Microbiol 68(9):4283–4291. doi:10.1128/AEM.68.9.4283-4291.2002
59. van Leeuwen SS, Kralj S, van Geel-Schutten IGH, Gerwig GJ, Dijkhuizen L, Kamerling JP (2008) Structural analysis of the α-d-glucan (EPS35-5) produced by the Lactobacillus reuteri strain 35-5 glucansucrase GTFA enzyme. Carbohydr Res 343(7):1251–1265. doi:10.1016/j.carres.2008.01.044
60. Kralj S, Stripling E, Sanders P, van Geel-Schutten IGH, Dijkhuizen L (2005) Highly hydrolytic reuteransucrase from probiotic Lactobacillus reuteri strain ATCC 55730. Appl Environ Microbiol 71(7):3942–3950. doi:10.1128/AEM.71.7.3942-3950.2005
61. Bounaix MS, Robert H, Gabriel V, Morel S, Remaud-Siméon M, Gabriel B, Fontagné-Faucher C (2010) Characterization of dextran-producing Weissella strains isolated from sourdoughs and evidence of constitutive dextransucrase expression. FEMS Microbiol Lett 311(1):18–26. doi:10.1111/j.1574-6968.2010.02067.x
62. Amari M, Arango LF, Gabriel V, Robert H, Morel S, Moulis C, Gabriel B, Remaud-Siméon M, Fontagné-Faucher C (2013) Characterization of a novel dextransucrase from Weissella confusa isolated from sourdough. Appl Microbiol Biotechnol 97(12):5413–5422. doi:10.1007/s00253-012-4447-8
63. Kang HK, Oh JS, Kim D (2009) Molecular characterization and expression analysis of the glucansucrase DSRWC from Weissella cibaria synthesizing a α(1 → 6) glucan. FEMS Microbiol Lett 292(1):33–41. doi:10.1111/j.1574-6968.2008.01460.x
64. Dimopoulou M, Vuillemin M, Campbell-Sills H, Lucas PM, Ballestra P, Miot-Sertier C, Favier M, Coulon J, Moine V, Doco T, Roques M, Williams P, Petrel M, Gontier E, Moulis C, Remaud-Siméon M, Dols-Lafargue M (2014) Exopolysaccharide (EPS) synthesis by Oenococcus oeni: from genes to phenotypes. PLoS One 9(6):e98898. doi:10.1371/journal.pone.0098898
65. Moulis C, Joucla G, Harrison D, Fabre E, Potocki-Vèronése G, Monsan P, Remaud-Siméon M (2006) Understanding the polymerization mechanism of glycoside-hydrolase family 70 glucansucrases. J Biol Chem 281(42):31254–31267. doi:10.1074/jbc.M604850200
66. Monchois V, Reverte A, Remaud-Siméon M, Monsan P, Willemot R-M (1998) Effect of Leuconostoc mesenteroides NRRL B-512F dextransucrase carboxy-terminal deletions on dextran and oligosaccharide synthesis. Appl Environ Microbiol 64(5):1644–1649
67. Janecek S, Svensson B, Russell RRB (2000) Location of repeat elements in glucansucrases of Leuconostoc and Streptococcus species. FEMS Microbiol Lett 192(1):53–57. doi:10.1111/j.1574-6968.2000.tb09358.x
68. Funane K, Mizuno K, Takahara H, Kobayashi M (2000) Gene encoding a dextransucrase-like protein in Leuconostoc mesenteroides NRRL B-512F. Biosci Biotechnol Biochem 64(1):29–38. doi:10.1271/bbb.64.29
69. Giffard PM, Jacques NA (1994) Definition of a fundamental repeating unit in Streptococcal glucosyltransferase glucan-binding regions and related sequences. J Dent Res 73(6):1133–1141. doi:10.1177/00220345940730060201
70. Kingston KB, Allen DM, Jacques NA (2002) Role of the C-terminal YG repeats of the primer-dependent streptococcal glucosyltransferase, GtfJ, in binding to dextran and mutan. Microbiology 148(Pt 2):549–558. doi:10.1099/00221287-148-2-549
71. Vujičić-Žagar A, Pijning T, Kralj S, López 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 USA 107(50):21406–21411. doi:10.1073/pnas.1007531107
72. 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(2):177–186. doi:10.1016/j.jmb.2011.02.028
73. Pijning T, Vujičić-Žagar 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 Sect F Struct Biol Cryst Commun 68(12):1448–1454. doi:10.1107/S1744309112044168
74. MacGregor EA, Jespersen HM, Svensson B (1996) A circularly permuted α-amylase-type α/β-barrel structure in glucan-synthesizing glucosyltransferases. FEBS Lett 378(3):263–266. doi:10.1016/0014-5793(95)01428-4
75. Svensson B (1994) Protein engineering in the α-amylase family: catalytic mechanism, substrate specificity, and stability. Plant Mol Biol 25(2):141–157. doi:10.1007/BF00023233
76. Monchois V, Vignon M, Escalier PC, Svensson B, Russell RRB (2000) Involvement of Gln937 of Streptococcus downei GTF-I glucansucrase in transition-state stabilization. Eur J Biochem 267(13):4127–4136. doi:10.1046/j.1432-1327.2000.01448.x
77. Uitdehaag JCM, Mosi R, Kalk KH, van der Veen BA, Dijkhuizen L, Withers SG, Dijkstra BW (1999) X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the α-amylase family. Nat Struct Biol 6(5):432–436. doi:10.1038/8235
78. Lis M, Shiroza T, Kuramitsu HK (1995) Role of the C-terminal direct repeating units of the Streptococcus mutans glucosyltransferase-S in glucan binding. Appl Environ Microbiol 61(5):2040–2042
79. Pijning T, Vujičić-Žagar A, Kralj S, Dijkhuizen L, Dijkstra BW (2014) Flexibility of truncated and full-length glucansucrase GTF180 enzymes from Lactobacillus reuteri 180. FEBS J 281(9):2159–2171. doi:10.1111/febs.12769
80. Meng X, Dobruchowska JM, Pijning T, Gerwig GJ, Kamerling JP, Dijkhuizen L (2015) Truncation of domain V of the multidomain glucansucrase GTF180 of Lactobacillus reuteri 180 heavily impairs its polysaccharide-synthesizing ability. Appl Microbiol Biotechnol 99(14):5885–5894. doi:10.1007/s00253-014-6361-8
81. van Leeuwen SS, Kralj S, Eeuwema W, Gerwig GJ, Dijkhuizen L, Kamerling JP (2009) Structural characterization of bioengineered α-d-glucans produced by mutant glucansucrase GTF180 enzymes of Lactobacillus reuteri strain 180. Biomacromolecules 10(3):580–588. doi:10.1021/bm801240r
82. van Leeuwen SS, Kralj S, van Geel-Schutten IGH, Gerwig GJ, Dijkhuizen L, Kamerling JP (2008) Structural analysis of the α-D-glucan (EPS180) produced by the Lactobacillus reuteri strain 180 glucansucrase GTF180 enzyme. Carbohydr Res 343(7):1237–1250. doi:10.1016/j.carres.2008.01.042
83. van Leeuwen SS, Kralj S, Gerwig GJ, Dijkhuizen L, Kamerling JP (2008) 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(8):2251–2258. doi:10.1021/bm800410w
84. Dobruchowska JM, Meng X, Leemhuis H, Gerwig GJ, Dijkhuizen L, Kamerling JP (2013) Gluco-oligomers initially formed by the reuteransucrase enzyme of Lactobacillus reuteri 121 incubated with sucrose and malto-oligosaccharides. Glycobiology 23(9):1084–1096. doi:10.1093/glycob/cwt048
85. Cheetham NWH, Slodki ME, Walker GJ (1991) Structure of the linear, low-molecular-weight dextran synthesized by a D-glucosyltransferase (Gtf-S3) of Streptococcus sobrinus. Carbohyd Polym 16(4):341–353. doi:10.1016/0144-8617(91)90053-F
86. Ebert KH, Schenk G (1968) Mechanisms of biopolymer growth: the formation of dextran and levan. Adv Enzymol Relat Areas Mol Biol 30:179–221. doi:10.1002/9780470122754.ch4
87. Meng X, Dobruchowska JM, Gerwig GJ, Kamerling JP, Dijkhuizen L (2015) Synthesis of oligo- and polysaccharides by Lactobacillus reuteri 121 reuteransucrase at high concentrations of sucrose. Carbohydr Res 414:85–92. doi:10.1016/j.carres.2015.07.011
88. Shah DSH, Joucla G, Remaud-Siméon M, Russell RRB (2004) Conserved repeat motifs and glucan binding by glucansucrases of oral Streptococci and Leuconostoc mesenteroides. J Bacteriol 186(24):8301–8308. doi:10.1128/JB.186.24.8301-8308.2004
89. Kralj S, Eeuwema W, Eckhardt TH, Dijkhuizen L (2006) Role of asparagine 1134 in glucosidic bond and transglycosylation specificity of reuteransucrase from Lactobacillus reuteri 121. FEBS J 273(16):3735–3742. doi:10.1111/j.1742-4658.2006.05376.x
90. Kralj S, van Geel-Schutten IGH, Faber EJ, van der Maarel MJEC, Dijkhuizen L (2005) Rational transformation of Lactobacillus reuteri 121 reuteransucrase into a dextransucrase. Biochemistry 44(25):9206–9216. doi:10.1021/bi050447q
91. Hellmuth H, Wittrock S, Kralj S, Dijkhuizen L, Hofer B, Seibel J (2008) Engineering the glucansucrase GTFR enzyme reaction and glycosidic bond specificity: toward tailor-made polymer and oligosaccharide products. Biochemistry 47(25):6678–6684. doi:10.1021/bi800563r
92. 940 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(47):32773–32782. doi:10.1074/jbc.M114.602524
93. Kim D, Robyt JF, Lee S-Y, Lee J-H, Kim Y-M (2003) Dextran molecular size and degree of branching as a function of sucrose concentration, pH, and temperature of reaction of Leuconostoc mesenteroides B-512FMCM dextransucrase. Carbohydr Res 338(11):1183–1189. doi:10.1016/S0008-6215(03)00148-4
94. Falconer DJ, Mukerjea R, Robyt JF (2011) Biosynthesis of dextrans with different molecular weights by selecting the concentration of Leuconostoc mesenteroides B-512FMC dextransucrase, the sucrose concentration, and the temperature. Carbohydr Res 346(2):280–284. doi:10.1016/j.carres.2010.10.024
95. Robyt JF, Taniguchi H (1976) The mechanism of dextransucrase action. Biosynthesis of branch linkages by acceptor reactions with dextran. Arch Biochem Biophys 174(1):129–135. doi:10.1016/0003-9861(76)90331-3
96. Leemhuis H, Pijning T, Dobruchowska JM, Dijkstra BW, Dijkhuizen L (2012) Glycosidic bond specificity of glucansucrases: on the role of acceptor substrate binding residues. Biocatal Biotransform 30(3):366–376. doi:10.3109/10242422.2012.676301
97. Meng X, Dobruchowska JM, Pijning T, Gerwig GJ, Dijkhuizen L (2016) Synthesis of new hyperbranched α-glucans from sucrose by Lactobacillus reuteri 180 glucansucrase mutants. J Agric Food Chem. doi:10.1021/acs.jafc.5b05161
98. Irague R, Tarquis L, André I, Moulis C, Morel S, Monsan P, Potocki-Vèronése G, Remaud-Siméon M (2013) Combinatorial engineering of dextransucrase specificity. PLoS One 8(10):e77837. doi:10.1371/journal.pone.0077837
99. Meng X, Pijning T, Dobruchowska JM, Gerwig GJ, Dijkhuizen L (2015) 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. doi:10.1074/jbc.M115.687558
100. Vuillemin M, Claverie M, Brison Y, Séverac E, Bondy P, Morel S, Monsan P, Moulis C, Remaud-Siméon M (2016) Characterization of the first α-(1 → 3) branching sucrases of GH70 family. J Biol Chem. doi:10.1074/jbc.M115.688044
101. Galle S, Schwab C, Dal Bello F, Coffey A, Gänzle MG, Arendt EK (2012) Influence of in situ synthesized exopolysaccharides on the quality of gluten-free sorghum sourdough bread. Int J Food Microbiol 155(3):105–112. doi:10.1016/j.ijfoodmicro.2012.01.009
102. Spence JH, Higgins AR, Kimmel JR (1952) The clinical effects of dextran as a plasma volume extender. US Armed Forces Med J 3(4):515–518
103. Kim D, Day D-F (1994) A new process for the production of clinical dextran by mixed-culture fermentation of Lipomyces starkeyi and Leuconostoc mesenteroides. Enzyme Microb Technol 16(10):844–848. doi:10.1016/0141-0229(94)90058-2
104. Finkenstadt VL, Côté GL, Willett JL (2011) Corrosion protection of low-carbon steel using exopolysaccharide coatings from Leuconostoc mesenteroides. Biotechnol Lett 33(6):1093–1100. doi:10.1007/s10529-011-0539-2
105. Scheerder J, Breur R, Slaghek T, Holtman W, Vennik M, Ferrari G (2012) Exopolysaccharides (EPS) as anti-corrosive additives for coatings. Prog Org Coat 75(3):224–230. doi:10.1016/j.porgcoat.2012.05.003
106. Olano-Martin E, Mountzouris KC, Gibson GR, Rastall RA (2000) In vitro fermentability of dextran, oligodextran and maltodextrin by human gut bacteria. Br J Nutr 83(3):247–255. doi:10.1017/S0007114500000325
107. Sarbini SR, Kolida S, Naeye T, Einerhand A, Brison Y, Remaud-Siméon M, Monsan P, Gibson GR, Rastall RA (2011) In vitro fermentation of linear and α-1,2-branched dextrans by the human fecal microbiota. Appl Environ Microbiol 77(15):5307–5315. doi:10.1128/AEM.02568-10
108. Monsan P, Paul F, Auriol D (1995) New developments in the application of enzymes to synthesis reactions. Peptides and oligosaccharides. Ann NY Acad Sci 750:357–363. doi:10.1111/j.1749-6632.1995.tb19980.x
109. Monchois V, Vignon M, Russell RRB (2000) Mutagenesis of Asp-569 of glucosyltransferase I glucansucrase modulates glucan and oligosaccharide synthesis. Appl Environ Microbiol 66(5):1923–1927. doi:10.1128/AEM.66.5.1923-1927.2000
110. Côté GL, Skory CD (2014) Effects of mutations at threonine-654 on the insoluble glucan synthesized by Leuconostoc mesenteroides NRRL B-1118 glucansucrase. Appl Microbiol Biotechnol 98(15):6651–6658. doi:10.1007/s00253-014-5622-x
111. Tsumori H, Minami T, Kuramitsu HK (1997) Identification of essential amino acids in the Streptococcus mutans glucosyltransferases. J Bacteriol 179(11):3391–3396
112. Binder TP, Côté GL, Robyt JF (1983) Disproportionation reactions catalyzed by Leuconostoc and Streptococcus glucansucrases. Carbohyd Res 124(2):275–286. doi:10.1016/0008-6215(83)88463-8
113. 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(4):517–528. doi:10.1093/glycob/cwr167
114. 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(1):181–193. doi:10.1007/s00253-012-3943-1
115. Leemhuis H, Dobruchowska JM, Ebbelaar M, Faber F, Buwalda PL, van der Maarel MJ, Kamerling JP, Dijkhuizen L (2014) Isomalto/malto-polysaccharide, a novel soluble dietary fiber made via enzymatic conversion of starch. J Agric Food Chem 62(49):12034–12044. doi:10.1021/jf503970a
116. Rodrigues DF, Goris J, Vishnivetskaya T, Gilichinsky D, Thomashow MF, Tiedje JM (2006) Characterization of Exiguobacterium isolates from the siberian permafrost. Description of Exiguobacterium sibiricum sp. nov. Extremophiles 10(4):285–294. doi:10.1007/s00792-005-0497-5
117. Rodrigues DF, Ivanova N, He Z, Huebner M, Zhou J, Tiedje JM (2008) Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: a genome and transcriptome approach. BMC Genom 9:547. doi:10.1186/1471-2164-9-547
118. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42 (Database issue):D490–D495. doi:10.1093/nar/gkt1178
119. 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(2):137–155. doi:10.1016/S0168-1656(01)00407-2
120. Janecek S, Svensson B, MacGregor EA (2014) α-Amylase: an enzyme specificity found in various families of glycoside hydrolases. Cell Mol Life Sci 71(7):1149–1170. doi:10.1007/s00018-013-1388-z
121. MacGregor EA, Janecek S, Svensson B (2001) Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim Biophys Acta 1546(1):1–20. doi:10.1016/S0167-4838(00)00302-2
122. Janecek S (2002) How many conserved sequence regions are there in the α-amylase family? Biologia 57:29–41
123. Peisajovich SG, Rockah L, Tawfik DS (2006) Evolution of new protein topologies through multistep gene rearrangements. Nat Genet 38(2):168–174. doi:10.1038/ng1717
124. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Diaz-Muniz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103(42):15611–15616. doi:10.1073/pnas.0607117103
125. Sun ZH, Harris HMB, McCann A, Guo CY, Argimon S, Zhang WY, Yang XW, Jeffery IB, Cooney JC, Kagawa TF, Liu WJ, Song YQ, Salvetti E, Wrobel A, Rasinkangas P, Parkhill J, Rea MC, O’Sullivan O, Ritari J, Douillard FP, Ross RP, Yang RF, Briner AE, Felis GE, de Vos WM, Barrangou R, Klaenhammer TR, Caufield PW, Cui YJ, Zhang HP, O’Toole PW (2015) Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nature communications. doi:10.1038/Ncomms9322
126. Funane K, Ishii T, Ono H, Kobayashi M (2005) Changes in linkage pattern of glucan products induced by substitution of Lys residues in the dextransucrase. FEBS Lett 579(21):4739–4745. doi:10.1016/j.febslet.2005.07.050
127. Irague R, Rolland-Sabaté A, Tarquis L, Doublier JL, Moulis C, Monsan P, Remaud-Siméon M, Potocki-Vèronése G, Buléon A (2012) Structure and property engineering of α-d-glucans synthesized by dextransucrase mutants. Biomacromolecules 13(1):187–195. doi:10.1021/bm201453r
128. Irague R, Massou S, Moulis C, Saurel O, Milon A, Monsan P, Remaud-Siméon M, Portais JC, Potocki-Vèronése G (2011) NMR-based structural glycomics for high-throughput screening of carbohydrate-active enzyme specificity. Anal Chem 83(4):1202–1206. doi:10.1021/ac1032148
129. Reetz MT (2011) Laboratory evolution of stereoselective enzymes: a prolific source of catalysts for asymmetric reactions. Angew Chem 50(1):138–174. doi:10.1002/anie.201000826
130. Wijma HJ, Floor RJ, Jekel PA, Baker D, Marrink SJ, Janssen DB (2014) Computationally designed libraries for rapid enzyme stabilization. Protein Eng Des Sel 27(2):49–58. doi:10.1093/protein/gzt061
131. Daude D, Remaud-Siméon M, Andre I (2012) Sucrose analogs: an attractive (bio)source for glycodiversification. Nat Prod Rep 29(9):945–960. doi:10.1039/C2np20054f
132. Seibel J, Jordening HJ, Buchholz K (2010) Extending synthetic routes for oligosaccharides by enzyme, substrate and reaction engineering. Adv Biochem Eng Biot 120:163–193. doi:10.1007/10_2009_54
133. Seibel J, Moraru R, Gotze S, Buchholz K, Na’amnieh S, Pawlowski A, Hecht HJ (2006) Synthesis of sucrose analogues and the mechanism of action of Bacillus subtilis fructosyltransferase (levansucrase). Carbohydr Res 341(14):2335–2349. doi:10.1016/j.carres.2006.07.001
134. Baciu IE, Jordening HJ, Seibel J, Buchholz K (2005) Investigations of the transfructosylation reaction by fructosyltransferase from B. subtilis NCIMB 11871 for the synthesis of the sucrose analogue galactosyl-fructoside. J Biotechnol 116(4):347–357. doi:10.1016/j.jbiotec.2004.10.019
135. Cheetham PSJ, Hacking AJ, Vlitos M (1989) Synthesis of novel disaccharides by a newly isolated fructosyl transferase from Bacillus subtilis. Enzyme Microb Technol 11(4):212–219. doi:10.1016/0141-0229(89)90095-1
136. Seibel J, Moraru R, Gotze S (2005) Biocatalytic and chemical investigations in the synthesis of sucrose analogues. Tetrahedron 61(30):7081–7086. doi:10.1016/j.tet.2005.05.063
137. Timm M, Gorl J, Kraus M, Kralj S, Hellmuth H, Beine R, Buchholz K, Dijkhuizen L, Seibel J (2013) An unconventional glycosyl transfer reaction: glucansucrase GTFA functions as an allosyltransferase enzyme. ChemBioChem 14(18):2423–2426. doi:10.1002/cbic.201300392
138. Monchois V, Remaud-Siméon M, Russell RRB, Monsan P, Willemot R-M (1997) Characterization of Leuconostoc mesenteroides NRRL B-512F dextransucrase (DSRS) and identification of amino-acid residues playing a key role in enzyme activity. Appl Microbiol Biotechnol 48(4):465–472. doi:10.1007/s002530051081
139. Ferretti JJ, Gilpin ML, Russell RRB (1987) Nucleotide sequence of a glucosyltransferase gene from Streptococcus sobrinus MFe28. J Bacteriol 169(9):4271–4278