Applied Microbiology and Biotechnology

, Volume 71, Issue 6, pp 790–803 | Cite as

Structure/function relationship of homopolysaccharide producing glycansucrases and therapeutic potential of their synthesised glycans

  • Maher KorakliEmail author
  • Rudi F. Vogel


The capability of lactic acid bacteria (LAB) to produce exopoly- and oligosaccharides was and is the subject of expanding research efforts. Due to their physicochemical properties and health-promoting potential, exopoly- and oligosaccharides from food-grade LAB can be used in the food and other industries and may have additional medical applications. In the last years, many LAB have been screened for their ability to produce exopoly- and oligosaccharides, and several glycosyltransferases involved in their biosynthesis have been characterised at biochemical and genetic levels. These research efforts aim to exploit the full potential of these organisms and to understand the structure/function relationship of glycosyltransferases. The latter knowledge is a prerequisite for the production of tailored exopoly- and oligosaccharides for the diverse applications. This review will survey the results of recent works on the structure/function relationship of homopolysaccharide producing glycosyltransferases and the therapeutic potential of their synthesised exopoly- and oligosaccharides.


Lactobacillus Lactic Acid Bacterium Glucan Inulin Sucrose Concentration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.















Intestinal epithelial cells















Part of the work discussed in this study was funded in project no. AiF-FV 14037N/2 of the Otto von Guericke Foundation (Arbeitsgemeinschaft industrieller Forschungsvereinigungen, AiF), Germany. The authors are indebted to Carrie Hew for proofreading the manuscript for style and language.


  1. Abo H, Matsumura T, Kodama T, Ohta H, Fukui K, Kato K, Kagawa H (1991) Peptide sequences for sucrose splitting and glucan binding within Streptococcus sobrinus glucosyltransferase (water-insoluble glucan synthetase). J Bacteriol 173:989–996PubMedGoogle Scholar
  2. Argüello-Morales MA, Remaud-Simeon M, Pizzut S, Sarçabal P, Willemot RM, Monsan P (2000) Sequence analysis of the gene encoding alternansucrase, a sucrose glucosyltransferase from Leuconostoc mesenteroides NRRL B-1355. FEMS Microbiol Lett 182:81–85CrossRefPubMedGoogle Scholar
  3. Barthelson R, Mobasseri A, Zopf D, Simon P (1998) Adherence of Streptococcus pneumoniae to respiratory epithelial cells is inhibited by sialylated oligosaccharides. Infect Immun 66:1439–1444PubMedGoogle Scholar
  4. Batista FR, Hernandez L, Fernandez JR, Arrieta J, Menendez C, Gomez R, Tambara Y, Pons T (1999) Substitution of Asp-309 by Asn in the Arg-Asp-Pro (RDP) motif of Acetobacter diazotrophicus levansucrase affects sucrose hydrolysis, but not enzyme specificity. Biochem J 337:503–506CrossRefPubMedGoogle Scholar
  5. Bergmaier D, Champagne CP, Lacroix C (2005) Growth and exopolysaccharide production during free and immobilized cell chemostat culture of Lactobacillus rhamnosus RW-9595M. J Appl Microbiol 98:272–284CrossRefPubMedGoogle Scholar
  6. Boker M, Jordening H, Buchholz K (1994) Kinetics of leucrose formation from sucrose by dextransucrase. Biotechnol Bioeng 43:392–394CrossRefGoogle Scholar
  7. Cerning J (1990) Exocellular polysaccharides produced by lactic acid bacteria. FEMS Microbiol Rev 87:113–130CrossRefGoogle Scholar
  8. Cummings JH, Macfarlane GT, Englyst HN (2001) Prebiotic digestion and fermentation. Am J Clin Nutr 73:415S–420SPubMedGoogle Scholar
  9. Davies G, Henrissat B (1995) Structures and mechanisms of glycosylhydrolases. Structure 15:853–859CrossRefGoogle Scholar
  10. Davies GJ, Gloster TM, Henrissat B (2005) Recent structural insights into the expanding world of carbohydrate-active enzymes. Curr Opin Struct Biol 15:637–645CrossRefPubMedGoogle Scholar
  11. De Vuyst L, Degeest B (1999) Heteropolysaccharides from lactic acid bacteria. FEMS Microbiol Rev 23:153–177CrossRefPubMedGoogle Scholar
  12. Dueñas-Chasco MT, Rodriguez-Carvajal MA, Tejero Mateo P, Franco-Rodriguez G, Espartero JL, Irastorza-Iribas A, Gil-Serrano AM (1997) Structural analysis of the exopolysaccharide produced by Pediococcus damnosus 2.6. Carbohydr Res 303:453–458CrossRefPubMedGoogle Scholar
  13. Dueñas-Chasco MT, Rodriguez-Carvajal MA, Tejero-Mateo P, Espartero JL, Irastorza-Iribas A, Gil-Serrano AM (1998) Structural analysis of the exopolysaccharides produced by Lactobacillus spp. G-77. Carbohydr Res 307:125–133CrossRefPubMedGoogle Scholar
  14. Ebisu S, Kato K, Kotani S, Misaki A (1975) Structural differences in fructans elaborated by Streptococcus mutans and Strep. salivarius. J Biochem 78:879–887PubMedGoogle Scholar
  15. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412PubMedGoogle Scholar
  16. Gibson GR, McCartney AL, Rastall RA (2005) Prebiotics and resistance to gastrointestinal infections. Br J Nutr 93:31S–34SCrossRefGoogle Scholar
  17. Giffard PM, Simpson CL, Milward CP, Jacques NA (1991) Molecular characterization of a cluster of at least two glucosyltransferases genes in Streptococcus salivarius ATCC 25975. J Gen Microbiol 137:2577–2593PubMedGoogle Scholar
  18. Giffard PM, Allen DM, Milward CP, Simpson CL, Jacques NA (1993) Sequence of the gtfK gene of Streptococcus salivarius ATCC 25975 and evolution of the gtf genes of oral streptococci. J Gen Microbiol 139:1511–1522PubMedGoogle Scholar
  19. Groenwall AJ, Ingelman BJA (1948) Manufacture of infusion and injection fluids. US Patent 2:437–518Google Scholar
  20. Kang HK, Seo MY, Seo ES, Kim D, Chung SY, Kimura A, Day DF, Robyt JF (2005) Cloning and expression of levansucrase from Leuconostoc mesenteroides B-512 FMC in Escherichia coli. Biochim Biophys Acta 1727:5–15PubMedGoogle Scholar
  21. Kato C, Nakano Y, Lis M, Kuramitsu HK (1992) Molecular genetic analysis of the catalytic site of Streptococcus mutans glucosyltransferases. Biochem Biophys Res Commun 189:1184–1188CrossRefPubMedGoogle Scholar
  22. Koepsell HJ, Tsuchiya HM, Hellman NN, Kasenko A, Hofman CA, Sharpe ES, Jackson RW (1953) Enzymatic synthesis of dextran, acceptor specificity and chain initiation. J Biol Chem 200:793–801PubMedGoogle Scholar
  23. Korakli M, Schwarz E, Wolf G, Hammes WP (2000) Production of mannitol by Lactobacillus sanfranciscensis. Adv Food Sci 22:1–4Google Scholar
  24. Korakli M, Rossman A, Gänzle MG, Vogel RF (2001) Sucrose metabolism and exopolysaccharide production in wheat and rye sourdoughs by L. sanfranciscensis. J Agric Food Chem 49:5194–5200CrossRefPubMedGoogle Scholar
  25. 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 92:958–965CrossRefPubMedGoogle Scholar
  26. Korakli M, Pavlovic M, Gänzle MG, Vogel RF (2003) Exopolysaccharide and kestose production by Lactobacillus sanfranciscensis LTH2590. Appl Environ Microbiol 69:2073–2079CrossRefPubMedGoogle Scholar
  27. Kralj S, van Geel-Schutten GH, 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 68:4283–4291CrossRefPubMedGoogle Scholar
  28. Kralj S, van Geel-Schutten GH, Dondroff MMG, Kirsanovs S, van der Maarel MJEC, Dijkhuizen L (2004a) Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 150:3681–3690CrossRefPubMedGoogle Scholar
  29. Kralj S, van Geel-Schutten GH, van der Maarel MJEC, Dijkhuizen L (2004b) Biochemical and molecular characterization of Lactobacillus reuteri 121 reuteransucrase. Microbiology 150:2099–2112CrossRefPubMedGoogle Scholar
  30. Kralj S, Stripling E, Sanders P, van Geel-Schutten GH, Dijkhuizen L (2005a) Highly hydrolytic reuteransucrase from probiotic Lactobacillus reuteri strain ATCC 55730. Appl Environ Microbiol 71:3942–3950CrossRefPubMedGoogle Scholar
  31. Kralj S, van Geel-Schutten GH, Faber EJ, van der Maarel MJEC, Dijkhuizen L (2005b) Rational transformation of Lactobacillus reuteri 121 reuteransucrase into a dextransucrase. Biochemistry 44:9206–9216CrossRefPubMedGoogle Scholar
  32. Kunz C, Rudloff S (1993) Biological functions of oligosaccharides in human milk. Acta Paediatr 82:903–912PubMedGoogle Scholar
  33. Martinez-Fleites C, Ortiz-Lombardia M, Pons T, Tarbouriech N, Taylor EJ, Arrieta JG, Hernandez L, Davies GJ (2005) Crystal structure of levansucrase from the Gram-negative bacterium Gluconacetobacter diazotrophicus. Biochem J 390:19–27CrossRefPubMedGoogle Scholar
  34. Mayer RM, Matthews MM, Futerman CL, Parnaik VK, Jung SM (1981) Dextransucrase: acceptor substrate reactions. Arch Biochem Biophys 208:278–287CrossRefPubMedGoogle Scholar
  35. Mckay LL, Baldwin KA (1990) Applications: present and future improvements in lactic acid bacteria. FEMS Microbiol Rev 87:3–14CrossRefGoogle Scholar
  36. Meng G, Futterer K (2003) Structural framework of fructosyl transfer in Bacillus subtilis levansucrase. Nat Struct Biol 10:935–941CrossRefPubMedGoogle Scholar
  37. Monchois V, Willemot RM, Remaud-Simeon 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 á(1–6) and á(1–3) linkages. Gene 182:23–32CrossRefPubMedGoogle Scholar
  38. Monchois V, Remaud-Simeon M, Russell RRB, Monsan P, Willemot RM (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 48:465–472CrossRefPubMedGoogle Scholar
  39. Monchois V, Willemot RM, Monsan P (1999) Glucansucrases: mechanism of action and structure–function relationships. FEMS Microbiol Rev 23:131–151CrossRefPubMedGoogle Scholar
  40. Monchois V, Vignon M, Russell RRB (2000) Mutagenesis of Asp-569 of glucosyltransferase I glucansucrase modulates glucan and oligosaccharide synthesis. Appl Environ Microbiol 66:1923–1927CrossRefPubMedGoogle Scholar
  41. Monsan P, Bozonnet S, Albenne C, Joucla G, Willemot RM, Remaud-Siméon M (2001) Homopolysaccharides from lactic acid bacteria. Int Dairy J 11:675–685CrossRefGoogle Scholar
  42. Mooser G, Hefta SA, Paxton RJ, Shively JE, Lee TD (1991) Isolation and sequence of an active-site peptide containing a catalytic aspartic acid from two Streptococcus sobrinus glucosyltransferases. J Biol Chem 266:8916–8922PubMedGoogle Scholar
  43. Okazaki M, Fujikawa S, Matsumoto N (1990) Effects of xylooligosaccharide on growth of bifidobacteria. J Jpn Soc Nutr Food Sci 43:395–401Google Scholar
  44. Olivares-Illana V, Lopez-Munguia A, Olvera C (2003) Molecular characterization of inulosucrase from Leuconostoc citreum: a fructosyltransferase with a glucosyltransferase. J Bacteriol 185:3606–3612CrossRefPubMedGoogle Scholar
  45. Ozimek LK, van Hijum SAFT, van Koningsveld GA, van der Maarel MJEC, van Geel-Schutten GH, Dijkhuizen L (2004) Site-directed mutagenesis study of the three catalytic residues of the fructosyltransferases of Lactobacillus reuteri 121. FEBS Lett 560:131–133CrossRefPubMedGoogle Scholar
  46. Park NH, Choi HJ, Oh DK (2005) Lactosucrose production by various microorganisms harbouring levansucrase activity. Biotechnol Lett 27:495–497CrossRefPubMedGoogle Scholar
  47. Pelenc V, Lopez-Munguia A, Remaud M, Biton J, Michel J, Paul F, Monsan P (1991) Enzymatic synthesis of oligoalternans. Sci Aliment 11:465–476Google Scholar
  48. Raschka L (2005) Mechanisms underlying the effects of inulin-type fructans on the intestinal calcium absorption. Doctoral Thesis, Technische Universität München, GermanyGoogle Scholar
  49. Robyt JF, Walseth TF (1978) The mechanism of acceptor reactions of Leuconostoc mesenteroides NRRL B-512F dextransucrase. Carbohydr Res 61:433–435CrossRefPubMedGoogle Scholar
  50. Rosell KG, Birkhed D (1974) An inulin-like fructan produced by Streptococcus mutans strain JC2. Acta Chem Scand B28:589CrossRefGoogle Scholar
  51. Shiroza T, Ueda S, Kuramitsu HK (1987) Sequence analysis of the gtfB gene from Streptococcus mutans. J Bacteriol 169:4263–4270PubMedGoogle Scholar
  52. Shoaf KS, Hutkins R (2005) Adherence inhibition of intestinal pathogens by anti-adhesive oligosaccharides. 8th symposium on lactic acid bacteria. Egmond aan Zee, The NetherlandsGoogle Scholar
  53. Simon PM, Goode PL, Mobasseri A, Zopf D (1997) Inhibition of Helicobacter pylori binding to gastrointestinal epithelial cells by sialic acid-containing oligosaccharides. Infect Immun 65:750–757PubMedGoogle Scholar
  54. Smith MR, Zahnley JC, Wong RY, Lundin RE, Ahlgren JA (1998) A mutant strain of Leuconostoc mesenteroides B-1355 producing a glucosyltransferase synthesising α-(1→2) glucosidic linkages. J Ind Microbiol Biotechnol 21:37–45CrossRefGoogle Scholar
  55. Soetaert W, Schwengers D, Buchholz K, Vandamme EJ (1995) A wide range of carbohydrate modifications by a single microorganism: Leuconostoc mesenteroides. In: Peterson SB, Svensson B, Pederson S (eds) Carbohydrate bioengineering. Elsevier, Amsterdam, pp 351–358Google Scholar
  56. Sutherland IW (1997) Biotechnology of microbial polysaccharides. Cambridge University Press, Cambridge, United KingdomGoogle Scholar
  57. Sutherland IW (1998) Novel and established applications of microbial polysaccharides. Trends Biotechnol 16:41–46CrossRefPubMedGoogle Scholar
  58. Thomas RJ, Brooks TJ (2004) Oligosaccharide receptor mimics inhibit Legionella pneumophila attachment to human respiratory epithelial cells. Microb Pathog 36:83–92CrossRefPubMedGoogle Scholar
  59. Tieking M, Gänzle M (2005) Exopolysaccharides from cereal-associated lactobacilli. Trends Food Sci Technol 16:79–84CrossRefGoogle Scholar
  60. Tieking M, Korakli M, Ehrmann MA, Gänzle MG, Vogel RF (2003) In situ production of exopolysaccharides during sourdough fermentation by cereal and intestinal isolates of lactic acid bacteria. Appl Environ Microbiol 69:945–952CrossRefPubMedGoogle Scholar
  61. Tieking M, Ehrmann MA, Vogel RF, Gänzle MG (2005a) Molecular and functional characterization of a levansucrase from the sourdough isolate Lactobacillus sanfranciscensis TMW 1.392. Appl Microbiol Biotechnol 66:655–663CrossRefPubMedGoogle Scholar
  62. Tieking M, Kaditzky S, Valcheva R, Korakli M, Vogel RF, Gänzle MG (2005b) Extracellular homopolysaccharides and oligosaccharides from intestinal lactobacilli. J Appl Microbiol 99:692–702CrossRefPubMedGoogle Scholar
  63. Tieking M, Kühnl W, Gänzle MG (2005c) Evidence for formation of heterooligosaccharides by Lactobacillus sanfranciscensis during growth in wheat sourdough. J Agric Food Chem 53:2456–2461CrossRefPubMedGoogle Scholar
  64. Tzortzis G, Jay AJ, Baillon MLA, Gibson GR, Rastall RA (2003) Synthesis of α-galactooligosaccharides with α-galactosidase from Lactobacillus reuteri of canine origin. Appl Microbiol Biotechnol 63:286–292CrossRefPubMedGoogle Scholar
  65. van Geel-Schutten GH, Flesch F, Ten Brink B, Smith MR, Dijkhuizen L (1998) Screening and characterisation of Lactobacillus strains producing large amounts of exopolysaccharides. Appl Microbiol Biotechnol 50:697–703CrossRefGoogle Scholar
  66. van Hijum SAFT, Bonting K, van der Maarel MJEC, Dijkhuizen L (2001) Purification of a novel fructosyltransferase from Lactobacillus reuteri strain 121 and characterization of the levan produced. FEMS Microbiol Lett 205:323–328CrossRefPubMedGoogle Scholar
  67. van Hijum SAFT, van Geel-Schutten GH, Rahaoui H, van der Maarel MJ, Dijkhuizen L (2002) Characterization of a novel fructosyltransferase from Lactobacillus reuteri that synthesizes high-molecular-weight inulin and inulin oligosaccharides. Appl Environ Microbiol 68:4390–4398CrossRefPubMedGoogle Scholar
  68. van Hijum SAFT, van der Maarel MJ, Dijkhuizen L (2003) Kinetic properties of an inulosucrase from Lactobacillus reuteri 121. FEBS Lett 534:207–210CrossRefPubMedGoogle Scholar
  69. van Hijum SAFT, Szalowska E, van der Maarel MJ, Dijkhuizen L (2004) Biochemical and molecular characterization of a levansucrase from Lactobacillus reuteri. Microbiology 150:621–630CrossRefPubMedGoogle Scholar
  70. Vickermann MM, Sulavik MC, Minick PE, Clewell DB (1996) Changes in the carboxy-terminal repeat region affect extracellular activity and glucan products of Streptococcus gordonii glucosyltransferase. Infect Immun 64:5117–5128PubMedGoogle Scholar
  71. Vincent S, Brandt MJ, Cavadini C, Hammes WP, Neeser JR, Waldbüsser S (2002) Lactobacillus strain producing levan and its use in human or pet food products. International Patent WO 02/50311 A3Google Scholar
  72. Werning ML, Ibarburu I, Dueñas MT, Irastorza A, Navas J, Lopez P (2006) Pediococcus parvulus gtf gene encoding GTF glycosyltransferase and its application for specific PCR detection of β-D-glucan-producing bacteria in foods and beverages. J Food Prot 69:161–169PubMedGoogle Scholar
  73. Whitfield C (1988) Bacterial extracellualr polysaccharides. Can J Microbiol 34:415–420PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Lehrstuhl für Technische MikrobiologieTechnische Universität MünchenFreisingGermany

Personalised recommendations