1887

Abstract

Polyfructans are synthesized from sucrose by plants (mostly inulin) and by both Gram-negative and Gram-positive bacteria (mostly levan). In the phylum only levan synthesis by species has been reported. We have identified a putative fructansucrase gene () in DSM40736 (Tü494). HugO was heterologously expressed and biochemically characterized. HPSEC-MALLS and 2D-H-C nuclear magnetic resonance (NMR) spectroscopy analysis showed that the fructan polymer produced has an Molecular Weight of 2.5*10 Da and is an inulin that is mainly composed of (β2–1)-linked fructose units. This is the first report of a fructansucrase from and an inulosucrase from . Database searches showed that fructansucrases clearly occur more widely in streptomycetes. Analysis of the active site of HugO and other actinobacterial Gram-positive fructansucrases revealed that their +1 substrate-binding sites are conserved, but are most similar to those in Gram-negative fructansucrases. HugO also resembles Gram-negative fructansucrases in not requiring calcium ions for activity. The origin and properties of HugO and other actinobacterial fructansucrases thus clearly differ from those of previously characterized Gram-positive fructansucrases.

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2017-07-01
2024-04-24
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References

  1. McCarthy AJ, Williams ST. Actinomycetes as agents of biodegradation in the environment-a review. Gene 1992; 115:189–192 [View Article][PubMed]
    [Google Scholar]
  2. Thomas L, Crawford DL. Cloning of clustered Streptomyces viridosporus T7A lignocellulose catabolism genes encoding peroxidase and endoglucanase and their extracellular expression in Pichia pastoris. Can J Microbiol 1998; 44:364–372 [View Article][PubMed]
    [Google Scholar]
  3. Rahman MA, Choi YH, Pradeep GC, Choi YS, Choi EJ et al. A novel low molecular weight endo-xylanase from Streptomyces sp. CS628 cultivated in wheat bran. Appl Biochem Biotechnol 2014; 173:1469–1480 [View Article][PubMed]
    [Google Scholar]
  4. Garcia-Dominguez M, Martin JF, Liras P. Characterization of sugar uptake in wild-type Streptomyces clavuligerus, which is impaired in glucose uptake, and in a glucose-utilizing mutant. J Bacteriol 1989; 171:6808–6814 [View Article][PubMed]
    [Google Scholar]
  5. Dilipkumar M, Rajasimman M, Rajamohan N. Optimization of inulinase production from garlic by Streptomyces sp. in solid state fermentation using statistical designs. Biotechnol Res Int 2011; 2011:1–7 [View Article][PubMed]
    [Google Scholar]
  6. Miyajima K, Tanaka F, Takeuchi T, Kuninaga S. Streptomyces turgidiscabies sp. nov. Int J Syst Bacteriol 1998; 48:495–502 [View Article][PubMed]
    [Google Scholar]
  7. Velázquez-Hernández ML, Baizabal-Aguirre VM, Bravo-Patiño A, Cajero-Juárez M, Chávez-Moctezuma MP et al. Microbial fructosyltransferases and the role of fructans. J Appl Microbiol 2009; 106:1763–1778 [View Article][PubMed]
    [Google Scholar]
  8. Mensink MA, Frijlink HW, van der Voort Maarschalk K, Hinrichs WL. Inulin, a flexible oligosaccharide I: review of its physicochemical characteristics. Carbohydr Polym 2015; 130:405–419 [View Article][PubMed]
    [Google Scholar]
  9. Srikanth R, Reddy CH, Siddartha G, Ramaiah MJ, Uppuluri KB. Review on production, characterization and applications of microbial levan. Carbohydr Polym 2015; 120:102–114 [View Article][PubMed]
    [Google Scholar]
  10. van Hijum SA, Kralj S, Ozimek LK, Dijkhuizen L, van Geel-Schutten IG. Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 2006; 70:157–176 [View Article][PubMed]
    [Google Scholar]
  11. Meng G, Fütterer K. Structural framework of fructosyl transfer in Bacillus subtilis levansucrase. Nat Struct Biol 2003; 10:935–941 [View Article][PubMed]
    [Google Scholar]
  12. Pijning T, Anwar MA, Böger M, Dobruchowska JM, Leemhuis H et al. Crystal structure of inulosucrase from Lactobacillus: insights into the substrate specificity and product specificity of GH68 fructansucrases. J Mol Biol 2011; 412:80–93 [View Article][PubMed]
    [Google Scholar]
  13. Martínez-Fleites C, Ortíz-Lombardía M, Pons T, Tarbouriech N, Taylor EJ et al. Crystal structure of levansucrase from the Gram-negative bacterium Gluconacetobacter diazotrophicus. Biochem J 2005; 390:19–27 [View Article][PubMed]
    [Google Scholar]
  14. Batista FR, Hernández L, Fernández JR, Arrieta J, Menéndez C et al. 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 1999; 337:503–506 [View Article][PubMed]
    [Google Scholar]
  15. Yanase H, Maeda M, Hagiwara E, Yagi H, Taniguchi K et al. Identification of functionally important amino acid residues in Zymomonas mobilis levansucrase. J Biochem 2002; 132:565–572 [View Article][PubMed]
    [Google Scholar]
  16. Chambert R, Treboul G, Dedonder R. Kinetic studies of levansucrase of Bacillus subtilis. Eur J Biochem 1974; 41:285–300 [View Article][PubMed]
    [Google Scholar]
  17. Ozimek LK, Kralj S, van der Maarel MJ, Dijkhuizen L. The levansucrase and inulosucrase enzymes of Lactobacillus reuteri 121 catalyse processive and non-processive transglycosylation reactions. Microbiology 2006; 152:1187–1196 [View Article][PubMed]
    [Google Scholar]
  18. Olivares-Illana V, López-Munguía A, Olvera C. Molecular characterization of inulosucrase from Leuconostoc citreum: a fructosyltransferase within a glucosyltransferase. J Bacteriol 2003; 185:3606–3612 [View Article][PubMed]
    [Google Scholar]
  19. Wada T, Ohguchi M, Iwai Y. A novel enzyme of Bacillus sp. 217C-11 that produces inulin from sucrose. Biosci Biotechnol Biochem 2003; 67:1327–1334 [View Article][PubMed]
    [Google Scholar]
  20. Pabst MJ. Levan and levansucrase of Actinomyces viscosus. Infect Immun 1977; 15:518–526[PubMed]
    [Google Scholar]
  21. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood D et al. Practical Streptomyces Genetics John Innes Foundation; 2000
    [Google Scholar]
  22. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
    [Google Scholar]
  23. Schinko E, Schad K, Eys S, Keller U, Wohlleben W. Phosphinothricin-tripeptide biosynthesis: an original version of bacterial secondary metabolism?. Phytochemistry 2009; 70:1787–1800 [View Article][PubMed]
    [Google Scholar]
  24. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008; 36:W465–W469 [View Article][PubMed]
    [Google Scholar]
  25. Dereeper A, Audic S, Claverie JM, Blanc G. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 2010; 10:8 [View Article][PubMed]
    [Google Scholar]
  26. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011; 8:785–786 [View Article][PubMed]
    [Google Scholar]
  27. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A et al. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 2011; 39:W13–W17 [View Article][PubMed]
    [Google Scholar]
  28. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009; 25:1189–1191 [View Article][PubMed]
    [Google Scholar]
  29. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2001
    [Google Scholar]
  30. Birnboim HC, Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 1979; 7:1513–1523 [View Article][PubMed]
    [Google Scholar]
  31. Leemhuis H, Dijkman WP, Dobruchowska JM, Pijning T, Grijpstra P et al. 4,6-α-Glucanotransferase activity occurs more widespread in Lactobacillus strains and constitutes a separate GH70 subfamily. Appl Microbiol Biotechnol 2013; 97:181–193 [View Article][PubMed]
    [Google Scholar]
  32. Robichon C, Luo J, Causey TB, Benner JS, Samuelson JC. Engineering Escherichia coli BL21(DE3) derivative strains to minimize E. coli protein contamination after purification by immobilized metal affinity chromatography. Appl Environ Microbiol 2011; 77:4634–4646 [View Article][PubMed]
    [Google Scholar]
  33. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685 [View Article][PubMed]
    [Google Scholar]
  34. Fairbanks G, Steck TL, Wallach DF. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry 1971; 10:2606–2617 [View Article][PubMed]
    [Google Scholar]
  35. van Hijum SA, Bonting K, van der Maarel MJ, Dijkhuizen L. Purification of a novel fructosyltransferase from Lactobacillus reuteri strain 121 and characterization of the levan produced. FEMS Microbiol Lett 2001; 205:323–328 [View Article][PubMed]
    [Google Scholar]
  36. Anwar MA, Kralj S, van der Maarel MJ, Dijkhuizen L. The probiotic Lactobacillus johnsonii NCC 533 produces high-molecular-mass inulin from sucrose by using an inulosucrase enzyme. Appl Environ Microbiol 2008; 74:3426–3433 [View Article][PubMed]
    [Google Scholar]
  37. Gangoiti J, Pijning T, Dijkhuizen L. The Exiguobacterium sibiricum 255-15 GtfC enzyme represents a novel glycoside hydrolase 70 subfamily of 4,6-α-glucanotransferase enzymes. Appl Environ Microbiol 2016; 82:756–766 [View Article]
    [Google Scholar]
  38. Wise CS, Dimler RJ, Davis HA, Rist CE. Determination of easily hydrolyzable fructose units in dextran preparations. Anal Chem 1955; 27:33–36 [View Article]
    [Google Scholar]
  39. Meng X, Pijning T, Dobruchowska JM, Gerwig GJ, Dijkhuizen L. Characterization of the functional roles of amino acid residues in acceptor-binding subsite +1 in the active site of the glucansucrase GTF180 from Lactobacillus reuteri 180. J Biol Chem 2015; 290:30131–30141 [View Article][PubMed]
    [Google Scholar]
  40. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J et al. The pfam protein families database: towards a more sustainable future. Nucleic Acids Res 2016; 44:D279–D285 [View Article][PubMed]
    [Google Scholar]
  41. Widdick DA, Dilks K, Chandra G, Bottrill A, Naldrett M et al. The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc Natl Acad Sci USA 2006; 103:17927–17932 [View Article][PubMed]
    [Google Scholar]
  42. Ozimek LK, Euverink GJ, van der Maarel MJ, Dijkhuizen L. Mutational analysis of the role of calcium ions in the Lactobacillus reuteri strain 121 fructosyltransferase (levansucrase and inulosucrase) enzymes. FEBS Lett 2005; 579:1124–1128 [View Article][PubMed]
    [Google Scholar]
  43. Anwar MA, Dijkhuizen L, Kralj S. How lactobacilli synthesize inulin. Phd thesis University of Groningen, Groningen, The Netherlands 2010
  44. Anwar MA, Kralj S, Piqué AV, Leemhuis H, van der Maarel MJ et al. Inulin and levan synthesis by probiotic Lactobacillus gasseri strains: characterization of three novel fructansucrase enzymes and their fructan products. Microbiology 2010; 156:1264–1274 [View Article][PubMed]
    [Google Scholar]
  45. Alméciga-Díaz CJ, Gutierrez AM, Bahamon I, Rodríguez A, Rodríguez MA et al. Computational analysis of the fructosyltransferase enzymes in plants, fungi and bacteria. Gene 2011; 484:26–34 [View Article][PubMed]
    [Google Scholar]
  46. Bergeron LJ, Morou-Bermudez E, Burne RA. Characterization of the fructosyltransferase gene of Actinomyces naeslundii WVU45. J Bacteriol 2000; 182:3649–3654 [View Article][PubMed]
    [Google Scholar]
  47. Ito T, Fujita K, Hara K, Tonozuka T, Sakano Y. Cloning and expression of β-fructofuranosidase gene from Arthrobacter sp. K-1. J Appl Glycosci 2002; 49:291–296 [View Article]
    [Google Scholar]
  48. Hettwer U, Gross M, Rudolph K. Purification and characterization of an extracellular levansucrase from Pseudomonas syringae pv. phaseolicola. J Bacteriol 1995; 177:2834–2839 [View Article][PubMed]
    [Google Scholar]
  49. Chambert R, Petit-Glatron MF. Polymerase and hydrolase activities of Bacillus subtilis levansucrase can be separately modulated by site-directed mutagenesis. Biochem J 1991; 279:35–41 [View Article][PubMed]
    [Google Scholar]
  50. Gay P, Le Coq D, Steinmetz M, Ferrari E, Hoch JA. Cloning structural gene sacB, which codes for exoenzyme levansucrase of Bacillus subtilis: expression of the gene in Escherichia coli. J Bacteriol 1983; 153:1424–1431[PubMed]
    [Google Scholar]
  51. van Hijum SA, Szalowska E, van der Maarel MJ, Dijkhuizen L. Biochemical and molecular characterization of a levansucrase from Lactobacillus reuteri. Microbiology 2004; 150:621–630 [View Article][PubMed]
    [Google Scholar]
  52. Kralj S, van Geel-Schutten GH, van der Maarel MJ, Dijkhuizen L. Biochemical and molecular characterization of Lactobacillus reuteri 121 reuteransucrase. Microbiology 2004; 150:2099–2112 [View Article][PubMed]
    [Google Scholar]
  53. Meng X, Dobruchowska JM, Pijning T, Gerwig GJ, Dijkhuizen L. Synthesis of new hyperbranched α-glucans from sucrose by Lactobacillus reuteri 180 glucansucrase mutants. J Agric Food Chem 2016; 64:433–442 [View Article][PubMed]
    [Google Scholar]
  54. Norman JM, Bunny KL, Giffard PM. Characterization of levJ, a sucrase/fructanase-encoding gene from Actinomyces naeslundii T14V, and comparison of its product with other sucrose-cleaving enzymes. Gene 1995; 152:93–98 [View Article][PubMed]
    [Google Scholar]
  55. Viaene T, Langendries S, Beirinckx S, Maes M, Goormachtig S. Streptomyces as a plant's best friend?. FEMS Microbiol Ecol 2016; 92:fiw119 [View Article][PubMed]
    [Google Scholar]
  56. Horlacher N, Nachtigall J, Schulz D, Süssmuth RD, Hampp R et al. Biotransformation of the fungal phytotoxin fomannoxin by soil Streptomycetes. J Chem Ecol 2013; 39:931–941 [View Article][PubMed]
    [Google Scholar]
  57. Leigh JA, Coplin DL. Exopolysaccharides in plant-bacterial interactions. Annu Rev Microbiol 1992; 46:307–346 [View Article][PubMed]
    [Google Scholar]
  58. Koczan JM, Mcgrath MJ, Zhao Y, Sundin GW. Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity. Phytopathology 2009; 99:1237–1244 [View Article][PubMed]
    [Google Scholar]
  59. Bayer E, Gugel KH, Hägele K, Hagenmaier H, Jessipow S et al. [Metabolic products of microorganisms. 98. Phosphinothricin and phosphinothricyl-alanyl-analine]. Helv Chim Acta 1972; 55:224–239 [View Article][PubMed]
    [Google Scholar]
  60. Bullock WO, Fernandez JM, Short JM. XL1-Blue, a high efficiency plasmid transforming recA Escherichia coli strain with beta galactosidase selection. Biotechniques 1987376–379
    [Google Scholar]
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