Biomolecular characterization of the levansucrase of erwinia amylovora, a promising biocatalyst for the synthesis of fructooligosaccharides

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 50, 2013, Pages 12265-12273

  Caputi, Lorenzo ^a,b   Nepogodiev, Sergey A ^b   Malnoy, Mickael ^c   Rejzek, Martin ^b   Field, Robert A ^b   Benini, Stefano ^a  

^a FREE UNIVERSITY OF BOZEN BOLZANO   (Italy)

^b JOHN INNES CENTRE   (United Kingdom)

^c RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

Erwinia amylovora; fructans; HPAEC PAD; infection; levansucrase

Indexed keywords

ERWINIA AMYLOVORA; FRUCTANS; HPAEC-PAD; INFECTION; LEVANSUCRASE;

ENZYMES; ESCHERICHIA COLI;

POLYSACCHARIDES;

BACTERIAL PROTEIN; GLYCOSYLTRANSFERASE; IDOLAX; LEVANSUCRASE; OLIGOSACCHARIDE;

ARTICLE; BIOCATALYSIS; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; ERWINIA AMYLOVORA; GENETICS; KINETICS; METABOLISM;

BACTERIAL PROTEINS; BIOCATALYSIS; ERWINIA AMYLOVORA; HEXOSYLTRANSFERASES; KINETICS; OLIGOSACCHARIDES;

EID: 84890753466     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf4023178     Document Type: Article

References (51)

1. Gross, M.; Geier, G.; Rudolph, K.; Geider, K. Levan and levansucrase synthesized by the fireblight pathogen Erwinia amylovora Physiol. Mol. Plant Pathol. 1992, 40, 371-381
2. Geier, G.; Geider, K. Characterization and influence on virulence of the levansucrase gene from the fire blight pathogen Erwinia amylovora Physiol. Mol. Plant Pathol. 1993, 42, 387-404
3. Bereswill, S.; Jock, S.; Aldridge, P.; Janse, J. D.; Geider, K. Molecular characterization of natural Erwinia amylovora strains deficient in levan synthesis Physiol. Mol. Plant Pathol. 1997, 51, 215-225
4. Zhao, Y.; Blumer, S. E.; Sundin, G. W. Identification of Erwinia amylovora genes induced during infection of immature pear tissue J. Bacteriol. 2005, 187, 8088-8103
5. Koczan, J. M.; McGrath, M. J.; Zhao, Y.; Sundin, G. W. Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity Phytopathology 2009, 99, 1237-1244
6. Mena-Arizmendi, A.; Alderete, J.; águila, S.; Marty, A.; Miranda-Molina, A.; López-Munguía, A.; Castillo, E. Enzymatic fructosylation of aromatic and aliphatic alcohols by Bacillus subtilis levansucrase: reactivity of acceptors J. Mol. Catal. B: Enzym. 2011, 70, 41-48
7. Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.; Bernard, T.; Lombard, V.; Henrissat, B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics Nucleic Acids Res. 2009, 37, D233-D238
8. Meng, G.; Fütterer, K. Structural framework of fructosyl transfer in Bacillus subtilis levansucrase Nat. Struct. Biol. 2003, 10, 935-941
9. Strube, C. P.; Homann, A.; Gamer, M.; Jahn, D.; Seibel, J.; Heinz, D. W. Polysaccharide synthesis of the levansucrase SacB from Bacillus megaterium is controlled by distinct surface motifs J. Biol. Chem. 2011, 286, 17593-17600
10. Tonozuka, T.; Tamaki, A.; Yokoi, G.; Miyazaki, T.; Ichikawa, M.; Nishikawa, A.; Ohta, Y.; Hidaka, Y.; Katayama, K.; Hatada, Y.; Ito, T.; Fujita, K. Crystal structure of a lactosucrose-producing enzyme, Arthrobacter sp. K-1 β-fructofuranosidase Enzyme Microb. Technol. 2012, 51, 359-365
11. Martínez-Fleites, C.; Ortíz-Lombardía, M.; Pons, T.; Tarbouriech, N.; Taylor, E. J.; Arrieta, J. G.; Hernández, L.; Davies, G. J. Crystal structure of levansucrase from the Gram-negative bacterium Gluconacetobacter diazotrophicus Biochem. J. 2005, 390, 19-27
12. Kralj, S.; van Leeuwen, S. S.; Valk, V.; Eeuwema, W.; Kamerling, J. P.; Dijkhuizen, L. Hybrid reuteransucrase enzymes reveal regions important for glucosidic linkage specificity and the transglucosylation/hydrolysis ratio FEBS J. 2008, 275, 6002-6010
13. Ozimek, L. K.; Kralj, S.; Kaper, T.; van der Maarel, M. J. E. C.; Dijkhuizen, L. Single amino acid residue changes in subsite -1 of inulosucrase from Lactobacillus reuteri 121 strongly influence the size of products synthesized FEBS J. 2006, 273, 4104-4113
14. Anwar, M. A.; Leemhuis, H.; Pijning, T.; Kralj, S.; Dijkstra, B. W.; Dijkhuizen, L. The role of conserved inulosucrase residues in the reaction and product specificity of Lactobacillus reuteri inulosucrase FEBS J. 2012, 279, 3612-3621
15. Yun, Y. W. Fructooligosaccharides-occurrence, preparation, and application Enzyme Microb. Technol. 1996, 19, 107-117
16. Hendry, G. A. F.; Wallace, R. K. The origin, distribution and evolutionary significance of fructans. In Science and Technology of Fructans; Suzuki, M.; Chatterton, N. J., Eds.; CRC Press: Boca Raton, FL, USA, 1993; pp 119-139.
17. Cote, G. L.; Ahlgren, J. A. Metabolism in microorganisms, part I: levan and levansucrase. In Science and Technology of Fructans; Suzuki, M.; Chatterton, N. J., Eds.; CRC Press: Boca Raton, FL, USA, 1993; pp 141-168.
18. Verdonk, J. M.; Shim, S. B.; van Leeuwen, P.; Verstegen, M. W. Application of inulin-type fructans in animal feed and pet food Br. J. Nutr. 2005, 93, S125-S138
19. Sabater-Molina, M.; Larqué, E.; Torrella, F.; Zamora, S. Dietary fructooligosaccharides and potential benefits on health J. Physiol. Biochem. 2009, 65, 315-328
20. Singh, R. S.; Singh, R. P. Production of fructooligosaccharides from inulin by endoinulinases and their prebiotic potential Food Technol. Biotechnol. 2010, 48, 435-450
21. Kang, S. A.; Hong, K. H.; Jang, K. H.; Kim, S. H.; Lee, K. H.; Chang, B. I.; Kim, C. H.; Choue, R. W. Anti-obesity and hypolipidemic effects of dietary levan in high fat diet-induced obese rats J. Microbiol. Biotechnol. 2004, 14, 796-804
22. Marx, S. P.; Winkler, S.; Hartmeier, W. Metabolization of β-(2,6)-linked fructose-oligosaccharides by different bifidobacteria FEMS Microbiol. Lett. 2000, 182, 163-169
23. Rastall, R. A. Functional oligosaccharides: application and manufacture Annu. Rev. Food Sci. Technol. 2010, 1, 305-339
24. van Arkel, J.; Sévenier, R.; Hakkert, J. C.; Bouwmeester, H. J.; Koops, A. J.; van der Meer, I. M. Tailor-made fructan synthesis in plants: a review Carbohydr. Polym. 2013, 93, 48-56
25. Caputi, L.; Cianci, M.; Benini, S. Cloning, expression, purification, crystallization and preliminary X-ray analysis of EaLsc, a levansucrase from Erwinia amylovora Acta Crystallogr. 2013, F69, 570-573
26. Dümmler, A.; Lawrence, A.-M.; de Marco, A. Simplified screening for the detection of soluble fusion constructs expressed in E. coli using a modular set of vectors Microb. Cell Fact. 2005, 4, 34
27. Cabrita, L. D.; Gilis, D.; Robertson, A. L.; Dehouck, Y.; Rooman, M.; Bottomley, S. P. Enhancing the stability and solubility of TEV protease using in silico design Protein Sci. 2007, 16, 2360-2367
28. Van Hijum, S. A. F. T.; Szalowska, E.; van der Maarel, M. J. E. C.; Dijkhuizen, L. Biochemical and molecular characterization of a levansucrase from Lactobacillus reuteri Microbiology 2004, 150, 621-630
29. Van Hijum, S. A. F. T.; Bonting, K.; van der Maarel, M. J. E. C.; 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
30. Smits, T. H.; Rezzonico, F.; Kamber, T.; Blom, J.; Goesmann, A.; Frey, J. E.; Duffy, B. Complete genome sequence of the fire blight pathogen Erwinia amylovora CFBP 1430 and comparison to other Erwinia spp Mol. Plant-Microbe Interact. 2010, 23, 384-93
31. Lombard, V.; Ramulu, H. G.; Drula, E.; Coutinho, P. M.; Henrissat, B. The Carbohydrate-Active EnZymes database (CAZy) in 2013. Nucleic Acids Res. 2013, 1-6 (doi:10.1093/nar/gkt1178).
32. Larkin, M. A.; Blackshields, G.; Brown, N. P.; Chenna, R.; McGettigan, P. A.; McWilliam, H.; Valentin, F.; Wallace, I. M.; Wilm, A.; Lopez, R.; Thompson, J. D.; Gibson, T. J.; Higgins, D. G. Clustal W and Clustal X version 2.0 Bioinformatics 2007, 23, 2947-2948
33. Goldman, D.; Lavid, N.; Schwartz, A.; Shoham, G.; Danino, D.; Shoham, Y. Two active forms of Zymomonas mobilis levansucrase. An ordered microfibril structure of the enzyme promotes levan polymerization J. Biol. Chem. 2008, 283, 32209-32217
34. Kim, H.-J.; Park, H.-E.; Kim, M.-J.; Lee, H.-G.; Yang, J.-Y.; Cha, J.-H. Enzymatic characterization of a recombinant levansucrase from Rahnella aquatilis ATCC 15552 J. Microbiol. Biotechnol. 2003, 13, 230-235
35. Dedonder, R. Levansucrase from Bacillus subtilis Methods Enzymol. 1966, 8, 500-505
36. Lyness, E. W.; Doelle, H. W. Levansucrase from Zymomonas mobilis Biotechnol. Lett. 1983, 5, 345-350
37. Homann, A.; Biedendieck, R.; Götze, S.; Jahn, D.; Seibel, J. Insights into polymer versus oligosaccharide synthesis: mutagenesis and mechanistic studies of a novel levansucrase from Bacillus megaterium Biochem. J. 2007, 407, 189-198
38. Hettwer, U.; Gross, M.; Rudolph, K. Purification and characterization of an extracellular levansucrase from Pseudomonas syringae pv. phaseolicola J. Bacteriol. 1995, 177, 2834-2839
39. Ohtsuka, K.; Hino, S.; Fukushima, T.; Ozawa, O.; Kanematsu, T.; Uchida, T. Characterization of levansucrase from Rahnella aquatilis JCM-1683 Biosci., Biotechnol., Biochem. 1992, 56, 1373-1377
40. Tian, F.; Inthanavong, L.; Karbourne, S. Purification and characterization of levansucrases from Bacillus amyloliquefaciens in intra- and extracellular forms useful for the synthesis of levan and fructooligosaccharides Biosci., Biotechnol., Biochem. 2011, 75, 1929-1938
41. Ozimek, L. K.; Kralj, S.; van der Maarel, M. J.; Dijkhuizen, L. The levansucrase and inulosucrase enzymes of Lactobacillus reuteri 121 catalyse processive and non-processive transglycosylation reactions Microbiology 2006, 152, 1187-1196
42. Chambert, R.; Treboule, G.; Dedonder, R. Kinetic studies of levansucrase of Bacillus subtilis Eur. J. Biochem. 1974, 41, 285-300
43. Jang, K. H.; Jang, E. K.; Kim, S. H.; Kim, I. H.; Kang, S. A.; Koh, I.; Park, Y. I.; Kim, Y. J.; Ha, S. D.; Chul, H. K. High-level production of low branched levan from Pseudomonas aurantiaca S-4380 for the production of di-β- d -fructofuranose dianhydride IV J. Microbiol. Biotechnol. 2006, 16, 102-108
44. Borromei, C.; Careri, M.; Cavazza, A.; Corradini, C.; Elviri, L.; Mangia, A.; Merusi, C. Evaluation of fructooligosaccharides and inulins as potentially health benefiting food ingredients by HPAEC-PAD and MALDI-TOF Int. J. Anal. Chem. 2009, 2009, 530639
45. Wang, J.; Sporns, P.; Low, N. H. Analysis of food oligosaccharides using MALDI-MS: quantification of fructoologosaccharides J. Agric. Food Chem. 1999, 47, 1549-1557
46. Visnappu, T.; Mäe, A.; Alamäe, T. Hansenula polymorphamaltase gene promoter with sigma 70-like elements is feasible for Escherichia coli -based biotechnological applications: expression of three genomic levansucrase genes of Pseudomonas syringae pv tomato Process. Biochem. 2008, 43, 414-422
47. Visnappu, T.; Mardo, K.; Mosoarca, C.; Zamfir, A. D.; Vigants, A. Levansucrases from Pseudomonas syringae pv. tomato and P. chlororaphis subsp. aurantiaca: substrate specificity, polymerizing properties and usage of different acceptors for fructosylation J. Biotechnol. 2011, 155, 338-349
48. Seibel, J.; Moraru, R.; Götze, S.; Buchholz, K.; Na'amnieh, S.; Pawlowski, A.; Hecht, H. J. Synthesis of sucrose analogues and the mechanism of action of Bacillus subtilis fructosyltransferase (levansucrase) Carbohydr. Res. 2006, 41, 2335-2349
49. Martínez-Villaluenga, C.; Frías, J.; Vidal-Valverde, C.; Gómez, R. Raffinose family of oligosaccharides from lupin seeds as prebiotics: application in dairy products J. Food Prot. 2005, 68, 1246-1252
50. Abou Hachem, M.; Fredslund, F.; Andersen, J. M.; Jonsgaard Larsen, R.; Majumder, A.; Ejby, M.; Van Zanten, G.; Lahtinen, S. J.; Barrangou, R.; Klaenhammer, T.; Jacobsen, S.; Coutinho, P. M.; Lo Leggio, L.; Svensson, B. Raffinose family oligosaccharide utilisation by probiotic bacteria: insight into substrate recognition, molecular architecture and diversity of GH36 α-galactosidases Biocatal. Biotransfor. 2012, 30, 316-325
51. Ortiz-Soto, M. E.; Rivera, M.; Rudiño-Piñera, E.; Olvera, C.; López-Munguía, A. Selected mutations in Bacillus subtilis levansucrase semi-conserved regions affecting its biochemical properties Protein Eng., Des. Sel. 2008, 2, 589-595