The Gram-negative bacterium Azotobacter chroococcum NCIMB 8003 employs a new glycoside hydrolase family 70 4,6-α-glucanotransferase enzyme (GtfD) to synthesize a reuteran like polymer from maltodextrins and starch

Biochimica et Biophysica Acta - General Subjects

Volumn 1860, Issue 6, 2016, Pages 1224-1236

  Gangoiti, Joana ^a   Van Leeuwen, Sander S ^a   Vafiadi, Christina ^b   Dijkhuizen, Lubbert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

4,6 glucanotransferase; Azotobacter chroococcum; Family GH70; Glucansucrase; Isomalto malto polysaccharide; Reuteran

Indexed keywords

AMYLOSE; CHEMICAL COMPOUND; GLUCAN; GLYCOSIDASE; GLYCOSIDE HYDROLASE FAMILY 70 4,6 ALPHA GLUCANOTRANSFERASE; MALTODEXTRIN; OLIGOSACCHARIDE; REUTERAN; STARCH; SUCROSE; UNCLASSIFIED DRUG; 4 ALPHA-GLUCANOTRANSFERASE; GLYCOGEN DEBRANCHING ENZYME; POLYSACCHARIDE;

ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; AZOTOBACTER CHROOCOCCUM; BACTERIAL GENE; BIOCHEMICAL COMPOSITION; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME SYNTHESIS; GTFD GENE; HIGH PERFORMANCE ANION EXCHANGE CHROMATOGRAPHY; HIGH PERFORMANCE SIZE EXCLUSION CHROMATOGRAPHY; HYDROLYSIS; LINKAGE ANALYSIS; METHYLATION; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE ANALYSIS; SIZE EXCLUSION CHROMATOGRAPHY; THIN LAYER CHROMATOGRAPHY; AMINO ACID SEQUENCE; AZOTOBACTER; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; AZOTOBACTER; GLUCANS; GLYCOGEN DEBRANCHING ENZYME SYSTEM; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; POLYSACCHARIDES; STARCH; SUBSTRATE SPECIFICITY;

EID: 84960899367     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2016.02.005     Document Type: Article

References (46)

1. V. Lombard, H. Golaconda Ramulu, E. Drula, P.M. Coutinho, and B. Henrissat The carbohydrate-active enzymes database (CAZy) in 2013 Nucleic Acids Res. 42 2014 D490 D495 10.1093/nar/gkt1178
2. M.R. Stam, E.G. Danchin, C. Rancurel, P.M. Coutinho, and B. Henrissat Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins Protein Eng. Des. Sel. 19 2006 555 562 (doi:gzl044)
3. S. Janecek, B. Svensson, and E.A. MacGregor Alpha-amylase: an enzyme specificity found in various families of glycoside hydrolases Cell. Mol. Life Sci. 71 2014 1149 1170 10.1007/s00018-013-1388-z
4. A. Vujičić-Žagar, T. Pijning, S. Kralj, C.A. Lopez, W. Eeuwema, L. Dijkhuizen, and B.W. Dijkstra 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 2010 21406 21411 10.1073/pnas.1007531107
5. K. Ito, S. Ito, T. Shimamura, S. Weyand, Y. Kawarasaki, T. Misaka, K. Abe, T. Kobayashi, A.D. Cameron, and S. Iwata Crystal structure of glucansucrase from the dental caries pathogen Streptococcus mutans J. Mol. Biol. 408 2011 177 186 10.1016/j.jmb.2011.02.028
6. Y. Brison, T. Pijning, Y. Malbert, E. Fabre, L. Mourey, S. Morel, G. Potocki-Veronese, P. Monsan, S. Tranier, M. Remaud-Simeon, and B.W. Dijkstra Functional and structural characterization of alpha-(1 → 2) branching sucrase derived from DSR-E glucansucrase J. Biol. Chem. 287 2012 7915 7924 10.1074/jbc.M111.305078
7. T. Pijning, A. Vujicic-Zagar, S. Kralj, L. Dijkhuizen, and B.W. Dijkstra Structure of the alpha-1,6/alpha-1,4-specific glucansucrase GTFA from Lactobacillus reuteri 121 Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 68 2012 1448 1454 10.1107/S1744309112044168
8. E.A. MacGregor, H.M. Jespersen, and B. Svensson A circularly permuted alpha-amylase-type alpha/beta-barrel structure in glucan-synthesizing glucosyltransferases FEBS Lett. 378 1996 263 266 10.1016/0014-5793(95)01428-4
9. E.A. MacGregor, S. Janecek, and B. Svensson Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes Biochim. Biophys. Acta 1546 2001 1 20 10.1016/S0167-4838(00)00302-2
10. X. Meng, J.M. Dobruchowska, T. Pijning, G.J. Gerwig, J.P. Kamerling, and L. Dijkhuizen Truncation of domain V of the multidomain glucansucrase GTF180 of Lactobacillus reuteri 180 heavily impairs its polysaccharide-synthesizing ability Appl. Microbiol. Biotechnol. 2015 10.1007/s00253-014-6361-8
11. Y. Bai, R.M. van der Kaaij, H. Leemhuis, T. Pijning, S.S. van Leeuwen, Z. Jin, and L. Dijkhuizen Biochemical characterization of the Lactobacillus reuteri glycoside hydrolase family 70 GTFB type of 4,6-alpha-glucanotransferase enzymes that synthesize soluble dietary starch fibers Appl. Environ. Microbiol. 81 2015 7223 7232 10.1128/AEM.01860-15
12. J. Gangoiti, T. Pijning, and L. Dijkhuizen Biochemical characterization of the Exiguobacterium sibiricum 255-15 GtfC enzyme representing a novel glycoside hydrolase 70 subfamily of 4,6-a-glucanotransferase enzymes Appl. Environ. Microbiol. 82 2015 756 766 10.1128/AEM.03420-15
13. M. Machius, G. Wiegand, and R. Huber Crystal structure of calcium-depleted Bacillus licheniformis alpha-amylase at 2.2 A resolution J. Mol. Biol. 246 1995 545 559 10.1016/S0022-2836(03)00633-8
14. S. Kralj, P. Grijpstra, S.S. van Leeuwen, H. Leemhuis, J.M. Dobruchowska, R.M. van der Kaaij, A. Malik, A. Oetari, J.P. Kamerling, and L. Dijkhuizen 4,6-Alpha-glucanotransferase, a novel enzyme that structurally and functionally provides an evolutionary link between glycoside hydrolase enzyme families 13 and 70 Appl. Environ. Microbiol. 77 2011 8154 8163 10.1128/AEM.05735-11
15. Y. Bai, R.M. van der Kaaij, A.J. Woortman, Z. Jin, and L. Dijkhuizen Characterization of the 4,6-alpha-glucanotransferase GTFB enzyme of Lactobacillus reuteri 121 isolated from inclusion bodies BMC Biotechnol. 15 2015 10.1186/s12896-015-0163-7 (49-015-0163-7)
16. J.M. Dobruchowska, G.J. Gerwig, S. Kralj, P. Grijpstra, H. Leemhuis, L. Dijkhuizen, and J.P. Kamerling Structural characterization of linear isomalto-/malto-oligomer products synthesized by the novel GTFB 4,6-alpha-glucanotransferase enzyme from Lactobacillus reuteri 121 Glycobiology 22 2012 517 528 10.1093/glycob/cwr167
17. L. Dijkhuizen, M.J.E.C. Van der Maarel, J.P. Kamerling, R.J. Leemuis, S. Kralj, and J.M. Dobruchowska Glucooligosaccharides comprising (alpha 1 → 4) and (alpha 1 → 6) glycosidic bonds, use thereof, and methods for producing them EP 2 2010 427 565 (B1)
18. H. Leemhuis, J.M. Dobruchowska, M. Ebbelaar, F. Faber, P.L. Buwalda, M.J. van der Maarel, J.P. Kamerling, and L. Dijkhuizen Isomalto/malto-polysaccharide, a novel soluble dietary fiber made via enzymatic conversion of starch J. Agric. Food Chem. 62 2014 12034 12044 10.1021/jf503970a
19. S. Kralj, G.H. van Geel-Schutten, H. Rahaoui, R.J. Leer, E.J. Faber, M.J. van der Maarel, and L. Dijkhuizen Molecular characterization of a novel glucosyltransferase from Lactobacillus reuteri strain 121 synthesizing a unique, highly branched glucan with alpha-(1 → 4) and alpha-(1 → 6) glucosidic bonds Appl. Environ. Microbiol. 68 2002 4283 4291
20. S.S. van Leeuwen, S. Kralj, I.H. van Geel-Schutten, G.J. Gerwig, L. Dijkhuizen, and J.P. Kamerling Structural analysis of the alpha-D-glucan (EPS35-5) produced by the Lactobacillus reuteri strain 35-5 glucansucrase GTFA enzyme Carbohydr. Res. 343 2008 1251 1265 10.1016/j.carres.2008.01.044
21. J.M. Dobruchowska, X. Meng, H. Leemhuis, G.J. Gerwig, L. Dijkhuizen, and J.P. Kamerling Gluco-oligomers initially formed by the reuteransucrase enzyme of Lactobacillus reuteri 121 incubated with sucrose and malto-oligosaccharides Glycobiology 23 2013 1084 1096 10.1093/glycob/cwt048
22. S. Kralj, G.H. van Geel-Schutten, M.J. van der Maarel, and L. Dijkhuizen Biochemical and molecular characterization of Lactobacillus reuteri 121 reuteransucrase Microbiology 150 2004 2099 2112 10.1099/mic.0.27105-0
23. R.L. Robson, R. Jones, R.M. Robson, A. Schwartz, and T.H. Richardson Azotobacter genomes: The genome of Azotobacter chroococcum NCIMB 8003 (ATCC 4412) PLoS One 10 2015 e0127997 10.1371/journal.pone.0127997
24. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: molecular evolutionary genetics analysis version 6.0 Mol. Biol. Evol. 30 2013 2725 2729 10.1093/molbev/mst197
25. A.M. Waterhouse, J.B. Procter, D.M. Martin, M. Clamp, and G.J. Barton Jalview version 2 - a multiple sequence alignment editor and analysis workbench Bioinformatics 25 2009 1189 1191 10.1093/bioinformatics/btp033
26. S.S. van Leeuwen, S. Kralj, I.H. van Geel-Schutten, G.J. Gerwig, L. Dijkhuizen, and J.P. Kamerling Structural analysis of the alpha-D-glucan (EPS180) produced by the Lactobacillus reuteri strain 180 glucansucrase GTF180 enzyme Carbohydr. Res. 343 2008 1237 1250 10.1016/j.carres.2008.01.042
27. R.L. Robson, J.A. Chesshyre, C. Wheeler, R. Jones, P.R. Woodley, and J.R. Postgate Genome size and complexity in Azotobacter chroococcum J. Gen. Microbiol. 130 1984 1603 1612 10.1099/00221287-130-7-1603
28. R.L. Robson Nitrogen fixation in strains of Azotobacter chroococcum bearing deletions of a cluster of genes coding for nitrogenase Arch. Microbiol. 146 1986 74 79
29. G.L. Lawson, and M. Stacey Immunopolysaccharides. I. Preliminary studies of a polysaccharide from Azotobacter chroococcum containing an uronic acid J. Chem. Soc. 1954 1954 1925 1931
30. G.L. Cote, and L.H. Krull Characterization of the exocellular polysaccharides from Azotobacter chroococcum Carbohydr. Res. 181 1988 143 152 10.1016/0008-6215(88)84030-8
31. K. Bath, S. Roos, T. Wall, and H. Jonsson The cell surface of Lactobacillus reuteri ATCC 55730 highlighted by identification of 126 extracellular proteins from the genome sequence FEMS Microbiol. Lett. 253 2005 75 82 10.1128/AEM.00659-06
32. S.A. van Hijum, S. Kralj, L.K. Ozimek, L. Dijkhuizen, and I.G. van Geel-Schutten Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria Microbiol. Mol. Biol. Rev. 70 2006 157 176 doi:70/1/157
33. H. Leemhuis, W.P. Dijkman, J.M. Dobruchowska, T. Pijning, P. Grijpstra, S. Kralj, J.P. Kamerling, and L. Dijkhuizen 4,6-alpha-glucanotransferase activity occurs more widespread in Lactobacillus strains and constitutes a separate GH70 subfamily Appl. Microbiol. Biotechnol. 97 2013 181 193 10.1007/s00253-012-3943-1
34. S.S. van Leeuwen, S. Kralj, W. Eeuwema, G.J. Gerwig, L. Dijkhuizen, and J.P. Kamerling Structural characterization of bioengineered alpha-D-glucans produced by mutant glucansucrase GTF180 enzymes of Lactobacillus reuteri strain 180 Biomacromolecules 10 2009 580 588 10.1021/bm801240r
35. S. Kralj, E. Stripling, P. Sanders, G.H. van Geel-Schutten, and L. Dijkhuizen Highly hydrolytic reuteransucrase from probiotic Lactobacillus reuteri strain ATCC 55730 Appl. Environ. Microbiol. 71 2005 3942 3950 (doi:71/7/3942)
36. J.C. Uitdehaag, G.J. van Alebeek, B.A. van Der Veen, L. Dijkhuizen, and B.W. Dijkstra Structures of maltohexaose and maltoheptaose bound at the donor sites of cyclodextrin glycosyltransferase give insight into the mechanisms of transglycosylation activity and cyclodextrin size specificity Biochemistry 39 2000 7772 7780 (doi:bi000340x)
37. I. Przylas, Y. Terada, K. Fujii, T. Takaha, W. Saenger, and Strater N. X-ray structure of acarbose bound to amylomaltase from Thermus aquaticus. Implications for the synthesis of large cyclic glucans Eur. J. Biochem. 267 2000 6903 6913 (doi:ejb1790)
38. T. Kaper, H. Leemhuis, J.C. Uitdehaag, B.A. van der Veen, B.W. Dijkstra, M.J. van der Maarel, and L. Dijkhuizen Identification of acceptor substrate binding subsites + 2 and + 3 in the amylomaltase from Thermus thermophilus HB8 Biochemistry 46 2007 5261 5269 10.1021/bi602408j
39. T.R. Barends, J.B. Bultema, T. Kaper, M.J. van der Maarel, L. Dijkhuizen, and B.W. Dijkstra Three-way stabilization of the covalent intermediate in amylomaltase, an alpha-amylase-like transglycosylase J. Biol. Chem. 282 2007 17242 17249 (doi:M701444200)
40. M. Palomo, T. Pijning, T. Booiman, J.M. Dobruchowska, J. van der Vlist, S. Kralj, A. Planas, K. Loos, J.P. Kamerling, B.W. Dijkstra, M.J. van der Maarel, L. Dijkhuizen, and H. Leemhuis Thermus thermophilus glycoside hydrolase family 57 branching enzyme: crystal structure, mechanism of action, and products formed J. Biol. Chem. 286 2011 3520 3530 10.1074/jbc.M110.179515
41. F. Grimaud, C. Lancelon-Pin, A. Rolland-Sabate, X. Roussel, S. Laguerre, A. Vikso-Nielsen, J.L. Putaux, S. Guilois, A. Buleon, C. D'Hulst, and G. Potocki-Veronese In vitro synthesis of hyperbranched alpha-glucans using a biomimetic enzymatic toolbox Biomacromolecules 14 2013 438 447 10.1021/bm301676c
42. M. Naessens, A. Cerdobbel, W. Soetaert, and E.J. Vandamme Dextran dextrinase and dextran of Gluconobacter oxydans J. Ind. Microbiol. Biotechnol. 32 2005 323 334 10.1007/s10295-005-0259-5
43. Ekhart P, van Geel-Schutten GH, Van Binsbergen M, Timmerman E. 2006. Branched alpha-glucans for weight management. US 20060100171 A1.
44. Plijter J, Jurgens A, Kats MP, Noort MWJ, Heddes CEA, Van Geel Schutten GH. 2009. Bread improver. US 20090297663 A1.
45. C. Núñez, S. Moreno, G. Soberon-Chavez, and G. Espin The Azotobacter vinelandii response regulator AlgR is essential for cyst formation J. Bacteriol. 181 1999 141 148
46. W. Sabra, A.P. Zeng, H. Lunsdorf, and W.D. Deckwer Effect of oxygen on formation and structure of Azotobacter vinelandii alginate and its role in protecting nitrogenase Appl. Environ. Microbiol. 66 2000 4037 4044