Amylomaltase of Pyrobaculum aerophilum IM2 produces thermoreversible starch gels

Applied and Environmental Microbiology

Volumn 71, Issue 9, 2005, Pages 5098-5106

  Kaper, Thijs ^a,b   Talik, Boguslawa ^a,b   Ettema, Thijs J ^c   Bos, Herman ^d   Van Der Maarel, Marc J E C ^a,d   Dijkhuizen, Lubbert ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d TNO   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; GELS; GLUCOSE; MATHEMATICAL MODELS; PH EFFECTS; STARCH;

ACHAEAL AMYLOMALTASE; AMYLOMALTASE; BINDING MODE; PYROBACULUM AEROPHILUM IM2;

ENZYME KINETICS;

4ALPHA GLUCANOTRANSFERASE; ACARBOSE; CYSTEINE; DISULFIDE; DITHIOTHREITOL; GELATIN; GENE PRODUCT; GLUCAN; GLUCOSE; GLYCOSIDASE; HYDROXYL GROUP; OLIGOSACCHARIDE; POTATO STARCH; STARCH;

ENZYME;

ARCHEAN; ARTICLE; CHEMICAL REACTION KINETICS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; FOOD INDUSTRY; GENE EXPRESSION; HEAT SENSITIVITY; MOLECULAR CLONING; NONHUMAN; PYROBACULUM; PYROBACULUM AEROPHILUM; THERMOSTABILITY;

BINDING SITES; CLONING, MOLECULAR; ENZYME STABILITY; ESCHERICHIA COLI; FOOD INDUSTRY; GELS; GLYCOGEN DEBRANCHING ENZYME SYSTEM; HEAT; KINETICS; PYROBACULUM; STARCH;

ARCHAEA; ESCHERICHIA COLI; PYROBACULUM AEROPHILUM; SOLANUM TUBEROSUM;

EID: 25144432239     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.9.5098-5106.2005     Document Type: Article

References (63)

1. Bhuiyan, S. H., M. Kitaoka, and K. Hayashi. 2003. A cycloamylose-forming hyperthermostable 4-α-glucanotransferase of Aquifex aeolicus expressed in Escherichia coli. J. Mol. Catal. B 22:45-53.
2. Binnema, D. J., and G. J. W. Euverink. 1998. Use of modified starch as an agent for forming a thermoreversible gel. Patent application WO9815347.
3. Bjork, A., B. Dalhus, D. Mantzilas, V. G. Eijsink, and R. Sirevag. 2003. Stabilization of a tetrameric malate dehydrogenase by introduction of a disulfide bridge at the dimer-dimer interface. J. Mol. Biol. 334:811-821.
4. Boos, W., and H. Shuraan. 1998. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol. Mol. Biol. Rev. 62:204-229.
5. Cason, C. J. 2002. Pov-Ray for Windows, 3.5 ed. Pov-Team, Williamstown, Victoria, Australia.
6. Chi, Y. I., L. A. Martinez-Cruz, J. Jancarik, R. V. Swanson, D. E. Robertson, and S. H. Kim. 1999. Crystal structure of the β-glucosidase from the hyperthermophile Thermosphaera aggregans: insights into its activity and thermostability. FEBS Lett. 445:375-383.
7. Colleoni, C., D. Dauville, G. Mouille, A. Bulon, D. Gallant, B. Bouchet, M. Morell, M. Samuel, B, Delrue, C. d'Hulst, C. Bliard, J. M. Nuzillard, and S. Ball. 1999. Genetic and biochemical evidence for the involvement of alpha-1,4 glucanotransferases in amylopectin synthesis. Plant Physiol. 120:993-1004.
8. Colleoni, C., D. Dauville, G. Mouille, M. Morell, M. Samuel, M. C. Slomiany, L. Linard, F. Wattebled, C. d'Hulst, and S. Ball. 1999. Biochemical characterization of the Chlamydomonas reinhardtii alpha-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis. Plant Physiol. 120:1005-1014.
9. Cornish-Bowden, A. 1999. Fundamentals of enzyme kinetics, revised ed. Portland Press, Cambridge, England.
10. Coutinho, P. M., and B. Henrissat. 1999. Carbohydrate-active enzymes: an integrated database approach, p. 3-12. In H. J. Gilbert, G. Davies, B. Henrissat, and B. Svensson (ed.), Recent advances in carbohydrate bioengineering. The Royal Society of Chemistry, Cambridge, United Kingdom.
11. Critchley, J. H., S. C. Zeeman, T. Takaha, A. M. Smith, and S. M. Smith. 2001. A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J. 26:89-100.
12. Davies, G. J., K. S. Wilson, and B. Henrissat. 1997. Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321:557-559. [Letter.]
13. DeDecker, B. S., R. O'Brien, P. J. Fleming, J. H. Geiger, S. P. Jackson, and P. B. Sigler. 1996. The crystal structure of a hyperthermophilic archaeal TATA-box binding protein. J. Mol. Biol. 264:1072-1084.
14. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
15. Fersht, A. 1999. Structure and mechanism in protein science. W. H. Freeman and Company, New York, N.Y.
16. Fitz-Gibbon, S. T., H. Ladner, U. J. Kim, K. O. Stetter, M. I. Simon, and J. H. Miller. 2002. Genome sequence of the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. Proc. Natl. Acad. Sci. USA 99:984-989.
17. Forterre, P., C. Brochier, and H. Philippe. 2002. Evolution of the Archaea. Theor. Popul. Biol. 61:409-422.
18. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
19. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
20. Heinrich, P., W. Huber, and W. Liebl. 1994. Expression in Escherichia coli and structure of the gene encoding 4-α-glucanotransferase from Thermotoga maritima. Classification of maltodextrin glycosyltransferases into two distantly related enzyme subfamilies. Syst. Appl. Microbiol. 17:297-305.
21. Imamura, H., S. Fushinobu, B. S. Jeon, T. Wakagi, and H. Matsuzawa. 2001. Identification of the catalytic residue of Thermococcus litoralis 4-alpha-glucanotransferase through mechanism-based labeling. Biochemistry 40:12400-12406.
22. Imamura, H., S. Fushinobu, M. Yamamoto, T. Kumasaka, B. S. Jeon, T. Wakagi, and H. Matsuzawa. 2003. Crystal structures of 4-alpha-glucanotransferase from Thermococcus litoralis and its complex with an inhibitor. J. Biol. Chem. 278:19378-19386.
23. Jane, J., Y. Y. Chen, L. F. Lee, A. E. McPherson, K. S. Wong, M. Radosavljevic, and T. Kasemsuwan. 1999. Effects of amylopectin branch chain length and amylose content on the gelatinization and pasting properties of starch. Cereal Chem. 76:629-637.
24. Jeon, B. S., H. Taguchi, H. Sakai, T. Ohshima, T. Wakagi, and H. Matsuzawa. 1997. 4-Alpha-glucanotransferase from the hyperthermophilic archaeon Thermococcus litoralis-enzyme purification and characterization, and gene cloning, sequencing and expression in Escherichia coli. Eur. J. Biochem. 248:171-178.
25. Jiang, Y., S. Nock, M. Nesper, M. Sprinzl, and P. B. Sigler. 1996. Structure and importance of the dimerization domain in elongation factor Ts from Thermus thermophilus. Biochemistry 35:10269-10278.
26. Jones, G., and W. J. Whelan. 1969. The action pattern of D-enzyme, a transmaltodextrinylase from potato. Carbohydr. Res. 9:483-490.
27. Kaper, T., M. J. van der Maarel, G. J. Euverink, and L. Dijkhuizen. 2004. Exploring and exploiting starch-modifying amylomaltases from thermophiles. Biochem. Soc. Trans. 32:279-282.
28. Kengen, S., and A. Stams. 1994. An extremely thermostable β-glucosidase from the hyperthermophilic archaeon Pyrococcus furiosus; a comparison with other glycosidases. Biocatalysis 11:79-88.
29. Kim, M. J., S. B. Lee, H. S. Lee, S. Y. Lee, J. S. Baek, D. Kim, T. W. Moon, J. F. Robyt, and K. H. Park. 1999. Comparative study of the inhibition of alpha-glucosidase, alpha-amylase, and cyclomaltodextrin glucanosyltransferase by acarbose, isoacarbose, and acarviosine-glucose. Arch. Biochem. Biophys. 371:277-283.
30. Leemhuis, H., B. W. Dijkstra, and L. Dijkhuizen. 2003, Thermoanaerobacterium thermosulfurigenes cyclodextrin glycosyltransferase. Eur. J. Biochem. 270:155-162.
31. Leemhuis, H., J. C. M. Uitdehaag, H. J. Rozeboom, B. W. Dijkstra, and L. Dijkhuizen. 2002. The remote substrate binding subsite-6 in cydodextrin- glycosyltransferase controls the transferase activity of the enzyme via an induced-fit mechanism. J. Biol. Chem. 277:1113-1119.
32. Liebl, W., R. Feil, J. Gabelsberger, J. Kellermann, and K. H. Schleifer. 1992. Purification and characterization of a novel thermostable 4-alpha-glucano-transferase of Thermotoga maritima cloned in Escherichia coli. Eur. J. Biochem. 207:81-88.
33. MacGregor, E. A., S. Janecek, and B. Svensson. 2001. Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochim. Biophys. Acta 1546:1-20.
34. Mallick, P., D. R. Boutz, D. Eisenberg, and T. O. Yeates. 2002. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc. Natl. Acad. Sci. USA 99:9679-9684.
35. Meissner, H., and W. Liebl. 1998. Thermotoga maritima maltosyltransferase, a novel type of maltodextrin glycosyltransferase acting on starch and maltooligosaccharides. Eur. J. Biochem. 258:1050-1058.
36. Meyer, J., M. D. Clay, M. K. Johnson, A. Stubna, E. Munck, C. Higgins, and P. Wittung-Stafshede. 2002. A hyperthermophilic plant-type [2Fe-2S] ferredoxin from Aquifex aeolicus is stabilized by a disulfide bond. Biochemistry 41:3096-3108.
37. Mosi, R., H. Sham, J. C. M. Uitdehaag, R. Ruiterkamp, B. W. Dijkstra, and S. G. Withers. 1998. Reassessment of acarbose as a transition state analogue inhibitor of cyclodextrin glycosyltransferase. Biochemistry 37:17192-17198.
38. Nielsen, M. S., P. Harris, B. L. Ooi, and H. E. Christensen. 2004. The 1.5 A resolution crystal structure of [Fe(3)S(4)]-ferredoxin from the hyperthermophilic archaeon Pyrococcus furiosus. Biochemistry 43:5188-5194.
39. Ogasahara, K., N. N. Khechinashvili, M. Nakamura, T. Yoshimoto, and K. Yutani. 2001, Thermal stability of pyrrolidone carboxyl peptidases from the hyperthermophilic archaeon, Pyrococcus furiosus. Eur. J. Biochem. 268:3233-3242.
40. Oudjeriouat, N., Y. Moreau, M. Santimone, B. Svensson, G. Marchis-Mouren, and V. Desseaux. 2003. On the mechanism of alpha-amylase, Eur. J. Biochem. 270:3871-3879.
41. Przylas, I., Y. Terada, K. Fujii, T. Takaha, W. Saenger, and N. Strater. 2000. X-ray structure of acarbose bound to amylomaltase from Thermus aquaticus. Implications for the synthesis of large cyclic glucans. Eur. J. Biochem, 267:6903-6913.
42. Przylas, I., K. Tomoo, Y. Terada, T. Takaha, K. Fujii, W. Saenger, and N. Strater. 2000. Crystal structure of amylomaltase from Thermus aquaticus, a glycosyltransferase catalysing the production of large cyclic glucans. J. Mol. Biol. 296:873-886.
43. Rüegg, U. T., and J. Rudinger. 1977. Reductive cleavage of cystine disulfides with tributyl phosphine. Methods Enzymol. 47:111-116.
44. Siebers, B., B. Tjaden, K. Michalke, C. Dorr, H. Ahmed, M. Zaparty, P. Gordon, C. W. Sensen, A. Zibat, H. P. Klenk, S. C. Schuster, and R. Hensel. 2004. Reconstruction of the central carbohydrate metabolism of Thermoproteus tenax by use of genomic and biochemical data. J. Bacteriol. 186:2179-2194.
45. Sogaard, M., A. Kadziola, R. Haser, and B. Svensson. 1993. Site-directed mutagenesis of histidine 93, aspartic acid 180, glutamic acid 205, histidine 290, and aspartic acid 291 at the active site and tryptophan 279 at the raw starch binding site in barley alpha-amylase 1. J. Biol. Chem. 268:22480-22484.
46. Spiro, G. 1966. Analysis of sugars found in glycoproteins. Methods Enzymol. 8:3-26.
47. Takaha, T., M. Yanase, S. Okada, and S. M. Smith. 1993. Disproportionating enzyme (4-alpha-glucanotransferase; EC 2.4.1.25) of potato. Purification, molecular cloning, and potential role in starch metabolism. J. Biol. Chem. 268:1391-1396.
48. Takaha, T., M. Yanase, H. Takata, S. Okada, and S. M. Smith. 1998. Cyclic glucans produced by the intramolecular transglycosylation activity of potato D-enzyme on amylopectin. Biochem. Biophys. Res. Commun. 247:493-497.
49. Takaha, T., M. Yanase, H. Takata, S. Okada, and S. M. Smith. 1996. Potato D-enzyme catalyzes the cyclization of amylose to produce cycloamylose, a novel cyclic glucan. J. Biol. Chem. 271:2902-2908.
50. Terada, Y., K. Fujii, T. Takaha, and S. Okada. 1999. Thermus aquaticus ATCC 33923 amylomaltase gene cloning and expression and enzyme characterization: production of cycloamylose. Appl. Environ. Microbiol. 65:910-915.
51. Uitdehaag, J. C. M., R. Mosi, K. H. Kalk, B. A. van der Veen, L. Dijkhuizen, S. G. Withers, and B. W. Dijkstra. 1999. X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the alpha-amylase family. Nat. Struct. Biol. 6:432-436.
52. Van der Maarel, M. J. E. C., G. J. W. Euverink, D. J. Binnema, H. T. P. Bos, and J. Bergsma. 2000. Amylomaltase from the hyperthermophilic bacterium Thermus thermophilus: enzyme characteristics and application in the starch industry. Med. Fac. Landbouww Univ. Gent 65/3a:231-234.
53. van der Veen, B. A., G. J. van Alebeek, J. C. M. Uitdehaag, B. W. Dijkstra, and L. Dijkhuizen. 2000. The three transglycosylation reactions catalyzed by cyclodextrin glycosyltransferase from Bacillus circulans (strain 251) proceed via different kinetic mechanisms. Eur. J. Biochem. 267:658-665.
54. Viles, F. J., and L. Silverman. 1949. Determination of starch and celluloses with anthrone. Anal. Chem. 21:950-953.
55. Volkl, P., R. Huber, E. Drobner, R. Rachel, S. Burggraf, A. Trincone, and K. O. Stetter. 1993. Pyrobaculum aerophilum sp. nov., a novel nitrate-reducing hyperthermophilic archaeum. Appl. Environ. Microbiol. 59:2918-2926.
56. von Mering, C., M. Huynen, D. Jaeggi, S. Schmidt, P. Bork, and B. Snel. 2003. STRING: a database of predicted functional associations between proteins. Nucleic Acids Res. 31:258-261.
57. Vriend, G. 1990. What If: a molecular modeling and drug design program. J. Mol. Graph. 8:52-56.
58. Vriend, G. 3 June 2003, posting date. The Whatlf Webserver interface. [Online.] http://www.cmbi.kun.nl/gv/servers/WIWWWI/.
59. Wattebled, F., J. P. Ral, D. Dauvillee, A. M. Myers, M. G. James, R. Schlichting, C. Giersch, S. G. Ball, and C. D'Hulst. 2003. STA11, a Chlamydomonas reinhardtii locus required for normal starch granule biogenesis, encodes disproportionating enzyme. Further evidence for a function of alpha-1,4 glucanotransferases during starch granule biosynthesis in green algae. Plant Physiol. 132:137-145.
60. Woese, C. R., O. Kandler, and M. L. Wheelis. 1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA 87:4576-4579.
61. Xavier, K. B., R. Peist, M. Kossmann, W. Boos, and H. Santos. 1999. Maltose metabolism in the hyperthermophilic archaeon Thermococcus litoralis: purification and characterization of key enzymes. J. Bacteriol. 181:3358-3367.
62. Yoon, S. H., and J. F. Robyt. 2003. Study of the inhibition of four alpha amylases by acarbose and its 4-alpha-maltohexaosyl and 4-alpha-maltododecaosyl analogues. Carbohydr. Res. 338:1969-1980.
63. Zona, R., F. Chang-Pi-Hin, M. J. O'Donohue, and S. Janecek. 2004. Bioinformatics of the glycoside hydrolase family 57 and identification of catalytic residues in amylopullulanase from Thermococcus hydrothermalis. Eur. J. Biochem. 271:2863-2872.