Crystal structure of a compact α-amylase from Geobacillus thermoleovorans

Enzyme and Microbial Technology

Volumn 53, Issue 1, 2013, Pages 46-54

  Mok, Sook Chen ^a   Teh, Aik Hong ^a   Saito, Jennifer A ^a   Najimudin, Nazalan ^a   Alam, Maqsudul ^a,b  

^a SCHOOL OF PHYSICS   (Malaysia)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

Amylase; Acarbose; Ca2+ binding; Compact fold; Crystal structure; Substrate binding; Thermostability

Indexed keywords

ACARBOSE; AROMATIC RESIDUES; COMPACT FOLD; STARCH BINDING DOMAIN; SUBSTRATE AFFINITY; SUBSTRATE BINDING; THERMOSTABILITY; TRANSMEMBRANE REGIONS;

CALCIUM; CRYSTAL STRUCTURE;

AMYLASES;

ACARBOSE; ALPHA AMYLASE SALIVA ISOENZYME; CALCIUM CHLORIDE; CALCIUM ION; EDETIC ACID; AMYLASE; CALCIUM;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; GEOBACILLUS THERMOLEOVORANS; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; THERMOSTABILITY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; CRYSTALLIZATION; ENZYME STABILITY; ENZYMOLOGY; GEOBACILLUS; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

GEOBACILLUS THERMOLEOVORANS;

ACARBOSE; ALPHA-AMYLASES; AMINO ACID SEQUENCE; BINDING SITES; CALCIUM; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; GEOBACILLUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; TEMPERATURE;

EID: 84878018073     PISSN: 01410229     EISSN: 18790909     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2013.03.009     Document Type: Article

References (62)

1. Henrissat B. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochemical Journal 1991, 280:309-316.
2. MacGregor E.A., Janecek S., Svensson B. Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochimica et Biophysica Acta 2001, 1546:1-20.
3. Stam M.R., Danchin E.G., Rancurel C., Coutinho P.M., Henrissat B. Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of α-amylase-related proteins. Protein Engineering Design and Selection 2006, 19:555-562.
4. 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 Research 2009, 37:D233-D238.
5. van der Maarel M.J., van der Veen B., Uitdehaag J.C., Leemhuis H., Dijkhuizen L. Properties and applications of starch-converting enzymes of the α-amylase family. Journal of Biotechnology 2002, 94:137-155.
6. Gupta R., Gigras P., Mohapatra H., Goswami V.K., Chauhan B. Microbial α-amylases: a biotechnological perspective. Process Biochemistry 2003, 38:1599-1616.
7. Goesaert H., Slade L., Levine H., Delcour J.A. Amylases and bread firming - an integrated view. Journal of Cereal Science 2009, 50:345-352.
8. Muhd Sakaff M.K., Abdul Rahman A.Y., Saito J.A., Hou S., Alam M. Complete genome sequence of the thermophilic bacterium Geobacillus thermoleovorans CCB_US3_UF5. Journal of Bacteriology 2012, 194:1239.
9. Finore I., Kasavi C., Poli A., Romano I., Oner E., Kirdar B., et al. Purification, biochemical characterization and gene sequencing of a thermostable raw starch digesting α-amylase from Geobacillus thermoleovorans subsp. stromboliensis subsp. nov. World Journal of Microbiology and Biotechnology 2011, 27:2425-2433.
10. Sun H., Zhao P., Ge X., Xia Y., Hao Z., Liu J., et al. Recent advances in microbial raw starch degrading enzymes. Applied Biochemistry and Biotechnology 2010, 160:988-1003.
11. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences of United States of America 1998, 95:5857-5864.
12. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 2011, 8:785-786.
13. Bernfeld P. Enzymes of starch degradation and synthesis. Advances in Enzymology and Related Subjects of Biochemistry 1951, 12:379-428.
14. Kabsch W. XDS. Acta Crystallographica Section D Biological Crystallography 2010, 66:125-132.
15. Brzozowski A.M., Davies G.J. Structure of the Aspergillus oryzae α-amylase complexed with the inhibitor acarbose at 2.0Å resolution. Biochemistry 1997, 36:10837-10845.
16. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. Journal of Applied Crystallography 1997, 30:1022-1025.
17. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., Echols N., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D Biological Crystallography 2010, 66:213-221.
18. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallographica Section D Biological Crystallography 2010, 66:486-501.
19. Holm L., Rosenstrom P. Dali server: conservation mapping in 3D. Nucleic Acids Research 2010, 38:W545-W549.
20. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
21. Uma Maheswar Rao J.L., Satyanarayana T. Purification and characterization of a hyperthermostable and high maltogenic α-amylase of an extreme thermophile Geobacillus thermoleovorans. Applied Biochemistry and Biotechnology 2007, 142:179-193.
22. Berekaa M.M., Soliman N.A., Abdel-Fattah Y.R. Production, partial characterization and cloning of thermostable α-amylase of a thermophile Geobacillus thermoleovorans YN. Biotechnology 2007, 6:175-183.
23. Malhotra R., Noorwez S.M., Satyanarayana T. Production and partial characterization of thermostable and calcium-independent α-amylase of an extreme thermophile Bacillus thermooleovorans NP54. Letters of Applied Microbiology 2000, 31:378-384.
24. Dheeran P., Kumar S., Jaiswal Y.K., Adhikari D.K. Characterization of hyperthermostable α-amylase from Geobacillus sp. IIPTN. Applied Microbiology and Biotechnology 2010, 86:1857-1866.
25. Vujicic-Zagar A., Dijkstra B.W. Monoclinic crystal form of Aspergillus niger α-amylase in complex with maltose at 1.8Å resolution. Acta Crystallographica Section F Structural Biology and Crystallization Communications 2006, 62:716-721.
26. ®, a thermostable α-amylase. Starch/Stärke 1998, 50:39-45.
27. Dauter Z., Dauter M., Brzozowski A.M., Christensen S., Borchert T.V., Beier L., et al. X-ray structure of Novamyl, the five-domain "maltogenic" α-amylase from Bacillus stearothermophilus: maltose and acarbose complexes at 1.7Å resolution. Biochemistry 1999, 38:8385-8392.
28. Kamasaka H., Sugimoto K., Takata H., Nishimura T., Kuriki T. Bacillus stearothermophilus neopullulanase selective hydrolysis of amylose to maltose in the presence of amylopectin. Applied and Environmental Microbiology 2002, 68:1658-1664.
29. Hondoh H., Kuriki T., Matsuura Y. Three-dimensional structure and substrate binding of Bacillus stearothermophilus neopullulanase. Journal of Molecular Biology 2003, 326:177-188.
30. Tonozuka T., Mogi S., Shimura Y., Ibuka A., Sakai H., Matsuzawa H., et al. Comparison of primary structures and substrate specificities of two pullulan-hydrolyzing α-amylases, TVA I and TVA II, from Thermoactinomyces vulgaris R-47. Biochimica et Biophysica Acta 1995, 1252:35-42.
31. Kamitori S., Kondo S., Okuyama K., Yokota T., Shimura Y., Tonozuka T., et al. Crystal structure of Thermoactinomyces vulgaris R-47 α-amylase II (TVAII) hydrolyzing cyclodextrins and pullulan at 2.6Å resolution. Journal of Molecular Biology 1999, 287:907-921.
32. Kamitori S., Abe A., Ohtaki A., Kaji A., Tonozuka T., Sakano Y. Crystal structures and structural comparison of Thermoactinomyces vulgaris R-47 α-amylase 1 (TVAI) at 1.6Å resolution and α-amylase 2 (TVAII) at 2.3Å resolution. Journal of Molecular Biology 2002, 318:443-453.
33. Kim T.J., Kim M.J., Kim B.C., Kim J.C., Cheong T.K., Kim J.W., et al. Modes of action of acarbose hydrolysis and transglycosylation catalyzed by a thermostable maltogenic amylase, the gene for which was cloned from a Thermus strain. Applied and Environmental Microbiology 1999, 65:1644-1651.
34. Kim J.S., Cha S.S., Kim H.J., Kim T.J., Ha N.C., Oh S.T., et al. Crystal structure of a maltogenic amylase provides insights into a catalytic versatility. Journal of Biological Chemistry 1999, 274:26279-26286.
35. Lee H.S., Kim M.S., Cho H.S., Kim J.I., Kim T.J., Choi J.H., et al. Cyclomaltodextrinase, neopullulanase, and maltogenic amylase are nearly indistinguishable from each other. Journal of Biological Chemistry 2002, 277:21891-21897.
36. Uitdehaag J.C., Kalk K.H., van Der Veen B.A., Dijkhuizen L., Dijkstra B.W. The cyclization mechanism of cyclodextrin glycosyltransferase (CGTase) as revealed by a γ-cyclodextrin-CGTase complex at 1.8Å resolution. Journal of Biological Chemistry 1999, 274:34868-34876.
37. Penninga D., Strokopytov B., Rozeboom H.J., Lawson C.L., Dijkstra B.W., Bergsma J., et al. Site-directed mutations in tyrosine 195 of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 affect activity and product specificity. Biochemistry 1995, 34:3368-3376.
38. Uitdehaag J.C., Mosi R., Kalk K.H., van der Veen B.A., Dijkhuizen L., Withers S.G., et al. X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the α-amylase family. Nature Structural Biology 1999, 6:432-436.
39. Kagawa M., Fujimoto Z., Momma M., Takase K., Mizuno H. Crystal structure of Bacillus subtilis α-amylase in complex with acarbose. Journal of Bacteriology 2003, 185:6981-6984.
40. Gilles C., Astier J.P., Marchis-Mouren G., Cambillau C., Payan F. Crystal structure of pig pancreatic α-amylase isoenzyme II, in complex with the carbohydrate inhibitor acarbose. FEBS Journal 1996, 238:561-569.
41. Qian M., Nahoum V., Bonicel J., Bischoff H., Henrissat B., Payan F. Enzyme-catalyzed condensation reaction in a mammalian α-amylase. High-resolution structural analysis of an enzyme-inhibitor complex. Biochemistry 2001, 40:7700-7709.
42. Leemhuis H., Uitdehaag J.C., Rozeboom H.J., Dijkstra B.W., Dijkhuizen L. The remote substrate binding subsite -6 in cyclodextrin-glycosyltransferase controls the transferase activity of the enzyme via an induced-fit mechanism. Journal of Biological Chemistry 2002, 277:1113-1119.
43. Machovic M., Janecek S. Starch-binding domains in the post-genome era. Cellular and Molecular Life Sciences 2006, 63:2710-2724.
44. Robert X., Haser R., Mori H., Svensson B., Aghajari N. Oligosaccharide binding to barley α-amylase 1. Journal of Biological Chemistry 2005, 280:32968-32978.
45. Hasan K., Tirta Ismaya W., Kardi I., Andiyana Y., Kusumawidjaya S., Ishmayana S., et al. Proteolysis of α-amylase from Saccharomycopsis fibuligera: characterization of digestion products. Biologia (Bratisl) 2008, 63:1044-1050.
46. Hostinova E., Janecek S., Gasperik J. Gene sequence, bioinformatics and enzymatic characterization of α-amylase from Saccharomycopsis fibuligera KZ. Protein Journal 2010, 29:355-364.
47. Puspasari F., Radjasa O.K., Noer A.S., Nurachman Z., Syah Y.M., van der Maarel M., et al. Raw starch-degrading α-amylase from Bacillus aquimaris MKSC 6.2: isolation and expression of the gene, bioinformatics and biochemical characterization of the recombinant enzyme. Journal of Applied Microbiology 2013, 114:108-120.
48. Robert X., Haser R., Gottschalk T.E., Ratajczak F., Driguez H., Svensson B., et al. The structure of barley α-amylase isozyme 1 reveals a novel role of domain C in substrate recognition and binding: a pair of sugar tongs. Structure 2003, 11:973-984.
49. Bozonnet S., Jensen M.T., Nielsen M.M., Aghajari N., Jensen M.H., Kramhoft B., et al. The 'pair of sugar tongs' site on the non-catalytic domain C of barley α-amylase participates in substrate binding and activity. FEBS Journal 2007, 274:5055-5067.
50. Fritzsche H.B., Schwede T., Schulz G.E. Covalent and three-dimensional structure of the cyclodextrinase from Flavobacterium sp. no. 92. European Journal of Biochemistry 2003, 270:2332-2341.
51. Buedenbender S., Schulz G.E. Structural base for enzymatic cyclodextrin hydrolysis. Journal of Molecular Biology 2009, 385:606-617.
52. Chai Y.Y., Rahman R.N., Illias R.M., Goh K.M. Cloning and characterization of two new thermostable and alkalitolerant α-amylases from the Anoxybacillus species that produce high levels of maltose. Journal of Industrial Microbiology and Biotechnology 2012, 39:731-741.
53. Hanrahan V.M., Caldwell M.L. Additional studies of the properties of Taka amylase. Journal of American Chemical Society 1953, 75:4030-4034.
54. Kim Y.W., Kim D.K., Kim M.J., Cha H., Park C.S., Moon T.W., et al. Engineering Thermus maltogenic amylase with improved thermostability: probing the role of the conserved calcium binding site in cyclodextrin-degrading enzymes. Journal of Applied Glycoscience 2005, 52:7-13.
55. Declerck N., Machius M., Wiegand G., Huber R., Gaillardin C. Probing structural determinants specifying high thermostability in Bacillus licheniformis α-amylase. Journal of Molecular Biology 2000, 301:1041-1057.
56. Suzuki Y., Ito N., Yuuki T., Yamagata H., Udaka S. Amino acid residues stabilizing a Bacillus α-amylase against irreversible thermoinactivation. Journal of Biological Chemistry 1989, 264:18933-18938.
57. Igarashi K., Hatada Y., Ikawa K., Araki H., Ozawa T., Kobayashi T., et al. Improved thermostability of a Bacillus α-amylase by deletion of an arginine-glycine residue is caused by enhanced calcium binding. Biochemical and Biophysical Research Communications 1998, 248:372-377.
58. Ben Ali M., Khemakhem B., Robert X., Haser R., Bejar S. Thermostability enhancement and change in starch hydrolysis profile of the maltohexaose-forming amylase of Bacillus stearothermophilus US100 strain. Biochemical Journal 2006, 394:51-56.
59. Lin L.L., Huang C.C., Lo H.F. Impact of Arg210-Ser211 deletion on thermostability of a truncated Bacillus sp. strain TS-23 α-amylase. Process Biochemistry 2008, 43:559-565.
60. Khemakhem B., Ali M.B., Aghajari N., Juy M., Haser R., Bejar S. Engineering of the α-amylase from Geobacillus stearothermophilus US100 for detergent incorporation. Biotechnology and Bioengineering 2009, 102:380-389.
61. Gray J.A., Bemiller J.N. Bread staling: molecular basis and control. Comprehensive Reviews in Food Science and Food Safety 2003, 2:1-21.
62. Kelly R.M., Dijkhuizen L., Leemhuis H. Starch and α-glucan acting enzymes, modulating their properties by directed evolution. Journal of Biotechnology 2009, 140:184-193.