Two potentially novel amylolytic enzyme specificities in the prokaryotic glycoside hydrolase α-amylase family GH57

Microbiology (United Kingdom)

Volumn 159, Issue PART 12, 2013, Pages 2584-2593

  Blesák, Karol ^a   Janeček, Štefan ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; 4ALPHA GLUCANOTRANSFERASE; ALPHA GALACTOSIDASE; AMYLASE; AMYLOPULLULANASE; GLYCOSIDASE; GLYCOSIDE HYDROLASE 57; UNCLASSIFIED DRUG;

ARCHAEON; ARTICLE; BACTERIUM; BIOINFORMATICS; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROKARYOTE; SEQUENCE DATABASE; STRUCTURE ACTIVITY RELATION;

ALPHA-AMYLASES; ARCHAEA; BACTERIA; CATALYTIC DOMAIN; COMPUTATIONAL BIOLOGY; MODELS, MOLECULAR; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84888878302     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.071084-0     Document Type: Article

References (62)

1. Aghajari, N., Haser, R., Feller, G. & Gerday, C. (1998). Crystal structures of the psychrophilic a-amylase from Alteromonas haloplanctis in its native form and complexed with an inhibitor. Protein Sci 7, 564-572.
2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
3. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. (2006). The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201.
4. Ball, S., Colleoni, C., Cenci, U., Raj, J. N. & Tirtiaux, C. (2011). The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 62, 1775-1801.
5. Ballschmiter, M., Fütterer, O. & Liebl, W. (2006). Identification and characterization of a novel intracellular alkaline a-amylase from the hyperthermophilic bacterium Thermotoga maritima MSB8. Appl Environ Microbiol 72, 2206-2211.
6. Benson, D. A., Karsch-Mizrachi, I., Clark, K., Lipman, D. J., Ostell, J. & Sayers, E. W. (2012). GenBank. Nucleic Acids Res 40 (Database issue), D48-D53.
7. Blesák, K. & Janeček, S. (2012). Sequence fingerprints of enzyme specificities from the glycoside hydrolase family GH57. Extremophiles 16, 497-506.
8. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V. & Henrissat, B. (2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37 (Database issue), D233-D238.
9. Comfort, D. A., Chou, C. J., Conners, S. B., VanFossen, A. L. & Kelly, R. M. (2008). Functional-genomics-based identification and characterization of open reading frames encoding a-glucoside-processing enzymes in the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 74, 1281-1283.
10. Coutinho, P. M. & Reilly, P. J. (1997). Glucoamylase structural, functional, and evolutionary relationships. Proteins 29, 334-347.
11. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. (2004). WebLogo: a sequence logo generator. Genome Res 14, 1188-1190.
12. Da Lage, J. L., Danchin, E. G. & Casane, D. (2007). Where do animal aamylases come from? An interkingdom trip. FEBS Lett 581, 3927-3935.
13. Davies, G. J., Wilson, K. S. & Henrissat, B. (1997). Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem J 321, 557-559.
14. Deshpande, N., Addess, K. J., Bluhm, W. F., Merino-Ott, J. C., Townsend-Merino, W., Zhang, Q., Knezevich, C., Xie, L., Chen, L. & other authors (2005). The RCSB Protein Data Bank: a redesigned query system and relational database based on the mmCIF schema. Nucleic Acids Res 33 (Suppl. 1, Database issue), D233-D237.
15. Dickmanns, A., Ballschmiter, M., Liebl, W. & Ficner, R. (2006). Structure of the novel a-amylase AmyC from Thermotoga maritima. Acta Crystallogr D Biol Crystallogr 62, 262-270.
16. Dong, G., Vieille, C. & Zeikus, J. G. (1997). Cloning, sequencing, and expression of the gene encoding amylopullulanase from Pyrococcus furiosus and biochemical characterization of the recombinant enzyme. Appl Environ Microbiol 63, 3577-3584.
17. Erra-Pujada, M., Debeire, P., Duchiron, F. & O'Donohue, M. J. (1999). The type II pullulanase of Thermococcus hydrothermalis: molecular characterization of the gene and expression of the catalytic domain. J Bacteriol 181, 3284-3287.
18. Felsenstein, J. (1985). Confidence limits on phylogenies-an approach using the bootstrap. Evolution 39, 783-791.
19. Ficko-Blean, E., Stuart, C. P. & Boraston, A. B. (2011). Structural analysis of CPF_2247, a novel a-amylase from Clostridium perfringens. Proteins 79, 2771-2777.
20. Fukusumi, S., Kamizono, A., Horinouchi, S. & Beppu, T. (1988). Cloning and nucleotide sequence of a heat-stable amylase gene from an anaerobic thermophile, Dictyoglomus thermophilum. Eur J Biochem 174, 15-21.
21. Henrissat, B. (1991). A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280, 309-316.
22. Henrissat, B. & Bairoch, A. (1996). Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316, 695-696.
23. Imamura, H., Fushinobu, S., Yamamoto, M., Kumasaka, T., Jeon, B. S., Wakagi, T. & Matsuzawa, H. (2003). Crystal structures of 4-aglucanotransferase from Thermococcus litoralis and its complex with an inhibitor. J Biol Chem 278, 19378-19386.
24. Imamura, H., Jeon, B. S. & Wakagi, T. (2004). Molecular evolution of the ATPase subunit of three archaeal sugar ABC transporters. Biochem Biophys Res Commun 319, 230-234.
25. Janeček, Š. (1997). a-Amylase family: molecular biology and evolution. Prog Biophys Mol Biol 67, 67-97.
26. Janeček, Š. (1998). Sequence of archaeal Methanococcus jannaschii aamylase contains features of families 13 and 57 of glycosyl hydrolases: a trace of their common ancestor? Folia Microbiol (Praha) 43, 123-128.
27. Janeček, Š. & Blesák, K. (2011). Sequence-structural features and evolutionary relationships of family GH57 a-amylases and their putative a-amylase-like homologues. Protein J 30, 429-435.
28. Janeček, Š. & Kuchtová, A. (2012). In silico identification of catalytic residues and domain fold of the family GH119 sharing the catalytic machinery with the a-amylase family GH57. FEBS Lett 586, 3360-3366.
29. Janeček, Š., Svensson, B. & MacGregor, E. A. (2011). Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzyme Microb Technol 49, 429-440.
30. Janeček, Š., Svensson, B. & Macgregor, E. A. (2013). a-Amylase: an enzyme specificity found in various families of glycoside hydrolases. Cell Mol Life Sci, doi: 10.1007/s00018-013-1388-z (in press).
31. Jeon, B. S., Taguchi, H., Sakai, H., Ohshima, T., Wakagi, T. & Matsuzawa, H. (1997). 4-a-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.
32. Jespersen, H. M., MacGregor, E. A., Sierks, M. R. & Svensson, B. (1991). Comparison of the domain-level organization of starch hydrolases and related enzymes. Biochem J 280, 51-55.
33. Jiao, Y. L., Wang, S. J., Lv, M. S., Xu, J. L., Fang, Y. W. & Liu, S. (2011). A GH57 family amylopullulanase from deep-sea Thermococcus siculi: expression of the gene and characterization of the recombinant enzyme. Curr Microbiol 62, 222-228.
34. Katsuya, Y., Mezaki, Y., Kubota, M. & Matsuura, Y. (1998). Threedimensional structure of Pseudomonas isoamylase at 2.2 A ° resolution. J Mol Biol 281, 885-897.
35. Kelley, L. A. & Sternberg, M. J. (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4, 363-371.
36. Kim, J. W., Flowers, L. O., Whiteley, M. & Peeples, T. L. (2001). Biochemical confirmation and characterization of the family-57-like aamylase of Methanococcus jannaschii. Folia Microbiol (Praha) 46, 467-473.
37. Labes, A. & Schönheit, P. (2007). Unusual starch degradation pathway via cyclodextrins in the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus strain 7324. J Bacteriol 189, 8901-8913.
38. Laderman, K. A., Asada, K., Uemori, T., Mukai, H., Taguchi, Y., Kato, I. & Anfinsen, C. B. (1993a). a-amylase from the hyperthermophilic archaebacterium Pyrococcus furiosus. Cloning and sequencing of the gene and expression in Escherichia coli. J Biol Chem 268, 24402-24407.
39. Laderman, K. A., Davis, B. R., Krutzsch, H. C., Lewis, M. S., Griko, Y. V., Privalov, P. L. & Anfinsen, C. B. (1993b). The purification and characterization of an extremely thermostable a-amylase from the hyperthermophilic archaebacterium Pyrococcus furiosus. J Biol Chem 268, 24394-24401.
40. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & other authors (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
41. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26, 283-291.
42. Laskowski, R. A., Hutchinson, E. G., Michie, A. D., Wallace, A. C., Jones, M. L. & Thornton, J. M. (1997). PDBsum: a Web-based database of summaries and analyses of all PDB structures. Trends Biochem Sci 22, 488-490.
43. Li, X., Li, D. & Park, K. H. (2013). An extremely thermostable amylopullulanase from Staphylothermus marinus displays both pullulan-and cyclodextrin-degrading activities. Appl Microbiol Biotechnol 97, 5359-5369.
44. MacGregor, E. A. & Svensson, B. (1989). A super-secondary structure predicted to be common to several a-1,4-D-glucan-cleaving enzymes. Biochem J 259, 145-152.
45. MacGregor, E. A., Janecek, S. & Svensson, B. (2001). Relationship of sequence and structure to specificity in the a-amylase family of enzymes. Biochim Biophys Acta 1546, 1-20.
46. Murakami, T., Kanai, T., Takata, H., Kuriki, T. & Imanaka, T. (2006). A novel branching enzyme of the GH-57 family in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Bacteriol 188, 5915-5924.
47. Nakajima, M., Imamura, H., Shoun, H., Horinouchi, S. & Wakagi, T. (2004). Transglycosylation activity of Dictyoglomus thermophilum amylase A. Biosci Biotechnol Biochem 68, 2369-2373.
48. Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357-358.
49. Palomo, M., Pijning, T., Booiman, T., Dobruchowska, J. M., van der Vlist, J., Kralj, S., Planas, A., Loos, K., Kamerling, J. P. & other authors (2011). Thermus thermophilus glycoside hydrolase family 57 branching enzyme: crystal structure, mechanism of action, and products formed. J Biol Chem 286, 3520-3530.
50. Pujadas, G., Ramírez, F. M., Valero, R. & Palau, J. (1996). Evolution of b-amylase: patterns of variation and conservation in subfamily sequences in relation to parsimony mechanisms. Proteins 25, 456-472.
51. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G. & other authors (2012). The Pfam protein families database. Nucleic Acids Res 40 (Database issue), D290-D301.
52. Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
53. Santos, C. R., Tonoli, C. C., Trindade, D. M., Betzel, C., Takata, H., Kuriki, T., Kanai, T., Imanaka, T., Arni, R. K. & Murakami, M. T. (2011). Structural basis for branching-enzyme activity of glycoside hydrolase family 57: structure and stability studies of a novel branching enzyme from the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. Proteins 79, 547-557.
54. Shatsky, M., Nussinov, R. & Wolfson, H. J. (2004). A method for simultaneous alignment ofmultiple protein structures. Proteins 56, 143-156.
55. Smith, A. M., Zeeman, S. C. & Smith, S. M. (2005). Starch degradation. Annu Rev Plant Biol 56, 73-98.
56. Tachibana, Y., Fujiwara, S., Takagi, M. & Imanaka, T. (1997). Cloning and expression of the 4-a-glucanotransferase gene from the hyperthermophilic archaeon Pyrococcus sp. KOD1, and characterization of the enzyme. J Ferment Bioeng 83, 540-548.
57. Takata, H., Kuriki, T., Okada, S., Takesada, Y., Iizuka, M., Minamiura, N. & Imanaka, T. (1992). Action of neopullulanase. Neopullulanase catalyzes both hydrolysis and transglycosylation at a-(1-4)-and a-(1-6)-glucosidic linkages. J Biol Chem 267, 18447-18452.
58. UniProt Consortium (2012). Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40 (Database issue), D71-D75.
59. van Lieshout, J. F. T., Verhees, C. H., Ettema, T. J. G., van der Sar, S., Imamura, H., Matsuzawa, H., van der Oost, J. & de Vos, W. M. (2003). Identification and molecular characterization of a novel type of a-galactosidase from Pyrococcus furiosus. Biocatalysis Biotransformation 21, 243-252.
60. Wang, H., Gong, Y., Xie, W., Xiao, W., Wang, J., Zheng, Y., Hu, J. & Liu, Z. (2011). Identification and characterization of a novel thermostable gh-57 gene from metagenomic fosmid library of the Juan de Fuca Ridge hydrothermal vent. Appl Biochem Biotechnol 164, 1323-1338.
61. Watanabe, H., Nishimoto, T., Kubota, M., Chaen, H. & Fukuda, S. (2006). Cloning, sequencing, and expression of the genes encoding an isocyclomaltooligosaccharide glucanotransferase and an a-amylase from a Bacillus circulans strain. Biosci Biotechnol Biochem 70, 2690-2702.
62. Zona, R., Chang-Pi-Hin, F., O'Donohue, M. J. & Janeček, Š. (2004). Bioinformatics of the glycoside hydrolase family 57 and identification of catalytic residues in amylopullulanase from Thermococcus hydrothermalis. Eur J Biochem 271, 2863-2872.