A novel GH13 subfamily of α-amylases with a pair of tryptophans in the helix α3 of the catalytic TIM-barrel, the LPDlx signature in the conserved sequence region V and a conserved aromatic motif at the C-terminus
Abstract
The α-amylase enzyme specificity has been classified in the Carbohydrate-Active enZyme (CAZy) database into the families GH13, GH57, GH119 and eventually also GH126. α-Amylase is a glycoside hydrolase (GH) that catalyses in an endo-fashion the hydrolysis of the α-1,4-glucosidic linkages in starch and related α-glucans employing the retaining reaction mechanism. The family GH13 is the main α-amylase family with more than 28,000 members and 30 different specificities. The entire family GH13 has already been divided into 40 subfamilies; the α-amylase enzyme specificity being found in the subfamilies GH13 1, 5, 6, 7, 15, 19, 24, 27, 28, 32, 36 and 37. The present in silico study delivers a proposal to create a novel GH13 subfamily with the specificity of α-amylase. The proposal is based on a detailed bioinformatics analysis consisting of sequence, structural and evolutionary comparison of experimentally characterized α-amylases from, e.g., Bacillus aquimaris, Anoxybacillus sp. SK3-4 and DT3-1 and Geobacillus thermoleovorans, and hypothetical proteins, accompanied by α-amylases from well-established GH13 subfamilies and by closely related amylolytic enzymes (mainly from the subfamily GH13 31). Three sequence-structural features can be ascribed to the members of the newly proposed GH13 subfamily: (i) the pair of adjacent tryptophan residues positioned between the CSR-V and CSR-II in the helix α3 of the catalytic TIM-barrel; (ii) the sequence LPDlx in their CSR-V; and (iii) a ~30-residue long C-terminal region with a motif of five conserved aromatic residues. From the evolutionary point of view, the novel GH13 α-amylase subfamily is most closely related to fungal and yeast α-amylases classified in the subfamily GH13_1.
References
Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J.1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.10.1016/S0022-2836(05)80360-2Search in Google Scholar
Ballschmiter M., Armbrecht M., Ivanova K., Antranikian G. & Liebl W. 2005. AmyA, an α-amylase with β-cyclodextrinforming activity, and AmyB from the thermoalkaliphilic organism Anaerobranca gottschalkii: two α-amylases adapted to their different cellular localizations. Appl. Environ. Microbiol. 71: 3709-3715.Search in Google Scholar
Benson D.A., Clark K., Karsch-Mizrachi I., Lipman D.J., Ostell J. & Sayers E.W. 2014. GenBank. Nucleic Acids Res 42: D32- D37.10.1093/nar/gkt1030Search in Google Scholar PubMed PubMed Central
Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N. & Bourne P.E. 2000. The Protein Data Bank. Nucleic Acids Res. 28: 235-242.10.1093/nar/28.1.235Search in Google Scholar PubMed PubMed Central
Blesak K. & Janecek S. 2012. Sequence fingerprints of enzyme specificities from the glycoside hydrolase family GH57. Extremophiles 16: 497-506.10.1007/s00792-012-0449-9Search in Google Scholar PubMed
Blesak K. & Janecek S. 2013. Two potentially novel amylolytic enzyme specificities in the prokaryotic glycoside hydrolase α- amylase family GH57. Microbiology 159: 2584-2593.10.1099/mic.0.071084-0Search in Google Scholar PubMed
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: D233-D238.10.1093/nar/gkn663Search in Google Scholar PubMed PubMed Central
Carvalho C.C., Phan N.N., Chen Y. & Reilly P.J. 2015. Carbohydrate-binding module tribes. Biopolymers 103: 203-214.10.1002/bip.22584Search in Google Scholar PubMed
Chai Y.Y., Rahman R.N., Illias R.M. & Goh K.M. 2012. Cloning and characterization of two new thermostable and alkalitolerant α-amylases from the Anoxybacillus species that produce high levels of maltose. J. Ind. Microbiol. Biotechnol. 39: 731-741.10.1007/s10295-011-1074-9Search in Google Scholar PubMed
Crooks G.E., Hon G., Chandonia J.M. & Brenner S.E. 2004. WebLogo: a sequence logo generator. Genome Res. 14: 1188-1190.10.1101/gr.849004Search in Google Scholar PubMed PubMed Central
Da Lage J.L., Binder M., Hua-Van A., Janecek S. & Casane D. 2013. Gene make-up: rapid and massive intron gains after horizontal transfer of a bacterial α-amylase gene to Basidiomycetes. BMC Evolutionary Biology 13: 40.10.1186/1471-2148-13-40Search in Google Scholar PubMed PubMed Central
Da Lage J.L., Danchin E.G. & Casane D. 2007. Where do animal α-amylases come from? An interkingdom trip. FEBS Lett. 581: 3927-3935.10.1016/j.febslet.2007.07.019Search in Google Scholar
Da Lage J.L., Feller G. & Janecek S. 2004. Horizontal gene transfer from Eukarya to bacteria and domain shuffling: the α- amylase model. Cell. Mol. Life Sci. 61: 97-109.10.1007/s00018-003-3334-ySearch in Google Scholar
D’Amico S., Gerday C. & Feller G. 2000. Structural similarities and evolutionary relationships in chloride-dependent α- amylases. Gene 253: 95-105.10.1016/S0378-1119(00)00229-8Search in Google Scholar
Felsenstein J. 1985. Confidence-limits on phylogenies - an approach using the bootstrap. Evolution 39: 783-791.10.1111/j.1558-5646.1985.tb00420.xSearch in Google Scholar PubMed
Ficko-Blean E., Stuart C.P. & Boraston A.B. 2011. Structural analysis of CPF 2247, a novel α-amylase from Clostridium perfringens. Proteins 79: 2771-2777.Search in Google Scholar
Finore I., Kasavi C., Poli A., Romano I., Toksoy Oner E., Kirdar B., Dipasquale L., Nicolaus B. & Lama L. 2011. Purification, biochemical characterization and gene sequencing of a thermostable raw starch digesting α-amylase from Geobacillus thermoleovorans subsp. stromboliensis subsp. nov. World J. Microbiol. Biotechnol. 27: 2425-2433.Search in Google Scholar
Fritzsche H.B., Schwede T. & Schulz G.E. 2003. Covalent and three-dimensional structure of the cyclodextrinase from Flavobacterium sp. no. 92. Eur. J. Biochem. 270: 2332-2341.10.1046/j.1432-1033.2003.03603.xSearch in Google Scholar PubMed
Henrissat B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280: 309-316.10.1042/bj2800309Search in Google Scholar PubMed PubMed Central
Hondoh H., Saburi W., Mori H., Okuyama M., Nakada T., Matsuura Y. & Kimura A. 2008. Substrate recognition mechanism of α-1,6-glucosidic linkage hydrolyzing enzyme, dextran glucosidase from Streptococcus mutans. J. Mol. Biol. 378: 913-922.Search in Google Scholar
Hostinova E., Janecek S. & Gasperik J. 2010. Gene sequence, bioinformatics and enzymatic characterization of α-amylase from Saccharomycopsis fibuligera KZ. Protein J. 29: 355-364.Search in Google Scholar
Janecek S. 1994. Sequence similarities and evolutionary relationships of microbial, plant and animal α-amylases. Eur. J. Biochem. 224: 519-524.Search in Google Scholar
Janecek S. 2002. How many conserved sequence regions are there in the α-amylase family? Biologia 57 (Suppl 11): 29-41.Search in Google Scholar
Janecek S. & Kuchtova A. 2012. In silico identification of catalytic residues and domain fold of the family GH119 sharing the catalytic machinery with the α-amylase family GH57. FEBS Lett. 586: 3360-3366.10.1016/j.febslet.2012.07.020Search in Google Scholar PubMed
Janecek S., 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: 429-440.10.1016/j.enzmictec.2011.07.002Search in Google Scholar PubMed
Janecek S., Svensson B. & MacGregor E.A. 2014. α-Amylase - an enzyme specificity found in various families of glycoside hydrolases. Cell. Mol. Life Sci. 71: 1149-1170.10.1007/s00018-013-1388-zSearch in Google Scholar PubMed
Kelley L.A. & Sternberg M.J.E. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4: 363-371.10.1038/nprot.2009.2Search in Google Scholar PubMed
Kelly R.M., Dijkhuizen L. & Leemhuis H. 2009. Starch and α- glucan acting enzymes, modulating their properties by directed evolution. J. Biotechnol. 140: 184-193.Search in Google Scholar
Kuriki T. & Imanaka T. 1999. The concept of the α-amylase family: structural similarity and common catalytic mechanism. J. Biosci. Bioeng. 87: 557-565.10.1016/S1389-1723(99)80114-5Search in Google Scholar
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. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.10.1093/bioinformatics/btm404Search in Google Scholar
Lei Y., Peng H., Wang Y., Liu Y., Han F., Xiao Y. & Gao Y.2012. Preferential and rapid degradation of raw rice starch by an α-amylase of glycoside hydrolase subfamily GH13 37. Appl. Microbiol. Biotechnol. 94: 1577-1584.10.1007/s00253-012-4114-0Search in Google Scholar
Letunic I. & Bork P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127-128.10.1093/bioinformatics/btl529Search in Google Scholar
Leveque E., Janecek S., Belarbi A. & Haye B. 2000. Thermophilic archaeal amylolytic enzymes. Enzyme Microb. Technol. 26: 2-13.10.1016/S0141-0229(99)00142-8Search in Google Scholar
Li C., Du M., Cheng B., Wang L., Liu X., Ma C., Yang C. & Xu P. 2014. Close relationship of a novel Flavobacteriaceae α-amylase with archaeal α-amylases and good potentials for industrial applications. Biotechnol. Biofuels 7: 18.10.1186/1754-6834-7-18Search in Google Scholar
Liu Y., Lei Y., Zhang X., Gao Y., Xiao Y. & Peng H. 2012. Identification and phylogenetic characterization of a new subfamily of α-amylase enzymes from marine microorganisms. Mar. Biotechnol. (NY) 14: 253-260.10.1007/s10126-011-9414-3Search in Google Scholar
Lombard V., Golaconda Ramulu H., Drula E., Coutinho P.M. & Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42: D490-D495.10.1093/nar/gkt1178Search in Google Scholar
Long C.M., Virolle M.J., Chang S.Y., Chang S. & Bibb M.J. 1987. α-Amylase gene of Streptomyces limosus: nucleotide sequence, expression motifs, and amino acid sequence homology to mammalian and invertebrate α-amylases. J. Bacteriol. 169: 5745-5754.Search in Google Scholar
MacGregor E.A., Janecek S. & Svensson B. 2001. Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim. Biophys. Acta 1546: 1-20.10.1016/S0167-4838(00)00302-2Search in Google Scholar
Majzlova K., Pukajova Z. & Janecek S. 2013. Tracing the evolution of the α-amylase subfamily GH13 36 covering the amylolytic enzymes intermediate between oligo-1,6-glucosidases and neopullulanases. Carbohydr. Res. 367: 48-57.Search in Google Scholar
Matsuura Y., Kusunoki M., HaradaW. & Kakudo M. 1984. Structure and possible catalytic residues of Taka-amylase A. J. Biochem. 95: 697-702.10.1093/oxfordjournals.jbchem.a134659Search in Google Scholar PubMed
Mehta D. & Satyanarayana T. 2014. Domain C of thermostable α- amylase of Geobacillus thermoleovorans mediates raw starch adsorption. Appl. Microbiol. Biotechnol. 98: 4503-4519. Mok S.C., Teh A.H., Saito J.A., Najimudin N. & Alam M. 2013. Crystal structure of a compact α-amylase from Geobacillus thermoleovorans. Enzyme Microb. Technol. 53: 46-54.Search in Google Scholar
Nakao M., Nakayama T., Kakudo A., Inohara M., Harada M., Omura F. & Shibano Y. 1994. Structure and expression of a gene coding for thermostable α-glucosidase with a broad substrate specificity from Bacillus sp. SAM1606. Eur J Biochem 220: 293-300.10.1111/j.1432-1033.1994.tb18625.xSearch in Google Scholar
Oslancova A. & Janecek S. 2002. Oligo-1,6-glucosidase and neopullulanase enzyme subfamilies from the α-amylase family defined by the fifth conserved sequence region. Cell. Mol. Life Sci. 59: 1945-1959.Search in Google Scholar
Palomo M., Pijning T., Booiman T., Dobruchowska J.M., van der Vlist J., Kralj S., Planas A., Loos K., Kamerling J.P., Dijkstra B.W., van der Maarel M.J., Dijkhuizen L. & Leemhuis H. 2011. Thermus thermophilus glycoside hydrolase family 57 branching enzyme:crystal structure, mechanism of action, and products formed. J. Biol. Chem. 286: 3520-3530.Search in Google Scholar
Park K.H., Jung J.H., Park S.G., Lee M.E., Holden J.F., Park C.S. & Woo E.J. 2014. Structural features underlying the selective cleavage of a novel exo-type maltose-forming amylase from Pyrococcus sp. ST04. Acta Crystallogr. D Biol. Crystallogr. 70: 1659-1668.10.1107/S1399004714006567Search in Google Scholar
Puspasari F., Nurachman Z., Noer A.S., Radjasa O.K., van der Maarel M.J.E.C. & Natalia D. 2011. Characteristics of raw starch degrading α-amylase from Bacillus aquimaris MKSC 6.2 associated with soft coral Sinularia sp. Starch - St¨arke 63: 461-467.10.1002/star.201000127Search in Google Scholar
Puspasari F., Radjasa O.K., Noer A.S., Nurachman Z., Syah Y.M., van der Maarel M., Dijkhuizen L., Janecek S. & Natalia D. 2013. 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. J. Appl. Microbiol. 114: 108-120.Search in Google Scholar
Ranjani V., Janecek S., Chai K.P., Shahir S., Noor R., Abdul Rahman Z.R., Chan K.G. & Goh K.M. 2014. Protein engineering of selected residues from conserved sequence regions of a novel Anoxybacillus α-amylase. Sci. Rep. 4: 5850.10.1038/srep05850Search in Google Scholar
Saitou N. & Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.Search in Google Scholar
Sharma A. & Satyanarayana T. 2013. Microbial acid-stable α- amylases: characteristics, genetic engineering and applications. Process Biochem. 48: 201-211.Search in Google Scholar
Shatsky M., Nussinov R. & Wolfson H.J. 2004. A method for simultaneous alignment of multiple protein structures. Proteins 56: 143-156.10.1002/prot.10628Search in Google Scholar
Sivakumar N., Li N., Tang J.W., Patel B.K. & Swaminathan K. 2006. Crystal structure of AmyA lacks acidic surface and provide insights into protein stability at poly-extreme condition. FEBS Lett. 580: 2646-2652.10.1016/j.febslet.2006.04.017Search in Google Scholar
Stam M.R., Danchin E.G., Rancurel C., Coutinho P.M. & Henrissat B. 2006. Dividing the large glycoside hydrolase family 13 into subfamilies:towards improved functional annotations of α-amylase-related proteins. Protein Eng. Des. Sel. 19: 555-562.10.1093/protein/gzl044Search in Google Scholar
Stanley D., Farnden K.J.F. & MacRae E.A. 2005. Plant α- amylases: functions and roles in carbohydrate metabolism. Biologia 60 (Suppl.16): 65-71.Search in Google Scholar
Svensson B. 1994. Protein engineering in the α-amylase family: catalytic mechanism, substrate specificity, and stability. Plant Mol. Biol. 25: 141-157.Search in Google Scholar
UniProt Consortium 2014. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res. 42: D191-D198.10.1093/nar/gkt1140Search in Google Scholar
van der Maarel M.J., van der Veen B., Uitdehaag J.C., Leemhuis H. & Dijkhuizen L. 2002. Properties and applications of starch-converting enzymes of the α-amylase family. J. Biotechnol. 94: 137-155.10.1016/S0168-1656(01)00407-2Search in Google Scholar
van Zyl W.H., Bloom M. & Viktor M.J. 2012. Engineering yeasts for raw starch conversion. Appl. Microbiol. Biotechnol. 95: 1377-1388. 10.1007/s00253-012-4248-0Search in Google Scholar PubMed
Watanabe H., Nishimoto T., Kubota M., Chaen H. & Fukuda S. 2006. Cloning, sequencing, and expression of the genes encoding an isocyclomaltooligosaccharide glucanotransferase and an α-amylase from a Bacillus circulans strain. Biosci. Biotechnol. Biochem. 70: 2690-2702.Search in Google Scholar
Watanabe K., Hata Y., Kizaki H., Katsube Y. & Suzuki Y. 1997. The refined crystal structure of Bacillus cereus oligo-1,6- glucosidase at 2.0 ˚A resolution: structural characterization of proline-substitution sites for protein thermostabilization. J. Mol. Biol. 269: 142-153. Search in Google Scholar
© 2016
Articles in the same Issue
- An overview of phytochrome: An important light switch and photo-sensory antenna for regulation of vital functioning of plants
- A novel GH13 subfamily of α-amylases with a pair of tryptophans in the helix α3 of the catalytic TIM-barrel, the LPDlx signature in the conserved sequence region V and a conserved aromatic motif at the C-terminus
- Biogenic synthesis of silver nanoparticles using cell-free extract of Bacillus safensis LAU 13: antimicrobial, free radical scavenging and larvicidal activities
- Understanding taxonomic position of local endemic Agropyron deweyi (Poaceae) using morphological characters and sequences of nuclear and chloroplast DNA regions
- Genetic status of the putative hybrid swarms of mountain dwarf pine and Scots pine in contact zones of their distribution in Slovakia
- Species delimitation and population structure in three Onosma (Boraginaceae) species
- Glycinebetaine priming improves salt tolerance of wheat
- The effect of nitrogen level on rice growth, carbon-nitrogen metabolism and gene expression
- High efficiency Agrobacterium-mediated transformation of Pinellia ternata using petiole explants from submerged cultures
- Cryopreservation of Serbian autochthonous Prunus spp. by droplet-vitrification
- Response of green hydra (Hydra viridissima) to variability and directional changes in food availability
- Data on some members of the family Tylenchidae (Nematoda: Tylenchina) from Iran
- New and firstly recorded oribatid mites from Turkey
- Reproductive parameters of four species of water mites (Acari: Hydrachnidia)
- A new species of the genus Aeolothrips (Thysanoptera: Aeolothripidae) from Iran
- Skull variability of mice and voles inhabiting the territory of a great cormorant colony
- High glucose-associated osmolality promotes adipocytogenic differentiation of primary rat osteoblasts in a protein kinase A and phosphatidylinositol 3-kinase/Akt-dependent manner
- Direct influence of rooibos-derived compound on rabbit ovarian functions and their response to gonadotropins
- Corrective notice to the European mudminnow (Umbra krameri Walbaum, 1792) record from the Black Sea
Articles in the same Issue
- An overview of phytochrome: An important light switch and photo-sensory antenna for regulation of vital functioning of plants
- A novel GH13 subfamily of α-amylases with a pair of tryptophans in the helix α3 of the catalytic TIM-barrel, the LPDlx signature in the conserved sequence region V and a conserved aromatic motif at the C-terminus
- Biogenic synthesis of silver nanoparticles using cell-free extract of Bacillus safensis LAU 13: antimicrobial, free radical scavenging and larvicidal activities
- Understanding taxonomic position of local endemic Agropyron deweyi (Poaceae) using morphological characters and sequences of nuclear and chloroplast DNA regions
- Genetic status of the putative hybrid swarms of mountain dwarf pine and Scots pine in contact zones of their distribution in Slovakia
- Species delimitation and population structure in three Onosma (Boraginaceae) species
- Glycinebetaine priming improves salt tolerance of wheat
- The effect of nitrogen level on rice growth, carbon-nitrogen metabolism and gene expression
- High efficiency Agrobacterium-mediated transformation of Pinellia ternata using petiole explants from submerged cultures
- Cryopreservation of Serbian autochthonous Prunus spp. by droplet-vitrification
- Response of green hydra (Hydra viridissima) to variability and directional changes in food availability
- Data on some members of the family Tylenchidae (Nematoda: Tylenchina) from Iran
- New and firstly recorded oribatid mites from Turkey
- Reproductive parameters of four species of water mites (Acari: Hydrachnidia)
- A new species of the genus Aeolothrips (Thysanoptera: Aeolothripidae) from Iran
- Skull variability of mice and voles inhabiting the territory of a great cormorant colony
- High glucose-associated osmolality promotes adipocytogenic differentiation of primary rat osteoblasts in a protein kinase A and phosphatidylinositol 3-kinase/Akt-dependent manner
- Direct influence of rooibos-derived compound on rabbit ovarian functions and their response to gonadotropins
- Corrective notice to the European mudminnow (Umbra krameri Walbaum, 1792) record from the Black Sea