Abstract
Starch binding domains (SBDs) are able to bind to and facilitate the degradation of raw starch and starchy substrates. In general, in the CAZy database they have been classified among the carbohydrate-binding module (CBM) families. The two families CBM25 and CBM26 together with families CBM20, 21, 34, 41, 45, 48, 53, 58, 68 and 69 belong to twelve SBD CAZy families. They represent a group of closely related modules exhibiting some sequence similarity, although each of the two families possesses its own features. Both CBM25 and CBM26 adopt a typical SBD fold of distorted β-barrel as recognized in the modules present in the maltohexaose-producing amylase from Bacillus halodurans. With regard to catalytic domains, most members are α-amylases and maltooligosaccharide-producing amylases from the α-amylase glycoside hydrolase (GH) family GH13, but also some β-amylases (GH14) and hypothetical proteins (e.g. from the family GH31) are known. The main goal of this review was to compare the available amino acid sequences of SBDs from both families CBM25 and CBM26 and to reveal, if possible, SBD(s) with the character “intermediary” between the CBM25 and CBM26. Emphasis was also given on a structural comparison of the identified intermediary SBD with the CBM25 and CBM26 representatives and a detailed evolutionary division of both CBM families that can be utilized for defining the future subfamilies.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- CAZy:
-
Carbohydrate-Active enzymes
- CBM:
-
carbohydrate-binding module
- GH:
-
glycoside hydrolase
- PDB:
-
Protein Data Bank
- SBD:
-
starch-binding domain
References
Abe A., Tonozuka T., Sakano Y. & Kamitori S. 2004. Complex structures of Thermoactinomyces vulgaris R-47 α-amylase 1 with malto-oligosaccharides demonstrate the role of domain N acting as a starch-binding domain. J. Mol. Biol. 335: 811–822.
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.
Ashikari T., Nakamura N., Tanaka Y., Kiuchi N., Shibano Y., Tanaka T., Amachi T. & Yoshizumi H. 1986. Rhizopus rawstarch-degrading glucoamylase: its cloning and expression in yeast. Agric. Biol. Chem. 50: 957–964.
Boraston A.B., Bolam D.N., Gilbert H.J. & Davies G.J. 2004. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382: 769–781.
Boraston A.B., Healey M., Klassen J., Ficko-Blean E., Lammerts van Bueren A. & Law V. 2006. A structural and functional analysis of α-glucan recognition by family 25 and 26 carbohydrate-binding modules reveals a conserved mode of starch recognition. J. Biol. Chem. 281: 587–598.
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.
Christiansen C., Abou Hachem M., Janecek S., Viksř-Nielsen A., Blennow A. & Svensson B. 2009. The carbohydrate-binding module family 20 — diversity, structure, and function. FEBS J. 276: 5006–5029.
Cockburn D., Wilkens C., Ruzanski C., Andersen S., Nielsen J.W., Smith A.M., Field R.A., Willemoës M., Abou Hachem M. & Svensson B. 2014. Analysis of surface binding sites (SBSs) in carbohydrate active enzymes with focus on glycoside hydrolase families 13 and 77 — a mini-review. Biologia 69: 705–712.
Deshpande N., Addess K.J., Bluhm W.F., Merino-Ott J.C., Townsend-Merino W., Zhang Q., Knezevich C., Xie L., Chen L., Feng Z., Green R.K., Flippen-Anderson J.L., Westbrook J., Berman H.M. & Bourne P.E. 2005. Nucleic Acids Res. 33: D233–D237.
Gentry M.S., Dixon J.E. & Worby C.A. 2009. Lafora disease: insights into neurodegeneration from plant metabolism. Trends Biochem. Sci. 34: 628–639.
Gentry M.S., Romá-Mateo C. & Sanz P. 2013. Laforin, a protein with many faces: glucan phosphatase, adapter protein, et alii. FEBS J. 280: 525–537.
Giraud E. & Cuny G. 1997. Molecular characterization of the α-amylase genes of Lactobacillus plantarum A6 and Lactobacillus amylovorus reveals an unusual 3’ end structure with direct tandem repeats and suggests a common evolutionary origin. Gene 198: 149–157.
Glaring M.A., Baumann M.J., Abou Hachem M., Nakai H., Nakai N., Santelia D., Sigurskjold B.W., Zeeman S.C., Blennow A. & Svensson B. 2011. Starch-binding domains in the CBM45 family — low-affinity domains from glucan, water dikinase and α-amylase involved in plastidial starch metabolism. FEBS J. 278: 1175–1185.
Guillen D., Sanchez S. & Rodriguez-Sanoja R. 2010. Carbohydrate-binding domains: multiplicity of biological roles. Appl. Microbiol. Biotechnol. 85: 1241–1249.
Guillen D., Santiago M., Linares L., Perez R., Morlon J., Ruiz B., Sanchez S. & Rodriguez-Sanoja R. 2007. α-Amylase starch binding domains: cooperative effects of binding to starch granules of multiple tandemly arranged domains. Appl. Environ. Microbiol. 73: 3833–3837.
Haas B.J., Kamoun S., Zody M.C., Jiang R.H., Handsaker R.E., Cano L.M., Grabherr M., … & Nusbaum C. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398.
Hudson E.R., Pan D.A., James J., Lucocq J.M., Hawley S.A., Green K.A., Baba O., Terashima T. & Hardie D.G. 2003. A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr. Biol. 13: 861–866.
Janecek S. 2002. A motif of a microbial starch-binding domain found in human genethonin. Bioinformatics 18: 1534–1537.
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.
Janecek S. & Sevcik J. 1999. The evolution of starch-binding domain. FEBS Lett. 456: 119–125.
Janecek S., Svensson B. & MacGregor E.A. 2003. Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starchbinding domain. Eur. J. Biochem. 270: 635–645.
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.
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.
Jiang S., Heller B., Tagliabracci V.S., Zhai L., Irimia J.M., DePaoli-Roach A.A., Wells C.D., Skurat A.V. & Roach P.J. 2010. Starch binding domain-containing protein 1/genethonin 1 is a novel participant in glycogen metabolism. J. Biol. Chem. 285: 34960–34971.
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.
Koropatkin N.M. & Smith T.J. 2010. SusG: a unique cellmembrane-associated α-amylase from a prominent human gut symbiont targets complex starch molecules. Structure 18: 200–215.
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.
Letunic I. & Bork P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127–128.
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.
Machovic M. & Janecek S. 2006a. The evolution of putative starch-binding domains. FEBS Lett. 580: 6349–6356.
Machovic M. & Janecek S. 2006b. Starch-binding domains in the post-genome era. Cell. Mol. Life Sci. 63: 2710–2724.
Machovic M., Svensson B., MacGregor E.A. & Janecek S. 2005. A new clan of CBM families based on bioinformatics of starchbinding domains from families CBM20 and CBM21. FEBS J. 272: 5497–5513.
Matsui Y., Okada S., Uchimura T., Kondo A. & Satoh E. 2007. Determination and analysis of the starch binding domain of Streptococcus bovis 148 raw-starch-hydrolyzing α-amylase. J. Appl. Glycosci. 54: 217–222.
Mikkelsen R., Suszkiewicz K. & Blennow A. 2006. A novel type carbohydrate-binding module identified in α-glucan, water dikinases is specific for regulated plastidial starch metabolism. Biochemistry 45: 4674–4682.
Minassian B.A., Ianzano L., Meloche M., Andermann E., Rouleau G.A., Delgado-Escueta A.V. & Scherer S.W. 2000. Mutation spectrum and predicted function of laforin in Lafora’s progressive myoclonus epilepsy. Neurology 55: 341–346.
Orzechowski S., Grabowska A., Sitnicka D., Siminska J., Felus M., Dudkiewicz M., Fudali S. & Sobczak M. 2013. Analysis of the expression, subcellular and tissue localisation of phosphoglucan, water dikinase (PWD/GWD3) in Solanum tuberosum L.: a bioinformatics approach for the comparative analysis of two α-glucan, water dikinases (GWDs) from Solanum tuberosum L. Acta Physiol. Plant. 35: 483–500.
Peng H., Zheng Y., Chen M., Wang Y., Xiao Y. & Gao Y. 2014. A starch-binding domain identified in α-amylase (AmyP) represents a new family of carbohydrate-binding modules that contribute to enzymatic hydrolysis of soluble starch. FEBS Lett. 588: 1161–1167.
Penninga D., van der Veen B.A., Knegtel R.M., van Hijum S.A., Rozeboom H.J., Kalk K.H., Dijkstra B.W. & Dijkhuizen L. 1996. The raw starch binding domain of cyclodextrin glycosyltransferase from Bacillus circulans strain 251. J. Biol. Chem. 271: 32777–32784.
Polekhina G., Gupta A., Michell B.J., van Denderen B., Murthy S., Feil S.C., Jennings I.G., Campbell D.J., Witters L.A., Parker M.W., Kemp B.E. & Stapleton D. 2003. AMPK β subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13: 867–871.
Polekhina G., Gupta A., van Denderen B.J., Feil S.C., Kemp B.E., Stapleton D. & Parker M.W. Structural basis for glycogen recognition by AMP-activated protein kinase. Structure 13: 1453–1462.
Rodriguez Sanoja R., Morlon-Guyot J., Jore J., Pintado J., Juge N. & Guyot J.P. 2000. Comparative characterization of complete and truncated forms of Lactobacillus amylovorus α-amylase and role of the C-terminal direct repeats in rawstarch binding. Appl. Environ. Microbiol. 66: 3350–3356.
Rodriguez-Sanoja R., Oviedo N., Escalante L., Ruiz B. & Sanchez S. 2009. A single residue mutation abolishes attachment of the CBM26 starch-binding domain from Lactobacillus amylovorus α-amylase. J. Ind. Microbiol. Biotechnol. 36: 341–346.
Rodriguez-Sanoja R., Oviedo N. & Sanchez S. 2005a. Microbial starch-binding domain. Curr. Opin. Microbiol. 8: 260–267.
Rodriguez-Sanoja R., Ruiz B., Guyot J.P. & Sanchez S. 2005b. Starch-binding domain affects catalysis in two Lactobacillus α-amylases. Appl. Environ. Microbiol. 71: 297–302.
Ryan S.M., Fitzgerald G.F. & van Sinderen D. 2006. Screening for and identification of starch-, amylopectin-, and pullulandegrading activities in bifidobacterial strains. Appl. Environ. Microbiol. 72: 5289–5296.
Saitou N. & Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.
Shatsky M., Nussinov R. & Wolfson H.J. 2004. A method for simultaneous alignment of multiple protein structures. Proteins 56: 143–156.
Siggens K.W. 1987. Molecular cloning and characterization of the β-amylase gene from Bacillus circulans. Mol. Microbiol. 1: 86–91.
Sorimachi K., Le Gal-Coëffet M.F., Williamson G., Archer D.B. & Williamson M.P. 1997. Solution structure of the granular starch binding domain of Aspergillus niger glucoamylase bound to β-cyclodextrin. Structure 5: 647–661.
Southall S.M., Simpson P.J., Gilbert H.J., Williamson G. & Williamson M.P. 1999. The starch-binding domain from glucoamylase disrupts the structure of starch. FEBS Lett. 447: 58–60.
Sumitani J., Tottori T., Kawaguchi T. & Arai M. 2000. New type of starch-binding domain: the direct repeat motif in the Cterminal region of Bacillus sp. no. 195 α-amylase contributes to starch binding and raw starch degrading. Biochem. J. 350: 477–484.
Svensson B., Jespersen H., Sierks M.R. & MacGregor E.A. 1989. Sequence homology between putative raw-starch binding domains from different starch-degrading enzymes. Biochem. J. 264: 309–311.
Tung J.Y., Chang M.D., Chou W.I., Liu Y.Y., Yeh Y.H., Chang F.Y., Lin S.C., Qiu Z.L. & Sun Y.J. 2008. Crystal structures of the starch-binding domain from Rhizopus oryzae glucoamylase reveal a polysaccharide-binding path. Biochem. J. 416: 27–36.
UniProt Consortium. 2013. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 41: D43–D47.
van Bueren A.L. & Boraston A.B. 2007. The structural basis of α-glucan recognition by a family 41 carbohydrate-binding module from Thermotoga maritima. J. Mol. Biol. 365: 555–560.
Vander Kooi C.W., Taylor A.O., Pace R.M., Meekins D.A., Guo H.F., Kim Y. & Gentry M.S. 2010. Structural basis for the glucan phosphatase activity of Starch Excess4. Proc. Natl. Acad. Sci. USA 107: 15379–15384.
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.
Wayllace N.Z., Valdez H.A., Ugalde R.A., Busi M.V. & Gomez-Casati D.F. 2010. The starch-binding capacity of the noncatalytic SBD2 region and the interaction between the N- and C-terminal domains are involved in the modulation of the activity of starch synthase III from Arabidopsis thaliana. FEBS J. 277: 428–440.
Xu J., Ren F., Huang C.H., Zheng Y., Zhen J., Sun H., Ko T.P., He M., Chen C.C., Chan H.C., Guo R.T., Song H. & Ma Y. 2014. Functional and structural studies of pullulanase from Anoxybacillus sp. LM18-11. Proteins (in press); doi: 10.1002/prot.24498.
Yamaguchi R., Arakawa T., Tokunaga H., Ishibashi M. & Tokunaga M. 2012a. Distinct characteristics of single starchbinding domain SBD1 derived from tandem domains SBD1-SBD2 of halophilic Kocuria varians α-amylase. Protein J. 31: 250–258.
Yamaguchi R., Inoue Y., Tokunaga H., Ishibashi M., Arakawa T., Sumitani J., Kawaguchi T. & Tokunaga M. 2012b. Halophilic characterization of starch-binding domain from Kocuria varians α-amylase. Int. J. Biol. Macromol. 50: 95–102.
Yamaguchi R., Tokunaga H., Ishibashi M., Arakawa T. & Tokunaga M. 2011. Salt-dependent thermo-reversible α-amylase: cloning and characterization of halophilic α-amylase from moderately halophilic bacterium, Kocuria varians. Appl. Microbiol. Biotechnol. 89: 673–684.
Author information
Authors and Affiliations
Corresponding author
Additional information
Electronic supplementary material. The online version of this article (DOI:10.2478/s11756-014-0415-3) contains supplementary material, which is available to authorized users.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Majzlová, K., Janeček, Š. Two structurally related starch-binding domain families CBM25 and CBM26. Biologia 69, 1087–1096 (2014). https://doi.org/10.2478/s11756-014-0415-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-014-0415-3