Applied Microbiology and Biotechnology

, Volume 85, Issue 5, pp 1241–1249 | Cite as

Carbohydrate-binding domains: multiplicity of biological roles

  • Daniel Guillén
  • Sergio Sánchez
  • Romina Rodríguez-Sanoja
Mini-Review

Abstract

Insoluble polysaccharides can be degraded by a set of hydrolytic enzymes formed by catalytic modules appended to one or more non-catalytic carbohydrate-binding modules (CBM). The most recognized function of these auxiliary domains is to bind polysaccharides, bringing the biocatalyst into close and prolonged vicinity with its substrate, allowing carbohydrate hydrolysis. Examples of insoluble polysaccharides recognized by these enzymes include cellulose, chitin, β-glucans, starch, glycogen, inulin, pullulan, and xylan. Based on their amino acid similarity, CBMs are grouped into 55 families that show notable variation in substrate specificity; as a result, their biological functions are miscellaneous. Carbohydrate or polysaccharide recognition by CBMs is an important event for processes related to metabolism, pathogen defense, polysaccharide biosynthesis, virulence, plant development, etc. Understanding of the CBMs properties and mechanisms in ligand binding is of vital significance for the development of new carbohydrate-recognition technologies and provide the basis for fine manipulation of the carbohydrate–CBM interactions.

Keywords

Carbohydrate-binding domains Carbohydrate-active proteins Glucoside hydrolases Carbohydrate targeting Expansins Lectins 

References

  1. Abbott DW, Hrynuik S, Boraston AB (2007) Identification and characterization of a novel periplasmic polygalacturonic acid binding protein from Yersinia enterolitica. J Mol Biol 367:1023–1033CrossRefGoogle Scholar
  2. Abe A, Tonozuka T, Sakano Y, Kamitori S (2004) Complex structures of Thermoactinomyces vulgaris R-47 alpha-amylase 1 with malto-oligosaccharides demonstrate the role of domain N acting as a starch-binding domain. J Mol Biol 335:811–822CrossRefGoogle Scholar
  3. Anderson KM, Ashida H, Maskos K, Dell A, Li S-C, Li Y-T (2005) A clostridial endo-beta-galactosidase that cleaves both blood group A and B glycotopes: the first member of a new glycoside hydrolase family, GH98. J Biol Chem 280:7720–7728CrossRefGoogle Scholar
  4. Barral P, Suárez C, Batanero E, Alfonso C, Alché JD, Rodríguez-García MI, Villalba M, Rivas G, Rodríguez R (2005) An olive pollen protein with allergenic activity, Ole e 10, defines a novel family of carbohydrate-binding modules and is potentially implicated in pollen germination. Biochem J 390:77–84CrossRefGoogle Scholar
  5. Blake AW, McCartney L, Flint JE, Bolam DN, Boraston AB, Gilbert HJ, Knox JP (2006) Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J Biol Chem 281:29321–29329CrossRefGoogle Scholar
  6. Bolam DN, Ciruela A, McQueen-Mason S, Simpson P, Williamson MP, Rixon JE, Boraston A, Hazlewood GP, Gilbert HJ (1998) Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity. Biochem J 331:775–781Google Scholar
  7. Boraston AB, Nurizzo D, Notenboom V, Ducros V, Rose DR, Kilburn DG, Davies GJ (2002) Differential oligosaccharide recognition by evolutionarily-related beta-1, 4 and beta-1, 3 glucan-binding modules. J Mol Biol 319:1143–1156CrossRefGoogle Scholar
  8. Boraston AB, Kwan E, Chiu P, Warren RAJ, Kilburn DG (2003) Recognition and hydrolysis of noncrystalline cellulose. J Biol Chem 278:6120–6127CrossRefGoogle Scholar
  9. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781CrossRefGoogle Scholar
  10. Boraston AB, Wang D, Burke RD (2006) Blood group antigen recognition by a Streptococcus pneumoniae virulence factor. J Biol Chem 281:35263–35271CrossRefGoogle Scholar
  11. Boraston AB, Ficko-Blean E, Healey M (2007) Carbohydrate recognition by a large sialidase toxin from Clostridium perfringens. Biochemistry 46:11352–11360CrossRefGoogle Scholar
  12. Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789CrossRefGoogle Scholar
  13. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:233–238CrossRefGoogle Scholar
  14. Christiansen C, Hachem MA, Glaring MA, Viksø-Nielsen A, Sigurskjold BW, Svensson B, Blennow A (2009) A CBM20 low-affinity starch-binding domain from glucan, water dikinase. FEBS Lett 583:1159–1163CrossRefGoogle Scholar
  15. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861CrossRefGoogle Scholar
  16. Din N, Gilkes NR, Tekant B Jr, RCM WRAJ, Kilburn DG (1991) Non-hydrolytic disruption of cellulose fibres by the binding domain of a bacterial cellulase. Bio/Technol 9:1096–1099CrossRefGoogle Scholar
  17. Dumas B, Bottin A, Gaulin E, Esquerré-Tugayé M-T (2008) Cellulose-binding domains: cellulose associated-defensive sensing partners? Trends Plant Sci 13:160–164CrossRefGoogle Scholar
  18. Ezer A, Matalon E, Jindou S, Borovok I, Atamna N, Yu Z, Morrison M, Bayer EA, Lamed R (2008) Cell surface enzyme attachment is mediated by family 37 carbohydrate-binding modules, unique to Ruminococcus albus. J Bacteriol 190:8220–8222CrossRefGoogle Scholar
  19. Felix M, Diana I, Shaolin C, David BW (2008) Regulation and characterization of Thermobifida fusca carbohydrate-binding module proteins E7 and E8. Biotechnol Bioeng 100:1066–1077CrossRefGoogle Scholar
  20. Ficko-Blean E, Boraston AB (2006) The interaction of a carbohydrate-binding module from a Clostridium perfringens N-acetyl-beta-hexosaminidase with its carbohydrate receptor. J Biol Chem 281:37748–37757CrossRefGoogle Scholar
  21. Ficko-Blean E, Boraston AB (2009) N-acetylglucosamine recognition by a family 32 carbohydrate-binding module from Clostridium perfringens NagH. J Mol Biol 390:208–220CrossRefGoogle Scholar
  22. Flint J, Bolam DN, Nurizzo D, Taylor EJ, Williamson MP, Walters C, Davies GJ, Gilbert HJ (2005) Probing the mechanism of ligand recognition in family 29 carbohydrate-binding modules. J Biol Chem 280:23718–23726CrossRefGoogle Scholar
  23. Gao P-J, Chen G-J, Wang T-H, Zhang Y-S, Liu J (2001) Non-hydrolytic disruption of crystalline structure of cellulose by cellulose binding domain and linker sequence of cellobiohydrolase I from Penicillium janthinellum. Acta Biochim Biophys Sin 33:13–18Google Scholar
  24. Gaulin E, Drame N, Lafitte C, Torto-Alalibo T, Martinez Y, Ameline-Torregrosa C, Khatib M, Mazarguil H, Villalba-Mateos F, Kamoun S, Mazars C, Dumas B, Bottin A, Esquerre-Tugaye M-T, Rickauer M (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18:1766–1777CrossRefGoogle Scholar
  25. Giardina T, Gunning AP, Juge N, Faulds CB, Furniss CSM, Svensson B, Morris VJ, Williamson G (2001) Both binding sites of the starch-binding domain of Aspergillus niger glucoamylase are essential for inducing a conformational change in amylose. J Mol Biol 313:1149CrossRefGoogle Scholar
  26. Giraud E, Cuny G (1997) Molecular characterization of the alpha-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 198:149–157CrossRefGoogle Scholar
  27. Goto M, Semimaru T, Furukawa K, Hayashida S (1994) Analysis of the raw starch-binding domain by mutation of a glucoamylase from Aspergillus awamori var. kawachi expressed in Saccharomyces cerevisiae. Appl Environ Microbiol 60:3926–3930Google Scholar
  28. Gregg KJ, Finn R, Abbott DW, Boraston AB (2008) Divergent modes of glycan recognition by a new family of carbohydrate-binding modules. J Biol Chem 283:12604–12613CrossRefGoogle Scholar
  29. Gut H, King SJ, Walsh MA (2008) Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase. FEBS Lett 582:3348–3352CrossRefGoogle Scholar
  30. Hashimoto H (2006) Recent structural studies of carbohydrate-binding modules. Cell Mol Life Sc 63:2954–2967CrossRefGoogle Scholar
  31. Ito Y, Tomita T, Roy N, Nakano A, Sugawara-Tomita N, Watanabe S, Okai N, Abe N, Kamio Y (2003) Cloning, expression, and cell surface localization of Paenibacillus sp. strain W-61 xylanase 5, a multidomain xylanase. Appl Environ Microbiol 69:6969–6978CrossRefGoogle Scholar
  32. Itoh Y, Watanabe J, Fukada H, Mizuno R, Kezuka Y, Nonaka T, Watanabe T (2006) Importance of Trp59 and Trp60 in chitin-binding, hydrolytic, and antifungal activities of Streptomyces griseus chitinase C. Appl Microbiol Biotechnol 72:1176–1184CrossRefGoogle Scholar
  33. Jervis EJ, Haynes CA, Kilburn DG (1997) Surface diffusion of cellulases and their isolated binding domains on cellulose. J Biol Chem 272:24016–24023CrossRefGoogle Scholar
  34. Jörg K, Wolfgang L (2006) Comparative characterization of deletion derivatives of the modular xylanase XynA of Thermotoga maritima. Extremophiles 10:373–381CrossRefGoogle Scholar
  35. Juge N, Gal-Coeffet ML, Furniss C, Gunning A, Kramhoft B, Morris VJ, Williamson G, Svensson B (2002) The starch binding domain of glucoamylase from Aspergillus niger: overview of its structure, function, and role in raw-starch hydrolysis. Biologia Bratisl 57:239–245Google Scholar
  36. Kawazu T, Nakanishi Y, Uozumi N, Sasaki T, Yamagata H, Tsukagoshi N, Udaka S (1987) Cloning and nucleotide sequence of the gene coding for enzymatically active fragments of the Bacillus polymyxa beta-amylase. J Bacteriol 169:1564–1570Google Scholar
  37. Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S, Filee P, Charlier P, Joris B, Tabuchi A, Nikolaidis N, Cosgrove DJ (2008) Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci U S A 105:16876–16881CrossRefGoogle Scholar
  38. Kraulis J, Clore G, Nilges MJ, TA PG, Knowles J, Gronenborn A (1987) Determination of the three-dimensional solution structure of the C-terminal domain of cellobiohydrolase I from Trichoderma reesei. A study using nuclear magnetic resonance and hybrid distance geometry-dynamical simulated annealing. Biochemistry 28:7241–7257CrossRefGoogle Scholar
  39. Liu Y-S, Zeng Y, Luo Y, Xu Q, Himmel ME, Smith SJ, Ding S-Y (2009) Does the cellulose-binding module move on the cellulose surface? Cellulose 16:587–597CrossRefGoogle Scholar
  40. McCartney L, Blake AW, Flint J, Bolam DN, Boraston AB, Gilbert HJ, Knox JP (2006) Differential recognition of plant cell walls by microbial xylan-specific carbohydrate-binding modules. Proc Natl Acad Sci U S A 103:4765–4770CrossRefGoogle Scholar
  41. McLean BW, Boraston AB, Brouwer D, Sanaie N, Fyfe CA, Warren RAJ, Kilburn DG, Haynes CA (2002) Carbohydrate-binding modules recognize fine substructures of cellulose. J Biol Chem 277:50245–50254CrossRefGoogle Scholar
  42. Michel G, Barbeyron T, Kloareg B, Czjzek M (2009) The family 6 carbohydrate-binding modules have coevolved with their appended catalytic modules toward similar substrate specificity. Glycobiology 19:615–623CrossRefGoogle Scholar
  43. 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 45:4674–4682CrossRefGoogle Scholar
  44. Miyanaga A, Koseki T, Miwa Y, Mese Y, Nakamura S, Kuno A, Hirabayashi J, Matsuzawa H, Wakagi T, Shoun H, Fushinobu S (2006) The family 42 carbohydrate-binding module of family 54 a-l-arabinofuranosidase specifically binds the arabinofuranose side chain of hemicellulose. Biochem J 399:503–511CrossRefGoogle Scholar
  45. Montanier C, van Bueren AL, Dumon C, Flint JE, Correia MA, Prates JA, Firbank SJ, Lewis RJ, Grondin GG, Ghinet MG, Gloster TM, Herve C, Knox JP, Talbot BG, Turkenburg JP, Kerovuo J, Brzezinski R, Fontes CMGA, Davies GJ, Boraston AB, Gilbert HJ (2009) Evidence that family 35 carbohydrate binding modules display conserved specificity but divergent function. Proc Natl Acad Sci U S A 106:3065–3070CrossRefGoogle Scholar
  46. Morlon-Guyot J, Mucciolo-Roux F, Rodríguez Sanoja R, Guyot JP (2001) Characterization of the Lactobacillus manihotivorans α-amylase gene. DNA Seq 12:27–37CrossRefGoogle Scholar
  47. Moustafa I, Connaris H, Taylor M, Zaitsev V, Wilson JC, Kiefel MJ, von Itzstein M, Taylor G (2004) Sialic acid recognition by Vibrio cholerae neuraminidase. J Biol Chem 279:40819–40826CrossRefGoogle Scholar
  48. Najmudin S, Guerreiro CIPD, Carvalho AL, Prates JAM, Correia MAS, Alves VD, Ferreira LMA, Romao MJ, Gilbert HJ, Bolam DN, Fontes CMGA (2006) Xyloglucan is recognized by carbohydrate-binding modules that interact with beta-glucan chains. J Biol Chem 281:8815–8828CrossRefGoogle Scholar
  49. Newstead SL, Watson JN, Bennet AJ, Taylor G (2005) Galactose recognition by the carbohydrate-binding module of a bacterial sialidase. Acta Cryst 61:1483–1491Google Scholar
  50. Notenboom V, Boraston AB, Kilburn DG, Rose DR (2001) Crystal structures of the family 9 carbohydrate-binding module from Thermotoga maritima xylanase 10A in native and ligand-bound forms. Biochemistry 40:6248–6256CrossRefGoogle Scholar
  51. Obembe O, Jacobsen E, Timmers J, Gilbert H, Blake A, Knox J, Visser R, Vincken J-P (2007) Promiscuous, non-catalytic, tandem carbohydrate-binding modules modulate the cell-wall structure and development of transgenic tobacco (Nicotiana tabacum) plants. J Plant Res 120:605–617CrossRefGoogle Scholar
  52. Pantoom S, Songsiriritthigul C, Suginta W (2008) The effects of the surface-exposed residues on the binding and hydrolytic activities of Vibrio carchariae chitinase A. BMC Biochem 9:2CrossRefGoogle Scholar
  53. Qin L, Kudla U, Roze EHA, Goverse A, Popeijus H, Nieuwland J, Overmars H, Jones JT, Schots A, Smant G, Bakker J, Helder J (2004) Plant degradation: a nematode expansin acting on plants. Nature 427:30CrossRefGoogle Scholar
  54. Raman J, Fritz TA, Gerken TA, Jamison O, Live D, Liu M, Tabak LA (2008) The catalytic and lectin domains of UDP-GalNAc:Polypeptide alpha-N-acetylgalactosaminyltransferase function in concert to direct glycosylation site selection. J Biol Chem 283:22942–22951CrossRefGoogle Scholar
  55. Rodríguez-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 36:341–346CrossRefGoogle Scholar
  56. Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70:283–295CrossRefGoogle Scholar
  57. Simpson PJ, Xie H, Bolam DN, Gilbert HJ, Williamson MP (2000) The structural basis for the ligand specificity of family 2 carbohydrate-binding modules. J Biol Chem 275:41137–41142CrossRefGoogle Scholar
  58. Sorimachi K, Gal-Coëffet M-FL, Williamson G, Archer DB, Williamson MP (1997) Solution structure of the granular starch binding domain of Aspergillus niger glucoamylase bound to β-cyclodextrin. Structure 5:647–661CrossRefGoogle Scholar
  59. Southall SM, Simpson PJ, Gilbert HJ, Williamson G, Williamson MP (1999) The starch-binding domain from glucoamylase disrupts the structure of starch. FEBS Lett 447:58–60CrossRefGoogle Scholar
  60. Thobhani S, Ember B, Siriwardena A, Boons G-J (2003) Multivalency and the mode of action of bacterial sialidases. J Am Chem Soc 125:7154–7155CrossRefGoogle Scholar
  61. Vaaje-Kolstad G, Horn SJ, van Aalten DMF, Synstad B, Eijsink VGH (2005a) The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 280:28492–28497CrossRefGoogle Scholar
  62. Vaaje-Kolstad G, Houston DR, Riemen AHK, Eijsink VGH, van Aalten DMF (2005b) Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J Biol Chem 280:11313–11319CrossRefGoogle Scholar
  63. Valdez HA, Busi MV, Wayllace NZ, Parisi G, Ugalde RA, Gomez-Casati DF (2008) Role of the N-terminal starch-binding domains in the kinetic properties of starch synthase III from Arabidopsis thaliana. Biochemistry 47:3026–3032CrossRefGoogle Scholar
  64. van Bueren AL, Higgins M, Wang D, Burke RD, Boraston AB (2007) Identification and structural basis of binding to host lung glycogen by streptococcal virulence factors. Nat Struct Mol Biol 14:76–84CrossRefGoogle Scholar
  65. Viegas A, Brás NF, Cerqueira NMFSA, Fernandes PA, Prates JAM, Fontes CMGA, Bruix M, Romão MJ, Carvalho AL, Ramos MJ, Macedo AL, Cabrita EJ (2008) Molecular determinants of ligand specificity in family 11 carbohydrate binding modules, an NMR, X-ray crystallography and computational chemistry approach. FEBS J 275:2524–2535CrossRefGoogle Scholar
  66. Waeonukul R, Pason P, Kyu KL, Sakka K, Kosugi A, Mori Y, Ratanakhanokchai K (2009) Cloning, sequencing, and expression of the gene encoding a multidomain endo-beta-1, 4-xylanase from Paenibacillus curdlanolyticus B-6, and characterization of the recombinant enzyme. J Microbiol Biotechnol 19:277–285Google Scholar
  67. Wang L, Zhang Y, Gao P (2008) A novel function for the cellulose binding module of cellobiohydrolase I. Sci China C Life Sci 51:620–629CrossRefGoogle Scholar
  68. Xu G, Potter JA, Russell RJM, Oggioni MR, Andrew PW, Taylor GL (2008) Crystal structure of the NanB sialidase from Streptococcus pneumoniae. J Mol Biol 384:436–449CrossRefGoogle Scholar
  69. Yi-Heng Percival Z, Lee RL (2004) Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems. Biotechnol Bioeng 88:797–824CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Daniel Guillén
    • 1
  • Sergio Sánchez
    • 1
  • Romina Rodríguez-Sanoja
    • 1
  1. 1.Departamento de Biología Molecular y Biotecnología del Instituto de Investigaciones BiomédicasUniversidad Nacional Autónoma de MéxicoMexicoMexico

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