Skip to main content
Log in

Carbohydrate-binding domains: multiplicity of biological roles

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbott DW, Hrynuik S, Boraston AB (2007) Identification and characterization of a novel periplasmic polygalacturonic acid binding protein from Yersinia enterolitica. J Mol Biol 367:1023–1033

    Article  CAS  Google Scholar 

  • 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 335:811–822

    Article  CAS  Google Scholar 

  • 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 280:7720–7728

    Article  CAS  Google Scholar 

  • 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 390:77–84

    Article  CAS  Google Scholar 

  • 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 281:29321–29329

    Article  CAS  Google Scholar 

  • 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 331:775–781

    CAS  Google Scholar 

  • 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 319:1143–1156

    Article  CAS  Google Scholar 

  • Boraston AB, Kwan E, Chiu P, Warren RAJ, Kilburn DG (2003) Recognition and hydrolysis of noncrystalline cellulose. J Biol Chem 278:6120–6127

    Article  CAS  Google Scholar 

  • Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    Article  CAS  Google Scholar 

  • Boraston AB, Wang D, Burke RD (2006) Blood group antigen recognition by a Streptococcus pneumoniae virulence factor. J Biol Chem 281:35263–35271

    Article  CAS  Google Scholar 

  • Boraston AB, Ficko-Blean E, Healey M (2007) Carbohydrate recognition by a large sialidase toxin from Clostridium perfringens. Biochemistry 46:11352–11360

    Article  CAS  Google Scholar 

  • Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789

    Article  CAS  Google Scholar 

  • 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 37:233–238

    Article  Google Scholar 

  • 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 583:1159–1163

    Article  CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  Google Scholar 

  • 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 9:1096–1099

    Article  CAS  Google Scholar 

  • Dumas B, Bottin A, Gaulin E, Esquerré-Tugayé M-T (2008) Cellulose-binding domains: cellulose associated-defensive sensing partners? Trends Plant Sci 13:160–164

    Article  CAS  Google Scholar 

  • 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 190:8220–8222

    Article  CAS  Google Scholar 

  • Felix M, Diana I, Shaolin C, David BW (2008) Regulation and characterization of Thermobifida fusca carbohydrate-binding module proteins E7 and E8. Biotechnol Bioeng 100:1066–1077

    Article  Google Scholar 

  • 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 281:37748–37757

    Article  CAS  Google Scholar 

  • Ficko-Blean E, Boraston AB (2009) N-acetylglucosamine recognition by a family 32 carbohydrate-binding module from Clostridium perfringens NagH. J Mol Biol 390:208–220

    Article  CAS  Google Scholar 

  • 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 280:23718–23726

    Article  CAS  Google Scholar 

  • 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 33:13–18

    CAS  Google Scholar 

  • 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 18:1766–1777

    Article  CAS  Google Scholar 

  • 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 313:1149

    Article  CAS  Google Scholar 

  • 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 198:149–157

    Article  CAS  Google Scholar 

  • 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 60:3926–3930

    CAS  Google Scholar 

  • 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 283:12604–12613

    Article  CAS  Google Scholar 

  • Gut H, King SJ, Walsh MA (2008) Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase. FEBS Lett 582:3348–3352

    Article  CAS  Google Scholar 

  • Hashimoto H (2006) Recent structural studies of carbohydrate-binding modules. Cell Mol Life Sc 63:2954–2967

    Article  CAS  Google Scholar 

  • 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 69:6969–6978

    Article  CAS  Google Scholar 

  • 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 72:1176–1184

    Article  CAS  Google Scholar 

  • Jervis EJ, Haynes CA, Kilburn DG (1997) Surface diffusion of cellulases and their isolated binding domains on cellulose. J Biol Chem 272:24016–24023

    Article  CAS  Google Scholar 

  • Jörg K, Wolfgang L (2006) Comparative characterization of deletion derivatives of the modular xylanase XynA of Thermotoga maritima. Extremophiles 10:373–381

    Article  Google Scholar 

  • 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 57:239–245

    CAS  Google Scholar 

  • 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 169:1564–1570

    CAS  Google Scholar 

  • 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 105:16876–16881

    Article  CAS  Google Scholar 

  • 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 28:7241–7257

    Article  Google Scholar 

  • 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 16:587–597

    Article  Google Scholar 

  • 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 103:4765–4770

    Article  CAS  Google Scholar 

  • 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 277:50245–50254

    Article  CAS  Google Scholar 

  • 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 19:615–623

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 399:503–511

    Article  CAS  Google Scholar 

  • 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 106:3065–3070

    Article  CAS  Google Scholar 

  • Morlon-Guyot J, Mucciolo-Roux F, Rodríguez Sanoja R, Guyot JP (2001) Characterization of the Lactobacillus manihotivorans α-amylase gene. DNA Seq 12:27–37

    Article  CAS  Google Scholar 

  • 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 279:40819–40826

    Article  CAS  Google Scholar 

  • 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 281:8815–8828

    Article  CAS  Google Scholar 

  • Newstead SL, Watson JN, Bennet AJ, Taylor G (2005) Galactose recognition by the carbohydrate-binding module of a bacterial sialidase. Acta Cryst 61:1483–1491

    Google Scholar 

  • 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 40:6248–6256

    Article  CAS  Google Scholar 

  • 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 120:605–617

    Article  CAS  Google Scholar 

  • 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 9:2

    Article  Google Scholar 

  • 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 427:30

    Article  CAS  Google Scholar 

  • 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 283:22942–22951

    Article  CAS  Google Scholar 

  • 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 36:341–346

    Article  Google Scholar 

  • Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70:283–295

    Article  CAS  Google Scholar 

  • 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 275:41137–41142

    Article  CAS  Google Scholar 

  • 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 5:647–661

    Article  CAS  Google Scholar 

  • Southall SM, Simpson PJ, Gilbert HJ, Williamson G, Williamson MP (1999) The starch-binding domain from glucoamylase disrupts the structure of starch. FEBS Lett 447:58–60

    Article  CAS  Google Scholar 

  • Thobhani S, Ember B, Siriwardena A, Boons G-J (2003) Multivalency and the mode of action of bacterial sialidases. J Am Chem Soc 125:7154–7155

    Article  CAS  Google Scholar 

  • 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 280:28492–28497

    Article  CAS  Google Scholar 

  • 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 280:11313–11319

    Article  CAS  Google Scholar 

  • 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 47:3026–3032

    Article  CAS  Google Scholar 

  • 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 14:76–84

    Article  Google Scholar 

  • 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 275:2524–2535

    Article  CAS  Google Scholar 

  • 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 19:277–285

    CAS  Google Scholar 

  • Wang L, Zhang Y, Gao P (2008) A novel function for the cellulose binding module of cellobiohydrolase I. Sci China C Life Sci 51:620–629

    Article  CAS  Google Scholar 

  • 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 384:436–449

    Article  CAS  Google Scholar 

  • Yi-Heng Percival Z, Lee RL (2004) Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems. Biotechnol Bioeng 88:797–824

    Article  Google Scholar 

Download references

Acknowledgments

We are indebted to Elizabeth Langley for language correction and to Beatriz Ruiz and Silvia Moreno for critical reading of the manuscript. Daniel Guillén is currently supported by a doctoral scholarship from Consejo Nacional de Ciencia y Tecnología, Mexico.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Romina Rodríguez-Sanoja.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guillén, D., Sánchez, S. & Rodríguez-Sanoja, R. Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 85, 1241–1249 (2010). https://doi.org/10.1007/s00253-009-2331-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-009-2331-y

Keywords

Navigation