Structural and biochemical analyses of glycoside hydrolase families 5 and 26 β-(1,4)-mannanases from Podospora anserina reveal differences upon manno-oligosaccharide catalysis

Journal of Biological Chemistry

Volumn 288, Issue 20, 2013, Pages 14624-14635

  Couturier, Marie ^a   Roussel, Alain ^a   Rosengren, Anna ^b   Leone, Philippe ^a   Stålbrand, Henrik ^b   Berrin, Jean Guy ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ANALYSIS; CARBOHYDRATE BINDING MODULES; COMPARATIVE ANALYSIS; ENZYMATIC DEGRADATION; GLYCOSIDE HYDROLASES; LIGNOCELLULOSIC BIOMASS; SUBSTRATE SPECIFICITY; TRANSGLYCOSYLATION;

BINDING ENERGY;

PLANT CELL CULTURE;

BETA MANNOSIDASE; FUNGAL ENZYME; GLYCOSIDASE; MANNOPENTAOSE; MANNOSE OLIGOSACCHARIDE; MANNOTETRAOSE; MONOSACCHARIDE; PROLINE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOHYDRATE METABOLISM; COMPARATIVE STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; GLYCOSYLATION; HYDROLYSIS; NONHUMAN; PODOSPORA ANSERINA; PRIORITY JOURNAL; PROTEIN FAMILY; STRUCTURE ACTIVITY RELATION;

CARBOHYDRATE; CAZYMES; ENZYME STRUCTURE; FUNGI; GLYCOSIDE HYDROLASES; MANNAN; PLANT CELL WALL; POLYSACCHARIDE;

CATALYSIS; CATALYTIC DOMAIN; CELL WALL; GLYCOSIDE HYDROLASES; GLYCOSYLATION; HYDROLYSIS; MUTAGENESIS; OLIGOSACCHARIDES; PODOSPORA; POLYSACCHARIDES; PROLINE; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 84877890782     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.459438     Document Type: Article

References (53)

1. Timell, T. E. (1967) Recent progress in the chemistry of wood hemicellulose. Wood Sci. Technol. 1, 45-70
2. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The carbohydrate-active EnZymes database (CAZy). An expert resource for glycogenomics. Nucleic Acids Res. 37, 233-238
3. Davies, G., and Henrissat, B. (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3, 853-859
4. Vocadlo, D. J., and Davies, G. J. (2008) Mechanistic insights into glycosidase chemistry. Curr. Opin. Chem. Biol. 12, 539-555
5. Gilbert, H. J., Stålbrand, H., and Brumer, H. (2008) How the walls come crumbling down. Recent structural biochemistry of plant polysaccharide degradation. Curr. Opin. Plant. Biol. 11, 338-348
6. Dilokpimol, A., Nakai, H., Gotfredsen, C. H., Baumann, M. J., Nakai, N., Abou Hachem, M., and Svensson, B. (2011) Recombinant production and characterization of two related GH5 endo-β-1,4-mannanases from Aspergillus nidulans FGSC A4 showing distinctly different transglycosylation capacity. Biochim. Biophys. Acta 1814, 1720-1729
7. Larsson, A. M., Anderson, L., Xu, B., Muñoz, I. G., Usón, I., Janson, J. C., Stålbrand, H., and Ståhlberg, J. (2006) Three-dimensional crystal structure and enzymic characterization of β-mannanase Man5A from blue mussel Mytilus edulis. J. Mol. Biol. 357, 1500-1510
8. Harjunpää, V., Helin, J., Koivula, A., Siika-aho, M., and Drakenberg, T. (1999) A comparative study of two retaining enzymes of Trichoderma reesei. Transglycosylation of oligosaccharides catalysed by the cellobiohydrolase I, Cel7A, and the β-mannanase, Man5A. FEBS Lett. 443, 149-153 (Pubitemid 29078621)
9. Zhang, Y., Ju, J., Peng, H., Gao, F., Zhou, C., Zeng, Y., Xue, Y., Li, Y., Henrissat, B., Gao, G. F., and Ma, Y. (2008) Biochemical and structural characterization of the intracellular mannanase AaManA of Alicyclobacillus acidocaldarius reveals a novel glycoside hydrolase family belonging to clan GH-A. J. Biol. Chem. 283, 31551-31558
10. Anderson, L., Hägglund, P., Stoll, D., Lo Leggio, L., Drakenberg, T., and Stålbrand, H. (2008) Kinetics and stereochemistry of the Cellulomonas fimi β-mannanase studied using 1H NMR. Biocatal. Biotransformation 26, 86-95
11. Stoll, D., Boraston, A., Stålbrand, H., McLean, B. W., Kilburn, D. G., and Warren, R. A. (2000) Mannanase Man26A from Cellulomonas fimi has a mannan binding module. FEMS Microbiol. Lett. 183, 265-269 (Pubitemid 30079659)
12. Hägglund, P., Eriksson, T., Collén, A., Nerinckx, W., Claeyssens, M., and Stålbrand, H. (2003)Acellulose binding module of the Trichoderma reesei β-mannanase Man5A increases the mannan-hydrolysis of complex substrates. J. Biotechnol. 101, 37-48
13. Fujimoto, Z., Kuno, A., Kaneko, S., Kobayashi, H., Kusakabe, I., and Mizuno, H. (2002) Crystal structures of the sugar complexes of Streptomyces olivaceoviridis E-86 xylanase. Sugar binding structure of the family 13 carbohydrate binding module. J. Mol. Biol. 316, 65-78 (Pubitemid 34729266)
14. Pell, G., Szabo, L., Charnock, S. J., Xie, H., Gloster, T. M., Davies, G. J., and Gilbert, H. J. (2004) Structural and biochemical analysis of Cellvibrio japonicus xylanase 10C. How variation in substrate binding cleft influences the catalytic profile of family GH-10 xylanases. J. Biol. Chem. 279, 11777-11788 (Pubitemid 38401683)
15. Sabini, E., Schubert, H., Murshudov, G., Wilson, K. S., Siika-Aho, M., and Penttilä, M. (2000) The three-dimensional structure of a Trichoderma reesei β-mannanase from glycoside hydrolase family 5. Acta Crystallogr. D. Biol. Crystallogr. 56, 3-13 (Pubitemid 30061536)
16. Bourgault, R., Oakley, A. J., Bewley, J. D., and Wilce, M. C. (2005) Threedimensional structure of (1,4)-β-D-mannan mannanohydrolase from tomato fruit. Protein Sci. 14, 1233-1241 (Pubitemid 40577803)
17. Le Nours, J., Anderson, L., Stoll, D., Stålbrand, H., and Lo Leggio, L. (2005) The structure and characterization of a modular endo-β-1,4-mannanase from Cellulomonas fimi. Biochemistry 44, 12700-12708 (Pubitemid 41377309)
18. Hogg, D., Woo, E. J., Bolam, D. N., McKie, V. A., Gilbert, H. J., and Pickersgill, R. W. (2001) Crystal structure of mannanase 26A from Pseudomonas cellulosa and analysis of residues involved in substrate binding. J. Biol. Chem. 276, 31186-31192
19. Fanutti, C., Ponyi, T., Black, G. W., Hazlewood, G. P., and Gilbert, H. J. (1995) The conserved noncatalytic 40-residue sequence in cellulases and hemicellulases from anaerobic fungi functions as a protein docking domain. J. Biol. Chem. 270, 29314-29322
20. Tailford, L. E., Ducros, V. M., Flint, J. E., Roberts, S. M., Morland, C., Zechel, D. L., Smith, N., Bjørnvad, M. E., Borchert, T. V., Wilson, K. S., Davies, G. J., and Gilbert, H. J. (2009) Understanding how diverse β-mannanases recognize heterogeneous substrates. Biochemistry 48, 7009-7018
21. Yan, X. X., An, X. M., Gui, L. L., and Liang, D. C. (2008) From structure to function. Insights into the catalytic substrate specificity and thermostability displayed by Bacillus subtilis mannanase BCman. J. Mol. Biol. 379, 535-544
22. Ducros, V. M., Zechel, D. L., Murshudov, G. N., Gilbert, H. J., Szabó, L., Stoll, D., Withers, S. G., and Davies, G. J. (2002) Substrate distortion by a β-mannanase. Snapshots of the Michaelis and covalent-intermediate complexes suggest a B(2,5) conformation for the transition state. Angew. Chem. Int. Ed. Engl. 41, 2824-2827
23. Cartmell, A., Topakas, E., Ducros, V. M., Suits, M. D., Davies, G. J., and Gilbert, H. J. (2008) The Cellvibrio japonicus mannanase CjMan26C displays a unique exo-mode of action that is conferred by subtle changes to the distal region of the active site. J. Biol. Chem. 283, 34403-34413
24. Setati, M. E., Ademark, P., van Zyl, W. H., Hahn-Hägerdal, B., and Stålbrand, H. (2001) Expression of the Aspergillus aculeatus endo-β-1,4-mannanase-encoding gene (man1) in Saccharomyces cerevisiae and characterization of the recombinant enzyme. Protein Expr. Purif. 21, 105-114 (Pubitemid 32620566)
25. Xu, B., Hägglund, P., Stålbrand, H., and Janson, J. C. (2002) Endo-β-1,4-Mannanases from blue mussel Mytilus edulis. Purification, characterization, and mode of action. J. Biotechnol. 92, 267-277 (Pubitemid 33022631)
26. Hogg, D., Pell, G., Dupree, P., Goubet, F., Martín-Orúe, S. M., Armand, S., and Gilbert, H. J. (2003) The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation. Biochem. J. 371, 1027-1043 (Pubitemid 36578903)
27. Espagne, E., Lespinet, O., Malagnac, F., Da Silva, C., Jaillon, O., Porcel, B. M., Couloux, A., Aury, J. M., Ségurens, B., Poulain, J., Anthouard, V., Grossetete, S., Khalili, H., Coppin, E., Déquard-Chablat, M., Picard, M., Contamine, V., Arnaise, S., Bourdais, A., Berteaux-Lecellier, V., Gautheret, D., de Vries, R. P., Battaglia, E., Coutinho, P. M., Danchin, E. G., Henrissat, B., Khoury, R. E., Sainsard-Chanet, A., Boivin, A., Pinan-Lucarré, B., Sellem, C. H., Debuchy, R., Wincker, P., Weissenbach, J., and Silar, P. (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol. 9, R77
28. Couturier, M., Haon, M., Coutinho, P. M., Henrissat, B., Lesage-Meessen, L., and Berrin, J.-G. (2011) Podospora anserina hemicellulases potentiate the Trichoderma reesei secretome for saccharification of lignocellulosic biomass. Appl. Environ. Microbiol. 77, 237-246
29. Matsui, I., Ishikawa, K., Matsui, E., Miyairi, S., Fukui, S., and Honda, K. (1991) Subsite structure of Saccharomycopsis α-amylase secreted from Saccharomyces cerevisiae. J. Biochem. 109, 566-569
30. Berrin, J.-G., Ajandouz, el H., Georis, J., Arnaut, F., and Juge, N. (2007) Substrate and product hydrolysis specificity in family 11 glycoside hydrolase. An analysis of Penicillium funiculosum and Penicillium griseofulvum xylanases. Appl. Microbiol. Biotechnol. 74, 1001-1010
31. Hekmat, O., Lo Leggio, L., Rosengren, A., Kamarauskaite, J., Kolenova, K., and Stålbrand, H. (2010) Rational engineering of mannosyl binding in the distal glycone subsites of Cellulomonas fimi endo-β-1,4-mannanase. Mannosyl binding promoted at subsite -2 and demoted at subsite -3. Biochemistry 49, 4884-4896
32. Rosengren, A., Hägglund, P., Anderson, L., Pavon-Orozco, P., Peterson-Wulff, R., Nerinckx, W., and Stålbrand, H. (2012) The role of subsite +2 of the Trichoderma reesei β-mannanase TrMan5A in hydrolysis and transglycosylation. Biocatal. Biotransformation 30, 338-352
33. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
34. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
35. Navaza, J. (2001) Implementation of molecular replacement in AMoRe. Acta Crystallogr. D. Biol. Crystallogr. 57, 1367-1372
36. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
37. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Sharff, A., Smart, O. S., Vonrhein, C., and Womack, T. O. (2011) BUSTER Version 2.11.2, Global Phasing Ltd., Cambridge, UK
38. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the web. A case study using the Phyre server. Nat. Protoc. 4, 363-371
39. Roussel, A., and Cambillau, C. (1991) Turbo-Frodo. in Silicon Graphics Geometry Partners Directory, p. 86, Mountain View Publications, CA
40. Stålbrand, H., Siika-aho, M., Tenkanen, M., and Viikari, L. (1993) Purification and characterization of two β-mannanases from Trichoderma reesei. J. Biotechnol. 29, 229-242
41. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559 (Pubitemid 27056509)
42. Jenkins, J., Lo Leggio, L., Harris, G., and Pickersgill, R. (1995) β-Glucosidase, β-galactosidase, family A cellulases, family F xylanases, and two barley glycanases form a superfamily of enzymes with 8-fold β/α architecture and with two conserved glutamates near the carboxyl-terminal ends of β-strands four and seven. FEBS Lett. 362, 281-285
43. Henrissat, B., Callebaut, I., Fabrega, S., Lehn, P., Mornon, J. P., and Davies, G. (1996) Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proc. Natl. Acad. Sci. U.S.A. 93, 5674
44. Hilge, M., Gloor, S., Winterhalter, K., Zimmermann, W., and Piontek, K. (1996) Crystallization and preliminary crystallographic analysis of two β-mannanase isoforms from Thermomonospora fusca KW3. Acta Crystallogr. D. Biol. Crystallogr. 52, 1224-1225
45. Bolam, D. N., Hughes, N., Virden, R., Lakey, J. H., Hazlewood, G. P., Henrissat, B., Braithwaite, K. L., and Gilbert, H. J. (1996) Mannanase A from Pseudomonas fluorescens ssp. cellulosa is a retaining glycosyl hydrolase in which E212 and E320 are the putative catalytic residues. Biochemistry 35, 16195-16204 (Pubitemid 27044081)
46. Kauppinen, M. S., Schulein, M., Schnorr, K., Andersen, L. N., and Mads E. (May 20, 2003) U. S. Patent 6,566,114
47. Ichinose, H., Yoshida, M., Kotake, T., Kuno, A., Igarashi, K., Tsumuraya, Y., Samejima, M., Hirabayashi, J., Kobayashi, H., and Kaneko, S. (2005) An exo-β-1,3-galactanase having a novel β-1,3-galactan-binding module from Phanerochaete chrysosporium. J. Biol. Chem. 280, 25820-25829 (Pubitemid 40962292)
48. Correia, M. A., Abbott, D. W., Gloster, T. M., Fernandes, V. O., Prates, J. A., Montanier, C., Dumon, C., Williamson, M. P., Tunnicliffe, R. B., Liu, Z., Flint, J. E., Davies, G. J., Henrissat, B., Coutinho, P. M., Fontes, C. M., and Gilbert, H. J. (2010) Signature active site architectures illuminate the molecular basis for ligand specificity in family 35 carbohydrate binding module. Biochemistry 49, 6193-6205
49. Holm, L., and Rosenström, P. (2010) Dali server. Conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
50. Montanier, C., van Bueren, A. L., Dumon, C., Flint, J. E., Correia, M. A., Prates, J. A., Firbank, S. J., Lewis, R. J., Grondin, G. G., Ghinet, M. G., Gloster, T. M., Herve, C., Knox, J. P., Talbot, B. G., Turkenburg, J. P., Kerovuo, J., Brzezinski, R., Fontes, C. M., Davies, G. J., Boraston, A. B., and Gilbert, H. J. (2009) Evidence that family 35 carbohydrate binding modules display conserved specificity but divergent function. Proc. Natl. Acad. Sci. U.S.A. 106, 3065-3070
51. Aspeborg, H., Coutinho, P. M., Wang, Y., Brumer, H., 3rd, and Henrissat, B. (2012) Evolution, substrate specificity, and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol. Biol. 12, 186
52. Bey, M., Zhou, S., Poidevin, L., Henrissat, B., Coutinho, P. M., Berrin, J.-G., and Sigoillot, J.-C. (2013) Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (family GH61) from Podospora anserina. Appl. Environ. Microbiol. 79, 488-496
53. Lafond, M., Navarro, D., Haon, M., Couturier, M., and Berrin, J.-G. (2012) Characterization of a broad-specificity β-glucanase acting on β-(1,3)-, β-(1,4)-, and β-(1,6)-glucans that defines a new glycoside hydrolase family. Appl. Environ. Microbiol. 78, 8540-8546