Expression and characterization of a bifidobacterium adolescentis beta-mannanase carrying mannan-binding and cell association motifs

Applied and Environmental Microbiology

Volumn 79, Issue 1, 2013, Pages 133-140

  Kulcinskaja, Evelina ^a   Rosengren, Anna ^a   Ibrahim, Romany ^a   Kolenová, Katarína ^a   Stålbrand, Henrik ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA-MANNANASE; BIFIDOBACTERIUM ADOLESCENTIS; CARBOHYDRATE-BINDING MODULES; CATALYTIC MODULES; DISSOCIATION CONSTANT; DOMINANT PRODUCT; GALACTOMANNANS; GENE PRODUCTS; GLYCOSIDE HYDROLASES; GUAR GUMS; HIGH-PERFORMANCE ANION-EXCHANGE CHROMATOGRAPHY; HUMAN GUTS; KONJAC GLUCOMANNAN; MANNANASE; MANNOBIOSE; PUTATIVE SIGNAL PEPTIDE; SIGNAL PEPTIDE; SORTASE; TRANSMEMBRANE HELICES;

CARBOHYDRATES; CHROMATOGRAPHY; CLONING; DISSOCIATION; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROLYSIS; OLIGOSACCHARIDES;

GENE ENCODING;

BETA MANNOSIDASE; GALACTOMANNAN; MANNAN; MANNOSE; RECOMBINANT PROTEIN;

BACTERIUM; CHEMICAL BINDING; CYTOLOGY; ENZYME; ENZYME ACTIVITY; GENE EXPRESSION; HYDROLYSIS; IMMUNOASSAY; PEPTIDE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BACTERIUM ADHERENCE; BIFIDOBACTERIUM; BINDING SITE; CAT; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; HYDROLYSIS; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN MOTIF; SEQUENCE ALIGNMENT;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; BETA-MANNOSIDASE; BIFIDOBACTERIUM; BINDING SITES; CATS; CLONING, MOLECULAR; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; HYDROLYSIS; KINETICS; MANNANS; MANNOSE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM ADOLESCENTIS; CERATONIA SILIQUA; CYAMOPSIS TETRAGONOLOBA; ESCHERICHIA COLI;

EID: 84871881296     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02118-12     Document Type: Article

References (61)

1. Lundqvist J, Teleman A, Junel L, Zacchi G, Dahlman O, Tjerneld F, Stålbrand H. 2002. Isolation and characterization of galactoglucomannan from spruce (Picea abies). Carbohydr. Polym. 48:29-39.
2. Scheller HV, Ulvskov P. 2010. Hemicelluloses. Annu. Rev. Plant Biol. 61:263-289.
3. Cerqueira MA, Bourbon AI, Pinheiro AC, Martins JT, Souza BWS, Teixeira JA, Vicente AA. 2011. Galactomannans use in the development of edible films/coatings for food applications. Trends Food Sci. Technol. 22:662-671.
4. Dave V, McCarthy SP. 1997. Review of konjac glucomannan. J. Environ. Polym. Degrad. 5:237-241.
5. Gilbert HJ, Stålbrand H, Brumer H. 2008. How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation. Curr. Opin. Plant Biol. 11:338-348.
6. Henrissat B, Davies G. 1997. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7:637-644.
7. 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:D233-D238.
8. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 2004. Carbohydratebinding modules: fine-tuning polysaccharide recognition. Biochem. J. 382:769-781.
9. Hilge M, Gloor SM, Rypniewski W, Sauer O, Heightman TD, Zimmermann W, Winterhalter K, Piontek K. 1998. High-resolution native and complex structures of thermostable beta-mannanase from Thermomonospora fusca-substrate specificity in glycosyl hydrolase family 5. Structure 6:1433-1444.
10. Hägglund P, Eriksson T, Collén A, Nerinckx W, Claeyssens M, Stålbrand H. 2003. A cellulose-binding module of the Trichoderma reesei β-mannanase Man5A increases the mannan-hydrolysis of complex substrates. J. Biotechnol. 101:37-48.
11. Rosengren A, Hägglund P, Anderson L, Pavon-Orozco P, Peterson Wulff R, Nerinckx W, Stålbrand H. 2012. The role of subsite +2 of the Trichoderma reesei β-mannanase TrMan5A in hydrolysis and transglycosylation. Biocatal. Biotransformation 30:338-352.
12. Sabini E, Schubert H, Murshudov G, Wilson KS, Siika-Aho M, Penttilä M. 2000. The three-dimensional structure of a Trichoderma reesei betamannanase from glycoside hydrolase family 5. Acta Crystallogr. D Biol. Crystallogr. 56:3-13.
13. Hekmat O, Lo Leggio L, Rosengren A, Kamarauskaite J, Kolenova K, Stålbrand H. 2010. Rational engineering of mannosyl binding in the distal glycone subsites of Cellulomonas fimi endo-beta-1,4-mannanase: mannosyl binding promoted at subsite-2 and demoted at subsite-3. Biochemistry 49:4884-4896.
14. Le Nours J, Anderson L, Stoll D, Stålbrand H, Lo Leggio L. 2005. The structure and characterization of a modular endo-beta-1,4-mannanase from Cellulomonas fimi. Biochemistry 44:12700-12708.
15. Stoll D, Boraston A, Stålbrand H, McLean BW, Kilburn DG, Warren RAJ. 2000. Mannanase Man26A from Cellulomonas fimi has a mannanbinding module. FEMS Microbiol. Lett. 183:265-269.
16. Stoll D, Stålbrand H, Warren RAJ. 1999. Mannan-degrading enzymes from Cellulomonas fimi. Appl. Environ. Microbiol. 65:2598-2605.
17. Cartmell A, Topakas E, Ducros VMA, Suits MDL, Davies GJ, Gilbert HJ. 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.
18. Hogg D, Woo EJ, Bolam DN, McKie VA, Gilbert HJ, Pickersgill RW. 2001. Crystal structure of mannanase 26A from Pseudomonas cellulosa and analysis of residues involved in substrate binding. J. Biol. Chem. 276: 31186-31192.
19. Tailford LE, Ducros VMA, Flint JE, Roberts SM, Morland C, Zechel DL, Smith N, Bjornvad ME, Borchert TV, Wilson KS, Davies GJ, Gilbert HJ. 2009. Understanding how diverse beta-mannanases recognize heterogeneous substrates. Biochemistry 48:7009-7018.
20. Yan X-X, An XM, Gui LL, Liang DC. 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.
21. Zhang YL, Ju JS, Peng H, Gao F, Zhou C, Zeng Y, Xue YF, Li Y, Henrissat B, Gao GF, Ma YH. 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.
22. Bourgault R, Oakley AJ, Bewley JD, Wilce MCJ. 2005. Threedimensional structure of (1,4)-beta-D-mannan mannanohydrolase from tomato fruit. Protein Sci. 14:1233-1241.
23. Larsson AM, Anderson L, Xu B, Muñoz IG, Uson I, Janson JC, Stålbrand H, Ståhlberg J. 2006. Three-dimensional crystal structure and enzymic characterization of beta-mannanase Man5A from blue mussel Mytilus edulis. J. Mol. Biol. 357:1500-1510.
24. Nyman M, Asp NG, Cummings J, Wiggins H. 1986. Fermentation of dietary fibre in the intestinal tract-comparison between man and rat. Br. J. Nutr. 55:487-496.
25. Tomlin J, Read NW, Edwards CA, Duerden BI. 1986. The degradation of guar gum by a fecal incubation system. Br. J. Nutr. 55:481-486.
26. Albrecht S, van Muiswinkel GC, Xu J, Schols HA, Voragen AG, Gruppen H. 2011. Enzymatic production and characterization of konjac glucomannan oligosaccharides. J. Agric. Food Chem. 59:12658-12666.
27. Asano I, Hamaguchi K, Fujii S, Iino H. 2003. In vitro digestibility and fermentation of mannooligosaccharides from coffee mannan. Food Sci. Technol. Res. 9:62-66.
28. Gibson GR. 2004. Fibre and effects on probiotics (the prebiotic concept). Clin. Nutr. 1:25-31.
29. Sears CL. 2005. A dynamic partnership: celebrating our gut flora. Anaerobe 11:247-251.
30. Picard C, Fioramonti J, Francois A, Robinson T, Neant F, Matuchansky C. 2005. Review article: bifidobacteria as probiotic agents-physiological effects and clinical benefits. Aliment. Pharmacol. Ther. 22:495-512.
31. Wang C-H, Lai P, Chen M-E, Chen H-L. 2008. Antioxidative capacity produced by Bifidobacterium-and Lactobacillus acidophilus-mediated fermentations of konjac glucomannan and glucomannan oligosaccharides. J. Sci. Food Agric. 88:1294-1300.
32. Gherardini FC, Salyers AA. 1987. Purification and characterization of a cell-associated, soluble mannanase from Bacteroides ovatus. J. Bacteriol. 169:2038-2043.
33. Macfarlane GT, Hay S, Macfarlane S, Gibson GR. 1990. Effect of different carbohydrates on growth, polysaccharidase and glycosidase production by Bacteriodes ovatus, in batch and continuous culture. J. Appl. Bacteriol. 68:179-187.
34. Tailford LE, Money VA, Smith NL, Dumon C, Davies GJ, Gilbert HJ. 2007. Mannose foraging by Bacteroides thetaiotaomicron-structure and specificity of the beta-mannosidase, BtMan2A. J. Biol. Chem. 282:11291-11299.
35. Pokusaeva K, Fitzgerald GF, van Sinderen D. 2011. Carbohydrate metabolism in bifidobacteria. Genes Nutr. 6:285-306.
36. van den Broek LAM, Hinz SWA, Beldman G, Vincken JP, Voragen AGJ. 2008. Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol. Nutr. Food Res. 52:146-163.
37. van den Broek LAM, Voragen AGJ. 2008. Bifidobacterium glycoside hydrolases and (potential) prebiotics. Innov. Food Sci. Emerg. Technol. 9:401-407.
38. Stålbrand H, Siika-aho, Tenkanen MM, Viikari L. 1993. Purification and characterization of 2 beta-mannanases from Trichoderma reesei. J. Biotechnol. 29:229-242.
39. Lawrence AM, Besir HU. 2009. Staining of proteins in gels with Coomassie G-250 without organic solvent and acetic acid. J. Vis. Exp. doi:10.3791/ 1350.
40. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server, p 571-607. In Walker JM (ed), The proteomics protocols handbook. Humana Press, Totowa, NJ.
41. Bounias M. 1980. N-(1-Naphthyl)ethylenediamine dihydrochloride as a new reagent for nanomole quantification of sugars on thin-layer plates by a mathematical calibration process. Anal. Biochem. 106:291-295.
42. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
43. Nordahl Petersen T, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786.
44. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23:2947-2948.
45. Hatada Y, Takeda N, Hirasawa K, Ohta Y, Usami R, Yoshida Y, Grant WD, Ito S, Horikoshi K. 2005. Sequence of the gene for a high-alkaline mannanase from an alkaliphilic Bacillus sp. strain JAMB-750, its expression in Bacillus subtilis and characterization of the recombinant enzyme. Extremophiles 9:497-500.
46. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371.
47. Antov M, Anderson L, Andersson A, Tjerneld F, Stålbrand H. 2006. Affinity partitioning of a Cellulomonas fimi beta-mannanase with a mannan-binding module in galactomannan/starch aqueous two-phase system. J. Chromatogr. A 1123:53-59.
48. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
49. Cabanes D, Dehoux P, Dussurget O, Frangeul L, Cossart P. 2002. Surface proteins and the pathogenic potential of Listeria monocytogenes. Trends Microbiol. 10:238-245.
50. Ton-That H, Marraffini LA, Schneewind O. 2004. Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim. Biophys. Acta 1694: 269-278.
51. Kruger RG, Otvos B, Frankel BA, Bentley M, Dostal P, McCafferty DG. 2004. Analysis of the substrate specificity of the Staphylococcus aureus sortase transpeptidase SrtA. Biochemistry 43:1541-1551.
52. Anderson L, Hägglund P, Stoll D, Lo Leggio L, Drakenberg T, Stålbrand H. 2008. Kinetics and stereochemistry of the Cellulomonas fimi betamannanase studied using H-1-NMR. Biocatal. Biotransformation 26: 86-95.
53. Degnan BA, Macfarlane GT. 1991. Comparison of carbohydrate substrate preferences in 8 species of bifidobacteria. FEMS Microbiol. Lett. 84:151-156.
54. Al-Ghazzewi FH, Khanna S, Tester RF, Piggott J. 2007. The potential use of hydrolysed konjac glucomannan as a prebiotic. J. Sci. Food Agric. 87: 1758-1766.
55. Schneewind O, Fowler A, Faull KF. 1995. Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science 268:103-106.
56. Halstead JR, Vercoe PE, Gilbert HJ, Davidson K, Hazlewood GP. 1999. A family 26 mannanase produced by Clostridium thermocellum as a component of the cellulosome contains a domain which is conserved in mannanases from anaerobic fungi. Microbiology 145:3101-3108.
57. Hogg D, Pell G, Dupree P, Goubet F, Martín-Orúe SM, Armand S, Gilbert HJ. 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.
58. Cuyvers S, Dornez E, Delcour JA, Courtin CM. 2012. Occurrence and functional significance of secondary carbohydrate binding sites in glycoside hydrolases. Crit. Rev. Biotechnol. 32:93-107.
59. Nielsen MM, Bozonnet S, Seo ES, Mótyán JA, Andersen JM, Dilokpimol A, Abou Hachem M, Gyémánt G, Naested H, Kandra L, Sigurskjold BW, Svensson B. 2009. Two secondary carbohydrate binding sites on the surface of barley alpha-amylase 1 have distinct functions and display synergy in hydrolysis of starch granules. Biochemistry 48:7686-7697.
60. Hinz SW, Pastink MI, van den Broek LA, Vincken JP, Voragen AG. 2005. Bifidobacterium longum endogalactanase liberates galactotriose from type I galactans. Appl. Environ. Microbiol. 71:5501-5510.
61. Hinz SWA, Doeswijk-Voragen CHL, Schipperus R, van den Broek LAM, Vincken JP, Voragen AGJ. 2006. Increasing the transglycosylation activity of alpha-galactosidase from Bifidobacterium adolescentis DSM 20083 by site-directed mutagenesis. Biotechnol. Bioeng. 93:122-131.