Thermostabilization of extremophilic Dictyoglomus thermophilum GH11 xylanase by an N-terminal disulfide bridge and the effect of ionic liquid [emim]OAc on the enzymatic performance

Enzyme and Microbial Technology

Volumn 53, Issue 6-7, 2013, Pages 414-419

  Li, He ^a   Kankaanpää, Anna ^a   Xiong, Hairong ^b   Hummel, Michael ^a   Sixta, Herbert ^a   Ojamo, Heikki ^a   Turunen, Ossi ^a  

^a AALTO UNIVERSITY   (Finland)

^b SOUTH CENTRAL UNIVERSITY FOR NATIONALITIES   (China)

Author keywords

emim OAc; Dictyoglomus thermophilum; GH11 xylanase; Ionic liquid; N terminal disulphide bridge; Thermostability

Indexed keywords

[EMIM]OAC; DICTYOGLOMUS THERMOPHILUM; DISULPHIDE BRIDGE; THERMOSTABILITY; XYLANASES;

COVALENT BONDS; IONIC LIQUIDS;

ENZYMES;

DISULFIDE; IONIC LIQUID; SIGNAL PEPTIDE; XYLAN ENDO 1,3 BETA XYLOSIDASE;

ARTICLE; BIOMASS; CHEMICAL ANALYSIS; DICTYOGLOMUS THERMOPHILUM; ENZYME ACTIVITY; HIGH TEMPERATURE; HYPERTHERMOPHILIC BACTERIUM; KINETICS; NONHUMAN; PECTOBACTERIUM CAROTOVORUM; PH; THERMOPHILIC BACTERIUM; THERMOSTABILITY; WILD TYPE;

BACTERIA (MICROORGANISMS); DICTYOGLOMUS THERMOPHILUM;

DICTYOGLOMUS THERMOPHILUM; GH11 XYLANASE; IONIC LIQUID; N-TERMINAL DISULPHIDE BRIDGE; THERMOSTABILITY; [EMIM]OAC;

AMINO ACID SUBSTITUTION; BACTERIA; BACTERIAL PROTEINS; BETA-GLUCOSIDASE; CATALYTIC DOMAIN; DISULFIDES; ENDO-1,4-BETA XYLANASES; ENZYME STABILITY; HALF-LIFE; IMIDAZOLES; IONIC LIQUIDS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN ENGINEERING; RECOMBINANT PROTEINS; TEMPERATURE;

EID: 84886430208     PISSN: 01410229     EISSN: 18790909     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2013.09.004     Document Type: Article

References (52)

1. Feltus F., Vandenbrink J.P. Bioenergy grass feedstock: current options and prospects for trait improvement using emerging genetic, genomic, and systems biology toolkits. Biotechnol Biofuels 2012, 5:80.
2. Petersen P.D., Lau J., Ebert B., Yang F., Verhertbruggen Y., Kim J.S., et al. Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants. Biotechnol Biofuels 2012, 5:84.
3. Zhao X., Zhang L., Liu D. Biomass recalcitrance. Part I. The chemical compositions and physical structures affecting the enzymatic hydrolysis of lignocellulose. Biofuels Bioprod Bioref 2012, 6:465-482.
4. Hu J., Arantes V., Saddler J. The enhancement of enzymatic hydrolysis of lignocellulosic substrates by the addition of accessory enzymes such as xylanase: is it an additive or synergistic effect?. Biotechnol Biofuels 2011, 4:36.
5. Ying Y., Meng D., Chen X., Li F. An extremely thermophilic anaerobic bacterium Caldicellulosiruptor sp. F32 exhibits distinctive properties in growth and xylanases during xylan hydrolysis. Enzyme Microb Technol 2013, 53:194-199.
6. Collins T., Gerday C., Feller G. Xylanases, xylanase families and extremophilic xylanases. FEMS Microb Rev 2005, 29:3-23.
7. Beg Q.K., Kapoor M., Mahajan L., Hoondal G.S. Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 2001, 56:326-338.
8. Paës G., Berrin J-G., Beaugrand J. GH11 xylanases: structure/function/properties relationships and applications. Biotechnol Adv 2011, 30:564-592.
9. Hakulinen N., Turunen O., Jänis J., Leisola M., Rouvinen J. Three-dimensional structures of thermophilic β-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa: comparison of twelve xylanases in relation to their thermal stability. Eur J Biochem 2003, 270:1399-1412.
10. Törrönen A., Rouvinen J. Structural and functional properties of low molecular weight endo-1,4-beta-xylanases. J Biotechnol 1997, 57:137-149.
11. Purmonen M., Valjakka J., Valjakka K., Laitinen T., Rouvinen J. Molecular dynamics studies on the thermostability of family 11 xylanases. Protein Eng Des Sel 2007, 20:551-559.
12. Wakarchuk W.W., Sung W.L., Campbell R.L., Cunningham A., Watson D.C., Yaguchi M. Thermostabilization of the Bacillus circulans xylanase by the introduction of disulfide bonds. Protein Eng Des Sel 1994, 7:1379-1386.
13. Sung WL, Yaguchi M, Ishikawa K. Modification of xylanase to improve thermophilicity, alkalophilicity and thermostability. US Patent 1998/5759840.
14. Fenel F., Leisola M., Jänis J., Turunen O. A de novo designed N-terminal disulphide bridge stabilizes the Trichoderma reesei endo-1,4-beta-xylanase II. J Biotechnol 2004, 108:137-143.
15. Jänis J., Turunen O., Leisola M., Derrick P., Rouvinen J., Vainiotalo P. Characterization of mutant xylanases using fourier transform ion cyclotron resonance mass spectrometry: stabilizing contributions of disulfide bridges and N-terminal extensions. Biochemistry 2004, 43:9556-9566.
16. Jänis J., Rouvinen J., Vainiotalo P., Turunen O., Shnyrov V.L. Irreversible thermal denaturation of Trichoderma reesei endo-1,4-beta-xylanase II and its three disulfide mutants characterized by differential scanning calorimetry. Int J Biol Macromol 2008, 42:75-80.
17. Wang Y., Fu Z., Huang H., Yao B., Zhang H., Xiong H., et al. Improved thermal performance of Thermomyces lanuginosus GH11 xylanase by engineering of an N-terminal disulfide bridge. Bioresour Technol 2012, 112:275-279.
18. Turunen O., Etuaho K., Fenal F., Vehmaanpera J., Wu X., Rouvinen J., et al. A combination of weakly stabilizing mutations with a disulfide bridge in the α-helix region of Trichoderma reesei endo-1,4-β-xylanase II increases the thermal stability through synergism. J Biotechnol 2001, 88:37-46.
19. Fenel F., Zitting A-J., Kantelinen A. Increased alkali stability in Trichoderma reesei endo-1,4-β-xylanase II by site directed mutagenesis. J Biotechnol 2006, 121:102-107.
20. Turunen O., Vuorio M., Fenel F., Leisola M. Engineering of multiple arginines into the Ser/Thr surface of Trichoderma reesei endo-1,4-beta-xylanase II increases the thermotolerance and shifts the pH optimum towards alkaline pH. Protein Eng Des Sel 2002, 15:141-145.
21. Xiong H., Fenel F., Leisola M., Turunen O. Engineering the thermostability of Trichoderma reesei endo-1,4-β-xylanase II by combination of disulphide bridges. Extremophiles 2004, 8:393-400.
22. Li H., Murtomäki L., Leisola M., Turunen O. The effect of thermostabilizing mutations on pressure stability of Trichoderma reesei GH11 xylanase. Protein Eng Des Sel 2012, 25:821-826.
23. Leisola M., Turunen O. Protein engineering: opportunities and challenges. Appl Microbiol Biotechnol 2007, 75:1225-1232.
24. Bommarius A.S., Blum J.K., Abrahamson M.J. Status of protein engineering for biocatalysts: how to design an industrially useful biocatalyst. Curr Opin Chem Biol 2011, 15:194-200.
25. Zhao H., Jones C.L., Baker G.A., Xia S., Olubajo O., Person V.N. Regenerating cellulose from ionic liquids for an accelerated enzymatic hydrolysis. J Biotechnol 2009, 139:47-54.
26. Mäki-Arvela P., Anugwom I., Virtanen P., Mikkola J-P. Dissolution of lignocellulosic materials and its constituents using ionic liquids: a review. Ind Crops and Prod 2010, 32:175-201.
27. Wang Y., Radosevich M., Hayes D., Labbe N. Compatible ionic liquid cellulases system for hydrolysis of lignocellulosic biomass. Biotechnol Bioeng 2011, 108:1042-1048.
28. Ang T., Ngoh G., Chua A.S., Lee M. Elucidation of the effect of ionic liquid pretreatment on rice husk via structural analyses. Biotechnol Biofuels 2012, 5:67.
29. Cruz A.G., Scullin C., Mu C., Cheng G., Stavila V., Varanasi P., et al. Impact of high biomass loading on ionic liquid pretreatment. Biotechnol Biofuels 2013, 6:52.
30. Zhao H. Methods for stabilizing and activating enzymes in ionic liquids: a review. J Chem Technol Biotechnol 2010, 85:891-907.
31. Lozano P., Bernal B., Bernal J.M., Pucheault M., Vaultier M. Stabilizing immobilized cellulase by ionic liquids for saccharification of cellulose solutions in 1-butyl-3-methylimidazolium chloride. Green Chem 2011, 13:1406-1410.
32. Bose S., Barnes C.A., Petrich J.W. Enhanced stability and activity of cellulase in an ionic liquid and the effect of pretreatment on cellulose hydrolysis. Biotechnol Bioeng 2012, 109:434-443.
33. Pottkämper J., Barthen P., Ilmberger N., Schwaneberg U., Schenk A., Schulte M., et al. Applying metagenomics for the identification of bacterial cellulases that are stable in ionic liquids. Green Chem 2009, 11:957-965.
34. Zhang T., Datta S., Eichler J., Ivanova N., Axen S.D., Kerfeld C.A., et al. Identification of a haloalkaliphilic and thermostable cellulase with improved ionic liquid tolerance. Green Chem 2011, 13:2083-2090.
35. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modelling. Electrophoresis 1997, 18:2714-2723.
36. McCarthy A.A., Morris D.D., Bergquist P.L., Baker E.N. Structure of XynB, a highly thermostable beta-1,4-xylanase from Dictyoglomus thermophilum Rt46B.1, at 1.8 A resolution. Acta Crystallogr D: Biol Crystallogr 2000, 56:1367-1375.
37. Choi J.H., Lee S.Y. Secretory and extracellular production of recombinant proteins using Escherichia coli. Appl Microbiol Biotechnol 2004, 64:625-635.
38. Bailey M.J., Biely P., Poutanen K. Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol 1992, 23:257-270.
39. Turunen O., Jänis J., Fenel F., Leisola M. Engineering the thermotolerance and pH optimum of family 11 xylanases by site-directed mutagenesis. Methods Enzymol 2004, 388:156-167.
40. Morris D.D., Gibbs M.D., Chin C.W., Koh M.H., Wong K.K., Allison R.W., et al. Cloning of the xynB gene from Dictyoglomus thermophilum Rt46B.1 and action of the gene product on kraft pulp. Appl Environ Microbiol 1998, 64:1759-1765.
41. Zhang W., Lou K., Li G. Expression and characterization of the Dictyoglomus thermophilum Rt46B.1 xylanase gene (xynB) in Bacillus subtilis. Appl Biochem Biotechnol 2010, 160:1484-1495.
42. Dumon C., Varvak A., Wall M.A., Flint J.E., Lewis R.J., Lakey J.H., et al. Engineering hyperthermostability into a GH11 xylanase is mediated by subtle changes to protein structure. J Biol Chem 2008, 283:22557-22564.
43. Palackal N., Brennan Y., Callen W.N., Dupree P., Frey G., Goubet F., et al. An evolutionary route to xylanase process fitness. Protein Sci 2004, 13:494-503.
44. Miyazaki K., Takenouchi M., Kondo H., Noro N., Suzuki M., Tsuda S. Thermal stabilization of Bacillus subtilis family-11 xylanase by directed evolution. J Biol Chem 2006, 281:10236-10242.
45. Ruller R., Deliberto L., Ferreira T.L., Ward R.J. Thermostable variants of the recombinant xylanase A from Bacillus subtilis produced by directed evolution show reduced heat capacity changes. Proteins 2008, 70:1280-1293.
46. Vieille C., Zeikus G.J. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microb Mol Biol Rev 2001, 65:1-43.
47. Wahlström R., Rovio S., Suurnäkki A. Partial enzymatic hydrolysis of microcrystalline cellulose in ionic liquids by Trichoderma reesei endoglucanases. RSC Adv 2012, 2:4472-4480.
48. Turner M.B., Spear S.K., Huddleston J.G., Holbrey J.D., Rogers R.D. Ionic liquid salt-induced inactivation and unfolding of cellulase from Trichoderma reesei. Green Chem 2003, 5:443-447.
49. Xiong H., Nyyssölä A., Jänis J., Santa H., Pastinen O., von Weymarn N., et al. Characterization of the xylanase produced by submerged cultivation of Thermomyces lanuginosus DSM 10635. Enzyme Microb Technol 2004, 35:93-99.
50. Jaeger V., Pfaendtner J. Structure, dynamics and activity of xylanase solvated in binary mixtures of ionic liquid and water. ACS Chem Biol 2013, 117:2662-2670.
51. Thomas M.F., Li L.L., Handley-Pendleton J.M., van der Lelie D., Dunn J.J., Wishart J.F. Enzyme activity in dialkyl phosphate ionic liquids. Bioresour Technol 2011, 102:11200-11203.
52. Nordwald E.M., Kaar J.L. Stabilization of enzymes in ionic liquids via modification of enzyme charge. Biotechnol Bioeng 2013, 110:2352-2360.