Insertion of endocellulase catalytic domains into thermostable consensus ankyrin scaffolds: Effects on stability and cellulolytic activity

Applied and Environmental Microbiology

Volumn 79, Issue 21, 2013, Pages 6684-6696

  Cunha, Eva S ^a,b   Hatem, Christine L ^b   Barrick, Doug ^b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMORPHOUS CELLULOSE; BIOFUELS PRODUCTION; CARBOXY-METHYL CELLULOSE; CLOSTRIDIUM THERMOCELLUM; ENZYMATIC ACTIVITIES; INSOLUBLE SUBSTRATES; MODULAR ARCHITECTURES; THERMOTOGA MARITIMA;

CELLULOSE; ENZYMES; SUBSTRATES;

SCAFFOLDS (BIOLOGY);

BIODEGRADATION; CATALYSIS; CELLULOSE; ENZYME ACTIVITY; HIGH TEMPERATURE; SUGAR; TEMPERATURE EFFECT;

ANKYRIN; BIOFUEL; CELLULASE; PRIMER DNA;

AMINO ACID SEQUENCE; ARTICLE; BIOTECHNOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; CLOSTRIDIUM THERMOCELLUM; GENETICS; MATRIX ATTACHMENT REGION; METABOLISM; METHODOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN CONFORMATION; THERMOTOGA MARITIMA;

AMINO ACID SEQUENCE; ANKYRINS; BASE SEQUENCE; BIOFUELS; BIOTECHNOLOGY; CELLULASES; CIRCULAR DICHROISM; CLONING, MOLECULAR; CLOSTRIDIUM THERMOCELLUM; DNA PRIMERS; MATRIX ATTACHMENT REGIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; THERMOTOGA MARITIMA;

EID: 84886918062     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02121-13     Document Type: Article

References (64)

1. Hill J, Nelson E, Tilman D, Polasky S, Tiffany D. 2006. Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc. Natl. Acad. Sci. U.S.A. 103:11206-11210.
2. Yang B, Dai Z, Ding S-Y, Wyman CE. 2011. Enzymatic hydrolysis of cellulosic biomass. Biofuels 2:421-450.
3. Sun Y, Cheng J. 2002. Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresour. Technol. 83:1-11.
4. Chhabra SR, Shockley KR, Conners SB, Scott KL, Wolfinger RD, Kelly RM. 2003. Carbohydrate-induced differential gene expression patterns in the hyperthermophilic bacterium Thermotoga maritima. J. Biol. Chem. 278:7540-7552.
5. Chhabra SR, Shockley KR, Ward DE, Kelly RM. 2002. Regulation of endo-acting glycosyl hydrolases in the hyperthermophilic bacterium Thermotoga maritima grown on glucan- and mannan-based polysaccharides. Appl. Environ. Microbiol. 68:545-554.
6. Bronnenmeier K, Kern A, Liebl W, Staudenbauer WL. 1995. Purification of Thermotoga maritima enzymes for the degradation of cellulosic materials. Appl. Environ. Microbiol. 61:1399-1407.
7. Beguin P, Lemaire M. 1996. The cellulosome: an exocellular, multiprotein complex specialized in cellulose degradation. Crit. Rev. Biochem. Mol. Biol. 31:201-236.
8. Krauss J, Zverlov VV, Schwarz WH. 2012. In vitro reconstitution of the omplete Clostridium thermocellum cellulosome and synergistic activity on crystalline cellulose. Appl. Environ. Microbiol. 78:4301-4307.
9. Matthews BW, Nicholson H, Becktel WJ. 1987. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc. Natl. Acad. Sci. U.S.A. 84:6663-6667.
10. DeSantis G, Jones JB. 1999. Chemical modification of enzymes for enhanced functionality. Curr. Opin. Biotechnol. 10:324-330.
11. Sriprapundh D, Vieille C, Zeikus JG. 2000. Molecular determinants of xylose isomerase thermal stability and activity: analysis of thermozymes by site-directed mutagenesis. Protein Eng. 13:259-265.
12. Liu W, Zhang XZ, Zhang Z, Zhang YH. 2010. Engineering of Clostridium phytofermentans endoglucanase Cel5A for improved thermostability. Appl. Environ. Microbiol. 76:4914-4917.
13. Bommarius AS, Broering JM, Chaparro-Riggers JF, Polizzi KM. 2006. High-throughput screening for enhanced protein stability. Curr. Opin. Biotechnol. 17:606-610.
14. Lehmann M, Wyss M. 2001. Engineering proteins for thermostability: the use of sequence alignments versus rational design and directed evolution. Curr. Opin. Biotechnol. 12:371-375.
15. Doi N, Yanagawa H. 1999. Insertional gene fusion technology. FEBS Lett. 457:1-4.
16. Kim CS, Pierre B, Ostermeier M, Looger LL, Kim JR. 2009. Enzyme stabilization by domain insertion into a thermophilic protein. Protein Eng. Des. Sel. 22:615-623.
17. Ha JH, Karchin JM, Walker-Kopp N, Huang LS, Berry EA, Loh SN. 2012. Engineering domain-swapped binding interfaces by mutually exclusive folding. J. Mol. Biol. 416:495-502.
18. 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.
19. Lamed R, Setter E, Bayer EA. 1983. Characterization of a cellulosebinding, cellulase-containing complex in Clostridium thermocellum. J. Bacteriol. 156:828-836.
20. Bayer EA, Belaich JP, Shoham Y, Lamed R. 2004. The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu. Rev. Microbiol. 58:521-554.
21. Betton JM, Jacob JP, Hofnung M, Broome-Smith JK. 1997. Creating a bifunctional protein by insertion of beta-lactamase into the maltodextrinbinding protein. Nat. Biotechnol. 15:1276-1279.
22. Cutler TA, Mills BM, Lubin DJ, Chong LT, Loh SN. 2009. Effect of interdomain linker length on an antagonistic folding-unfolding equilibrium between two protein domains. J. Mol. Biol. 386:854-868.
23. Sedgwick SG, Smerdon SJ. 1999. The ankyrin repeat: a diversity of interactions on acommonstructural framework. Trends Biochem. Sci. 24:311-316.
24. Zweifel ME, Barrick D. 2001. Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. 2. Solution stability and cooperativity of unfolding. Biochemistry 40:14357-14367.
25. Zweifel ME, Leahy DJ, Hughson FM, Barrick D. 2003. Structure and stability of the ankyrin domain of the Drosophila Notch receptor. Protein Sci. 12:2622-2632.
26. Wetzel SK, Settanni G, Kenig M, Binz HK, Pluckthun A. 2008. Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J. Mol. Biol. 376:241-257.
27. Tripp KW, Barrick D. 2008. Rerouting the folding pathway of the Notch ankyrin domain by reshaping the energy landscape. J. Am. Chem. Soc. 130:5681-5688.
28. Aksel T, Majumdar A, Barrick D. 2011. The contribution of entropy, enthalpy, and hydrophobic desolvation to cooperativity in repeat-protein folding. Structure 19:349-360.
29. Aksel T, Barrick D. 2009. Analysis of repeat-protein folding using nearest- neighbor statistical mechanical models. Methods Enzymol. 455:95-125.
30. Carrion-Vazquez M, Oberhauser AF, Fowler SB, Marszalek PE, Broedel SE, Clarke J, Fernandez JM. 1999. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. U.S.A. 96:3694-3699.
31. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41:207-234.
32. Edelhoch H. 1967. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6:1948-1954.
33. Pace NC, Tanford C. 1968. Thermodynamics of the unfolding of betalactoglobulin A in aqueous urea solutions between 5 and 55 degrees. Biochemistry 7:198-208.
34. Scholtz JM, Grimsley GR, Pace CN. 2009. Solvent denaturation of proteins and interpretations of themvalue. Methods Enzymol. 466:549-565.
35. Pace CN, Shaw KL. 2000. Linear extrapolation method of analyzing solvent denaturation curves. Proteins Suppl. 4:1-7.
36. Pace CN. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:266-280.
37. Pace CN, Vanderburg KE. 1979. Determining globular protein stability: guanidine hydrochloride denaturation of myoglobin. Biochemistry 18: 288-292.
38. Greene RF, Jr, Pace CN. 1974. Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and betalactoglobulin. J. Biol. Chem. 249:5388-5393.
39. Zhang YH, Cui J, Lynd LR, Kuang LR. 2006. A transition from cellulose swelling to cellulose dissolution by o-phosphoric acid: evidence from enzymatic hydrolysis and supramolecular structure. Biomacromolecules 7:644-648.
40. Ghose T. 1987. Measurement of cellulase activities. Pure Appl. Chem. 59:257-268.
41. Johnson EA, Sakajoh M, Halliwell G, Madia A, Demain AL. 1982. Saccharification of complex cellulosic substrates by the cellulase system from Clostridium thermocellum. Appl. Environ. Microbiol. 43: 1125-1132.
42. Schwarz WH, Grabnitz F, Staudenbauer WL. 1986. Properties of a Clostridium thermocellum endoglucanase produced in Escherichia coli. Appl. Environ. Microbiol. 51:1293-1299.
43. Liebl W, Ruile P, Bronnenmeier K, Riedel K, Lottspeich F, Greif I. 1996. Analysis of a Thermotoga maritima DNA fragment encoding two similar thermostable cellulases, CelA and CelB, and characterization of the recombinant enzymes. Microbiology 142:2533-2542.
44. Schuster-Bockler B, Schultz J, Rahmann S. 2004. HMM logos for visualization of protein families. BMC Bioinformatics 5:7. doi:10.1186/1471 -2105-5-7.
45. Cheng YS, Ko TP, Wu TH, Ma Y, Huang CH, Lai HL, Wang AH, Liu JR, Guo RT. Crystal structure and substrate-binding mode of cellulase 12A from Thermotoga maritima. Proteins 79:1193-1204.
46. Alzari PM, Souchon H, Dominguez R. 1996. The crystal structure of endoglucanase CelA, a family 8 glycosyl hydrolase from Clostridium thermocellum. Structure 4:265-275.
47. Faure E, Bagnara C, Belaich A, Belaich JP. 1988. Cloning and expression of two cellulase genes of Clostridium cellulolyticum in Escherichia coli. Gene 65:51-58.
48. Chhabra SR, Kelly RM. 2002. Biochemical characterization of Thermotoga maritima endoglucanase Cel74 with and without a carbohydrate binding module (CBM). FEBS Lett. 531:375-380.
49. Jackson WM, Brandts JF. 1970. Thermodynamics of protein denaturation. A calorimetric study of the reversible denaturation of chymotrypsinogen and conclusions regarding the accuracy of the two-state approximation. Biochemistry 9:2294-2301.
50. Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31:426-428.
51. US Department of Energy. 2006. Breaking the biological barriers to cellulosic ethanol: a joint research agenda. A research roadmap resulting from the Biomass to Biofuels Workshop, December 7-9, 2005, Rockville, Maryland. DOE/SC-0095. US Department of Energy Office of Science, Washington, DC.
52. Fierobe HP, Bayer EA, Tardif C, Czjzek M, Mechaly A, Belaich A, Lamed R, Shoham Y, Belaich JP. 2002. Degradation of cellulose substrates by cellulosome chimeras: substrate targeting versus proximity of enzyme components. J. Biol. Chem. 277:49621-49630.
53. Fierobe HP, Mingardon F, Mechaly A, Belaich A, Rincon MT, Pages S, Lamed R, Tardif C, Belaich JP, Bayer EA. 2005. Action of designer cellulosomes on homogeneous versus complex substrates: controlled incorporation of three distinct enzymes into a defined trifunctional scaffoldin. J. Biol. Chem. 280:16325-16334.
54. Mitsuzawa S, Kagawa H, Li Y, Chan SL, Paavola CD, Trent JD. 2009. The rosettazyme: a synthetic cellulosome. J. Biotechnol. 143:139-144.
55. Collins T, Meuwis MA, Gerday C, Feller G. 2003. Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J. Mol. Biol. 328:419-428.
56. Vieille C, Zeikus GJ. 2001. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev. 65:1-43.
57. Merz T, Wetzel SK, Firbank S, Plückthun A, Grütter MG, Mittl PR. 2008. Stabilizing ionic interactions in a full-consensus ankyrin repeat protein. J. Mol. Biol. 376:232-240.
58. Cheng YS, Ko TP, Huang JW, Wu TH, Lin CY, Luo W, Li Q, Ma Y, Huang CH, Wang AH, Liu JR, Guo RT. 2012. Enhanced activity of Thermotoga maritima cellulase 12A by mutating a unique surface loop. Appl. Microbiol. Biotechnol. 95:661-669.
59. Sandgren M, Gualfetti PJ, Shaw A, Gross LS, Saldajeno M, Day AG, Jones TA, Mitchinson C. 2003. Comparison of family 12 glycoside hydrolases and recruited substitutions important for thermal stability. Protein Sci. 12:848-860.
60. Sandgren M, Stahlberg J, Mitchinson C. 2005. Structural and biochemical studies of GH family 12 cellulases: improved thermal stability, and ligand complexes. Prog. Biophys. Mol. Biol. 89:246-291.
61. Myers JK, Pace CN, Scholtz JM. 1995. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4:2138-2148.
62. Fontana A. 1988. Structure and stability of thermophilic enzymes: studies on thermolysin. Biophys. Chem. 29:181-193.
63. D'Amico S, Marx JC, Gerday C, Feller G. 2003. Activity-stability relationships in extremophilic enzymes. J. Biol. Chem. 278:7891-7896.
64. Beaucamp N, Hofmann A, Kellerer B, Jaenicke R. 1997. Dissection of the gene of the bifunctional PGK-TIM fusion protein from the hyperthermophilic bacterium Thermotoga maritima: design and characterization of the separate triosephosphate isomerase. Protein Sci. 6:2159-2165.