Engineered thermostable fungal Cel6A and Cel7A cellobiohydrolases hydrolyze cellulose efficiently at elevated temperatures

Biotechnology and Bioengineering

Volumn 110, Issue 7, 2013, Pages 1874-1883

  Wu, Indira ^a   Arnold, Frances H ^a  

^a California Institute of Technology   (United States)

Author keywords

Biofuel; CBHII; Cellulase synergy; Enzyme thermostability; Fungal cellulase; Proline substitutions

Indexed keywords

CBHII; CELLULASE SYNERGY; ELEVATED TEMPERATURE; FUNGAL CELLULASE; HYDROLYZE CELLULOSE; HYDROPHOBIC INTERACTIONS; OPTIMUM TEMPERATURE; THERMOSTABILIZATION;

BINARY MIXTURES; BIOFUELS; FUNGI;

HYDROLYSIS;

CELLOBIOSE; CELLULASE; CELLULOSE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; PROLINE; PROTEIN CEL6A; PROTEIN CEL7A; UNCLASSIFIED DRUG;

ARTICLE; BIOENGINEERING; CONTROLLED STUDY; CRYSTAL STRUCTURE; FUNGUS; GENETIC RECOMBINATION; HIGH TEMPERATURE; HUMICOLA INSOLENS; HYDROLYSIS; HYDROPHOBICITY; HYPOCREA JECORINA; MUTAGENESIS; NONHUMAN; THERMOSTABILITY;

CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; CRYSTALLOGRAPHY, X-RAY; DIRECTED MOLECULAR EVOLUTION; ENZYME STABILITY; HYDROLYSIS; HYPOCREA; KINETICS; MODELS, MOLECULAR; MUTAGENESIS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC; SORDARIALES; TEMPERATURE;

HUMICOLA INSOLENS; HYPOCREA JECORINA;

EID: 84878391705     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24864     Document Type: Article

References (53)

1. Abdel-Banat BMA, Hoshida H, Ano A, Nonklang S, Akada R. 2010. High-temperature fermentation: How can processes for ethanol production at high temperatures become superior to the traditional process using mesophilic yeast? Appl Microbiol Biotechnol 85(4):861-867.
2. Anbar M, Bayer EA. 2012. Approaches for improving thermostability characteristics in cellulases. Methods Enzymol 510:261-271.
3. Bajaj K, Madhusudhan MS, Adkar BV, Chakrabarti P, Ramakrishnan C, Sali A, Varadarajan R. 2007. Stereochemical criteria for prediction of the effects of proline mutations on protein stability. PLoS Comput Biol 3(12):e241.
4. Boisset C, Fraschini C, Schulein M, Henrissat B, Chanzy H. 2000. Imaging the enzymatic digestion of bacterial cellulose ribbons reveals the endo character of the cellobiohydrolase Cel6a from Humicola insolens and its mode of synergy with cellobiohydrolase Cel7a. Appl Environ Microbiol 66(4):1444-1452.
5. Boisset C, Petrequin C, Chanzy H, Henrissat B, Schulein M. 2001. Optimized mixtures of recombinant Humicola insolens cellulases for the biodegradation of crystalline cellulose. Biotechnol Bioeng 72(3):339-345.
6. 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(Database issue):D233-D238.
7. Carrard G, Linder M. 1999. Widely different off rates of two closely related cellulose-binding domains from Trichoderma reesei. Eur J Biochem 262(3):637-643.
8. Chao G, Lau WL, Hackel BJ, Sazinsky SL, Lippow SM, Wittrup KD. 2006. Isolating and engineering human antibodies using yeast surface display. Nat Protoc 1(2):755-768.
9. Chen Y, Stevens MA, Zhu Y, Holmes J, Moxley G, Xu H. 2012. Reducing acid in dilute acid pretreatment and the impact on enzymatic saccharification. J Ind Microbiol Biotechnol 39(5):691-700.
10. Cherry JR, Fidantsef AL. 2003. Directed evolution of industrial enzymes: An update. Curr Opin Biotechnol 14(4):438-443.
11. Cirino PC, Mayer KM, Umeno D. 2003. Generating mutant libraries using error-prone PCR. In: Arnold FH, Georgiou G, editors. Methods in molecular biology, vol 231: Directed evolution library creation: Methods and protocols. Totowa, NJ: Humana Press. p 3-9.
12. Cuneo MJ, Tian Y, Allert M, Hellinga HW. 2008. The backbone structure of the thermophilic thermoanaerobacter tengcongensis ribose binding protein is essentially identical to its mesophilic E. coli homolog. BMC Struct Biol 8:20.
13. Dana CM, Saija P, Kal SM, Bryan MB, Blanch HW, Clark DS. 2012. Biased clique shuffling reveals stabilizing mutations in cellulase Cel7A. Biotechnol Bioeng 109(11):2710-2719.
14. Dumon C, Varvak A, Wall MA, Flint JE, Lewis RJ, Lakey JH, Morland C, Luginbuhl P, Healey S, Todaro T, DeSantis G, Sun M, Parra-Gessert L, Tan X, Weiner DP, Gilbert HJ. 2008. Engineering hyperthermostability into a GH11 xylanase is mediated by subtle changes to protein structure. J Biol Chem 283(33):22557-22564.
15. Ferdjani S, Ionita M, Roy B, Dion M, Djeghaba Z, Rabiller C, Tellier C. 2011. Correlation between thermostability and stability of glycosidases in ionic liquid. Biotechnol Lett 33(6):1215-1219.
16. Fu H, Grimsley GR, Razvi A, Scholtz JM, Pace CN. 2009. Increasing protein stability by improving beta-turns. Proteins 77(3):491-498.
17. Fu C, Mielenz JR, Xiao X, Ge Y, Hamilton CY, Rodriguez M, Jr. Chen F, Foston M, Ragauskas A, Bouton J, Dixon RA, Wang ZY. 2011. Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci U S A 108(9):3803-3808.
18. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In: Walker, JM, editor. The proteomics protocols handbook. Totowa, NJ: Humana Press. p 571-607.
19. Georgescu R, Bandara G, Sun L. 2003. Saturation mutagenesis. In: Arnold FH, Georgiou G, editors. Methods in molecular biology, vol 231: Directed evolution library creation: Methods and protocols. Totowa, NJ: Humana Press. p 75-83.
20. Heinzelman P, Snow CD, Wu I, Nguyen C, Villalobos A, Govindarajan S, Minshull J, Arnold FH. 2009a. A family of thermostable fungal cellulases created by structure-guided recombination. Proc Natl Acad Sci U S A 106(14):5610-5615.
21. Heinzelman P, Snow CD, Smith MA, Yu X, Kannan A, Boulware K, Villalobos A, Govindarajan S, Minshull J, Arnold FH. 2009b. Schema recombination of a fungal cellulase uncovers a single mutation that contributes markedly to stability. J Biol Chem 284(39):26229-26233.
22. Heinzelman P, Komor R, Kannan A, Romero P, Yu X, Mohler S, Snow C, Arnold FH. 2010. Efficient screening of fungal cellobiohydrolase class I enzymes for thermostabilizing sequence blocks by schema structure-guided recombination. Protein Eng Des Sel 23(11). 871-880.
23. Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VGH. 2012. Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45.
24. Hutchinson EG, Thornton JM. 1994. A revised set of potentials for beta-turn formation in proteins. Protein Sci 3(12):2207-2216.
25. Igarashi K, Uchihashi T, Koivula A, Wada M, Kimura S, Okamoto T, Penttila M, Ando T, Samejima M. 2011. Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 333(6047):1279-1282.
26. Jordan DB, Bowman MJ, Braker JD, Dien BS, Hector RE, Lee CC, Mertens JA, Wagschal K. 2012. Plant cell walls to ethanol. Biochem J 442(2):241-252.
27. Jung JH, Fouad WM, Vermerris W, Gallo M, Altpeter F. 2012. RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass. Plant Biotechnol J 10(9):1067-1076.
28. Klein-Marcuschamer D, Oleskowicz-Popiel P, Simmons BA, Blanch HW. 2012. The challenge of enzyme cost in the production of lignocellulosic biofuels. Biotechnol Bioeng 109(4):1083-1087.
29. Komor RS, Romero PA, Xie CB, Arnold FH. 2012. Highly thermostable fungal cellobiohydrolase I (Cel7A) engineered using predictive methods. Protein Eng Des Sel 25(12):827-833.
30. Kuhad RC, Gupta R, Singh A. 2011. Microbial cellulases and their industrial applications. Enzyme Res 2011:280696.
31. Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E, Sweeney MD. 2011. Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77(19):7007-7015.
32. Lantz SE, Goedegebuur F, Hommes R, Kaper T, Kelemen BR, Mitchinson C, Wallace L, Stahlberg J, Larenas EA. 2010. Hypocrea jecorina CEL6A protein engineering. Biotechnol Biofuels 3:20.
33. MacArthur MW, Thornton JM. 1991. Influence of proline residues on protein conformation. J Mol Biol 218(2):397-412.
34. 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(19):6663-6667.
35. Medve J, Stahlberg J, Tjerneld F. 1994. Adsorption and synergism of cellobiohydrolase I and II of Trichoderma reesei during hydrolysis of microcrystalline cellulose. Biotechnol Bioeng 44(9):1064-1073.
36. Nelson N. 1944. A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375-380.
37. Ohage EC, Graml W, Walter MM, Steinbacher S, Steipe B. 1997. Beta-turn propensities as paradigms for the analysis of structural motifs to engineer protein stability. Protein Sci 6(1):233-241.
38. Parry NJ, Beever DE, Owen E, Nerinckx W, Claeyssens M, Van Beeumen J, Bhat MK. 2002. Biochemical characterization and mode of action of a thermostable endoglucanase purified from Thermoascus aurantiacus. Arch Biochem Biophys 404(2):243-253.
39. Prajapati RS, Das M, Sreeramulu S, Sirajuddin M, Srinivasan S, Krishnamurthy V, Ranjani R, Ramakrishnan C, Varadarajan R. 2007. Thermodynamic effects of proline introduction on protein stability. Proteins 66(2):480-491.
40. Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen JCN, Johansen KS, Krogh K, Jorgensen CI, Tovborg M, Anthonsen A, Tryfona T, Walter CP, Dupree P, Xu F, Davies GJ, Walton PH. 2011. Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci U S A 108:15079-15084.
41. Rosgaard L, Pedersen S, Cherry JR, Harris P, Meyer AS. 2006. Efficiency of new fungal cellulase systems in boosting enzymatic degradation of barley straw lignocellulose. Biotechnol Prog 22(2):493-498.
42. Saloheimo M, Pakula TM. 2012. The cargo and the transport system: Secreted proteins and protein secretion in Trichoderma reesei (Hypocrea jecorina). Microbiology 158(Pt 1):46-57.
43. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssonen E, Bhatia A, Ward M, Penttila M. 2002. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269:4202-4211.
44. Shaw AJ, Podkaminer KK, Desai SG, Bardsley JS, Rogers SR, Thorne PG, Hogsett DA, Lynd LR. 2008. Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield. Proc Natl Acad Sci U S A 105(37):13769-13774.
45. Somogyi M. 1951. Notes on sugar determination. J Biol Chem 195:19-23.
46. Suwannarangsee S, Bunterngsook B, Arnthong J, Paemanee A, Thamchaipenet A, Eurwilaichitr L, Laosiripojana N, Champreda V. 2012. Optimisation of synergistic biomass-degrading enzyme systems for efficient rice straw hydrolysis using an experimental mixture design. Bioresour Technol 119:252-261.
47. Tao L, Aden A, Elander RT, Pallapolu VR, Lee YY, Garlock RJ, Balan V, Dale BE, Kim Y, Mosier NS, Ladisch MR, Falls M, Holtzapple MT, Sierra R, Shi J, Ebrik MA, Redmond T, Yang B, Wyman CE, Hames B, Thomas S, Warner RE. 2011. Process and technoeconomic analysis of leading pretreatment technologies for lignocellulosic ethanol production using switchgrass. Bioresour Technol 102(24):11105-11114.
48. Tomme P, Warren RA, Gilkes NR. 1995. Cellulose hydrolysis by bacteria and fungi. Adv Microb Physiol 37:1-81.
49. Trevino SR, Schaefer S, Scholtz JM, Pace CN. 2007. Increasing protein conformational stability by optimizing beta-turn sequence. J Mol Biol 373(1):211-218.
50. Vieille C, Zeikus GJ. 2001. Hyperthermophilic enzymes: Sources uses and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65(1):1-43.
51. Viikari L, Alapuranen M, Puranen T, Vehmaanpera J, Siika-Aho M. 2007. Thermostable enzymes in lignocellulose hydrolysis. Adv Biochem Eng Biotechnol 108:121-145.
52. Watanabe K, Masuda T, Ohashi H, Mihara H, Suzuki Y. 1994. Multiple proline substitutions cumulatively thermostabilize Bacillus cereus ATCC7064 oligo-1, 6-glucosidase. Irrefragable proof supporting the proline rule. Eur J Biochem 226(2):277-283.
53. Woodward J, Hayes MK, Lee NE. 1988. Hydrolysis of cellulose by saturating and non-saturating concentrations of cellulase: Implications for synergism. Nat Biotechnol 6:301-304.