Discovery and characterization of a thermostable and highly halotolerant GH5 cellulase from an icelandic hot spring isolate

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Zarafeta, Dimitra ^a,b   Kissas, Dimitrios ^a,b   Sayer, Christopher ^c   Gudbergsdottir, Sóley R ^d   Ladoukakis, Efthymios ^b   Isupov, Michail N ^c   Chatziioannou, Aristotelis ^a   Peng, Xu ^d   Littlechild, Jennifer A ^c   Skretas, Georgios ^a   Kolisis, Fragiskos N ^b  

^a INSTITUTE OF BIOLOGY   (Greece)

^b NATIONAL TECHNICAL UNIVERSITY OF ATHENS   (Greece)

^c UNIVERSITY OF EXETER   (United Kingdom)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CALCIUM CHLORIDE; CARBOXYMETHYLCELLULOSE; CELDZ1ALPHA ENZYME; CELLULASE; COPPER CHLORIDE; FERROUS CHLORIDE; GLUCAN SYNTHASE; GLYCOSIDASE; LITHIUM CHLORIDE; MANGANESE CHLORIDE; MERCAPTOETHANOL; METAL ION; METHANOL; UNCLASSIFIED DRUG; ZINC CHLORIDE; BACTERIAL PROTEIN; CELLULOSE; CHLORIDE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATE; BIOCHEMICAL ANALYSIS; BIOINFORMATICS; CATALYSIS; CELDZ1ALPHA GENE; CELLULOLYTIC ACTIVITY; CONTROLLED STUDY; DEGRADATION; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME STRUCTURE; HIGH TEMPERATURE; HYDROLYSIS; ICELAND; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PH; PROTEIN DOMAIN; SALT TOLERANCE; STRUCTURE ANALYSIS; THERMAL SPRING; THERMOANAEROBACTERIUM; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; HEAT; KINETICS; MICROBIOLOGY; MOLECULAR MODEL; THERMOANAEROBACTER;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; CELLULASE; CELLULOSE; CHLORIDES; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; HOT SPRINGS; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; ICELAND; KINETICS; MODELS, MOLECULAR; SALT-TOLERANCE; SUBSTRATE SPECIFICITY; THERMOANAEROBACTER;

EID: 84954143417     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146454     Document Type: Article

References (64)

1. Klemm D, Schmauder HP, Heinze T. Cellulose. Biopolymers online. 2005.
2. Bayer EA, Chanzy H, Lamed R, Shoham Y. Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol. 1998;8(5):548-57. PMID: 9818257
3. Bhat M. Cellulases and related enzymes in biotechnology. Biotechnol Adv. 2000;18(5):355-83. PMID: 14538100
4. Klemm D, Heublein B, Fink HP, Bohn A. Cellulose: fascinating biopolymer and sustainable raw material. Angew Chem Int Ed Engl. 2005;44(22):3358-93. PMID: 15861454
5. Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG. Novel enzymes for the degradation of cellulose. Biotechnol Biofuels. 2012;5(1):1-13.
6. Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, et al. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science. 2007;315(5813):804-7. PMID: 17289988
7. Zhang XZ, Zhang YHP. Cellulases: Characteristics, Sources, Production, and Applications. Bioprocessing Technologies in Biorefinery for Sustainable Production of Fuels, Chemicals, and Polymers.. 2013:131-46.
8. Dalby PA. Strategy and success for the directed evolution of enzymes. Curr Opin Struct Biol. 2011;21(4):473-80. doi: 10.1016/j.sbi.2011.05.003 PMID: 21684150
9. Bornscheuer U, Huisman G, Kazlauskas R, Lutz S, Moore J, Robins K. Engineering the third wave of biocatalysis. Nature. 2012;485(7397):185-94. doi: 10.1038/nature11117 PMID: 22575958
10. Bornscheuer UT, Pohl M. Improved biocatalysts by directed evolution and rational protein design. Curr Opin Chem Biol. 2001;5(2):137-43. PMID: 11282339
11. Ito Y, Ikeuchi A, Imamura C. Advanced evolutionary molecular engineering to produce thermostable cellulase by using a small but efficient library. Protein Eng Des Sel. 2013;26(1):73-9. doi: 10.1093/protein/gzs072 PMID: 23091162
12. Liang C, Fioroni M, Rodríguez-Ropero F, Xue Y, Schwaneberg U, Ma Y. Directed evolution of a thermophilic endoglucanase (Cel5A) into highly active Cel5A variants with an expanded temperature profile. J Biotechnology. 2011;154(1):46-53.
13. Kim Y-S, Jung H-C, Pan J-G. Bacterial cell surface display of an enzyme library for selective screening of improved cellulase variants. Appl Environ Microbiol. 2000;66(2):788-93. PMID: 10653752
14. Lorenz P, Liebeton K, Niehaus F, Eck J. Screening for novel enzymes for biocatalytic processes: accessing the metagenome as a resource of novel functional sequence space. Curr Opin Biotechnol. 2002;13(6):572-7. PMID: 12482516
15. Alvarez TM, Paiva JH, Ruiz DM, Cairo JPL, Pereira IO, Paixão DA, et al. Structure and Function of a Novel Cellulase 5 from Sugarcane Soil Metagenome. PLoS One. 2013;8(12):e83635. doi: 10.1371/journal.pone.0083635 PMID: 24358302
16. Voget S, Steele H, Streit W. Characterization of a metagenome-derived halotolerant cellulase. J Biotechnology. 2006;126(1):26-36.
17. Wang F, Li F, Chen G, Liu W. Isolation and characterization of novel cellulase genes from uncultured microorganisms in different environmental niches. Microbiol Res. 2009;164(6):650-7. doi: 10.1016/j. micres.2008.12.002 PMID: 19230636
18. Graham JE, Clark ME, Nadler DC, Huffer S, Chokhawala HA, Rowland SE, et al. Identification and characterization of a multidomain hyperthermophilic cellulase from an archaeal enrichment. Nat Commun. 2011;2:375. doi: 10.1038/ncomms1373 PMID: 21730956
19. Kim JW, Peeples TL. Screening extremophiles for bioconversion potentials. Biotechnol Prog. 2006;22(6):1720-4. PMID: 17137324
20. Demirjian DC, Morís-Varas F, Cassidy CS. Enzymes from extremophiles. Curr Opin Chem Biol. 2001;5(2):144-51. PMID: 11282340
21. Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data. Genome Res. 2007;17(3):377-86. PMID: 17255551
22. Fukumori F, Kudo T, Narahashi Y, Horikoshi K. Molecular cloning and nucleotide sequence of the alkaline cellulase gene from the alkalophilic Bacillus sp. strain 1139. J Gen Microbiol. 1986;132(8):2329-35. PMID: 3098909
23. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, et al. The Pfam protein families database. Nucleic Acids Res. 2004;32(suppl 1):D138-D41.
24. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011;39:W29-W37. gkr367 doi: 10.1093/nar/gkr367 PMID: 21593126
25. Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42(D1):D490-D5.
26. Petersen TN, Brunak S, Von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785-6. doi: 10.1038/nmeth.1701 PMID: 21959131
27. Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem. 1959;31(3):426-8.
28. Liang C, Xue Y, Fioroni M, Rodríguez-Ropero F, Zhou C, Schwaneberg U, et al. Cloning and characterization of a thermostable and halo-tolerant endoglucanase from Thermoanaerobacter tengcongensis MB4. Appl Microbiol Biotechnol. 2011;89(2):315-26. doi: 10.1007/s00253-010-2842-6 PMID: 20803139
29. Shirai T, Ishida H, Noda J-I, Yamane T, Ozaki K, Hakamada Y, et al. Crystal structure of alkaline cellulase K: insight into the alkaline adaptation of an industrial enzyme. J Mol Biol. 2001;310(5):1079-87. PMID: 11501997
30. Klinke HB, Thomsen A, Ahring BK. Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol. 2004;66(1):10-26. PMID: 15300416
31. Patel S, Saraf M. Perspectives and Application of Halophilic Enzymes. Halophiles: Springer; 2015. p. 403-19.
32. Sá-Pereira P, Mesquita A, Duarte JC, Barros MRA, Costa-Ferreira M. Rapid production of thermostable cellulase-free xylanase by a strain of Bacillus subtilis and its properties. Enzyme Microb Technol. 2002;30(7):924-33.
33. Dutta T, Sengupta R, Sahoo R, Sinha Ray S, Bhattacharjee A, Ghosh S. A novel cellulase free alkaliphilic xylanase from alkali tolerant Penicillium citrinum: production, purification and characterization. Lett Appl Microbiol. 2007;44(2):206-11. PMID: 17257262
34. Silva JCR, Guimarães LHS, Salgado JCS, Furriel RPM, Polizeli MLT, Rosa JC, et al. Purification and biochemical characterization of glucose-cellobiose-tolerant cellulases from Scytalidium thermophilum. Folia Microbiol (Praha). 2013;58(6):561-8.
35. Caldwell P, Luk DC, Weissbach H, Brot N. Oxidation of the methionine residues of Escherichia coli ribosomal protein L12 decreases the protein's biological activity. Proc Natl Acad Sci U S A. 1978;75(11):5349-52. PMID: 364476
36. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr. 1993;26(2):283-91.
37. Vaguine AA, Richelle J, Wodak S. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr D Biol Crystallogr. 1999;55(1):191-205.
38. Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007;372(3):774-97. PMID: 17681537
39. Varrot A, Schu Èlein M, Fruchard S, Driguez H, Davies GJ. Atomic resolution structure of endoglucanase Cel5A in complex with methyl 4, 4II, 4III, 4IV-tetrathio-α-cellopentoside highlights the alternative binding modes targeted by substrate mimics. Acta Crystallogr D Biol Crystallogr. 2001;57(11):1739-42.
40. De Lano WL. The PyMOL molecular graphics system. 2002. Availiable: http://www.pymol.org
41. McNicholas S, Potterton E, Wilson K, Noble M. Presenting your structures: the CCP4mg moleculargraphics software. Acta Crystallogr D Biol Crystallogr. 2011;67(4):386-94.
42. Fukuchi S, Yoshimune K, Wakayama M, Moriguchi M, Nishikawa K. Unique amino acid composition of proteins in halophilic bacteria. J Mol Biol. 2003;327(2):347-57. PMID: 12628242
43. Elcock AH, McCammon JA. Electrostatic contributions to the stability of halophilic proteins. J Mol Biol. 1998;280(4):731-48. PMID: 9677300
44. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18(5):821-9. doi: 10.1101/gr.074492.107 PMID: 18349386
45. Noguchi H, Taniguchi T, Itoh T. MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. Genome Res. 2008;15(6):387-96.
46. Zhu Wenhan. Improvement of ab initio methods of gene prediction in genomic and metagenomic sequences. Dissemination. Georgia Intitute of Technology, 2010. Available: https://smartech.gatech.edu/handle/1853/33869?show=full
47. Hyatt D, Chen G-L, Lo Cascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11(1):119.
48. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-10. PMID: 2231712
49. Consortium U. UniProt: a hub for protein information. Nucleic Acids Res. 2014:gku989.
50. MySQL A. MySQL. 2001. Accesed: https://www.mysql.com
51. Kumar N, Skolnick J. EFICAz2. 5: application of a high-precision enzyme function predictor to 396 proteomes. Bioinformatics. 2012;28(20):2687-8. doi: 10.1093/bioinformatics/bts510 PMID: 22923291
52. Claudel-Renard C, Chevalet C, Faraut T, Kahn D. Enzyme-specific profiles for genome annotation: PRIAM. Nucleic Acids Res. 2003;31(22):6633-9. PMID: 14602924
53. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1):248-54.
54. Teather RM, Wood PJ. Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol. 1982;43(4):777-80. PMID: 7081984
55. Kabsch W. Xds. Acta Crystallogr D Biol Crystallogr. 2010;66(2):125-32.
56. Evans PR, Murshudov GN. How good are my data and what is the resolution? Acta Crystallogr D Biol Crystallogr. 2013;69(7):1204-14.
57. Winter G, Lobley CM, Prince SM. Decision making in xia2. Acta Crystallogr D Biol Crystallogr. 2013;69(7):1260-73.
58. Lebedev AA, Young P, Isupov MN, Moroz OV, Vagin AA, Murshudov GN. JLigand: a graphical tool for the CCP4 template-restraint library. Acta Crystallogr D Biol Crystallogr. 2012;68(4):431-40.
59. Vagin A, Teplyakov A. Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr. 2009;66(1):22-5.
60. Langer GG, Hazledine S, Wiegels T, Carolan C, Lamzin VS. Visual automated macromolecular model building. Acta Crystallogr D Biol Crystallogr. 2013;69(4):635-41.
61. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010;66(4):486-501.
62. Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr. 2011;67(4):355-67.
63. Cowtan K. Recent developments in classical density modification. Acta Crystallogr D Biol Crystallogr. 2010;66(4):470-8.
64. Pannu NS, Murshudov GN, Dodson EJ, Read RJ. Incorporation of prior phase information strengthens maximum-likelihood structure refinement. Acta Crystallogr D Biol Crystallogr. 1998;54(6):1285-94.