Identification of novel biomass-degrading enzymes from genomic dark matter: Populating genomic sequence space with functional annotation

Biotechnology and Bioengineering

Volumn 111, Issue 8, 2014, Pages 1550-1565

  Piao, Hailan ^a,b   Froula, Jeff ^c   Du, Changbin ^c   Kim, Tae Wan ^d,e   Hawley, Erik R ^a,b   Bauer, Stefan ^e   Wang, Zhong ^c   Ivanova, Nathalia ^c   Clark, Douglas S ^d,e   Klenk, Hans Peter ^f   Hess, Matthias ^a,b,c,g  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^c DOE JOINT GENOME INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Energy Biosciences Institute   (United States)

^f LEIBNIZ INSTITUTE DSMZ GERMAN COLLECTION OF MICROORGANISMS AND CELL CULTURES   (Germany)

^g PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Biomass degradation; CAZymes; Cellulases; Gene neighborhood analysis; Genomic dark matter; Gut microorganisms

Indexed keywords

BIOMASS; ENZYMES; GALAXIES; MICROORGANISMS; PROTEINS;

BIOMASS-DEGRADATION; CAZYMES; CELLULASES; DARK MATTER; GENE-NEIGHBORHOOD ANALYSIS;

GENES;

CARBOXYMETHYLCELLULOSE; CELLULASE; RECOMBINANT PROTEIN; BACTERIAL PROTEIN; CELLULOSE; LIGNIN; LIGNOCELLULOSE;

ARTICLE; BIOFUEL PRODUCTION; BIOMASS; ENZYME ACTIVITY; ENZYME DEGRADATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; GENE SYNTHESIS; HYDROLYSIS; MICROBIAL GENOME; NONHUMAN; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; BACTERIA; BACTERIAL GENE; GENETICS; GENOMICS; METABOLISM; MOLECULAR CLONING;

BACTERIA; BACTERIAL PROTEINS; BIOMASS; CELLULASES; CELLULOSE; CLONING, MOLECULAR; GENES, BACTERIAL; GENOMICS; HYDROLYSIS; LIGNIN;

EID: 84903266916     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25250     Document Type: Article

References (89)

1. Abdel-Hamid AM, Solbiati JO, Cann IK. 2013. Insights into lignin degradation and its potential industrial applications. Adv Appl Microbiol 82:1-28.
2. Abt B, Teshima H, Lucas S, Lapidus A, Del Rio TG, Nolan M, Tice H, Cheng JF, Pitluck S, Liolios K, Pagani I, Ivanova N, Mavromatis K, Pati A, Tapia R, Han C, Goodwin L, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Rohde M, Goker M, Tindall BJ, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Klenk HP, Kyrpides NC. 2011. Complete genome sequence of Leadbetterella byssophila type strain (4M15). Stand Genomic Sci 4:2-12.
3. Al-Shahib A, Breitling R, Gilbert DR. 2007. Predicting protein function by machine learning on amino acid sequences-A critical evaluation. BMC Genomics 8:78.
4. Amore A, Pepe O, Ventorino V, Birolo L, Giangrande C, Faraco V. 2012. Cloning and recombinant expression of a cellulase from the cellulolytic strain Streptomyces sp. G12 isolated from compost. Microb Cell Fact 11:164.
5. Bakir MA, Kitahara M, Sakamoto M, Matsumoto M, Benno Y. 2006. Bacteroides finegoldii sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 56:931-935.
6. Bolam DN, Xie HF, White P, Simpson PJ, Hancock SM, Williamson MP, Gilbert HJ. 2001. Evidence for synergy between family 2b carbohydrate binding modules in Cellulomonas fimi xylanase11A. Biochemistry 40:2468-2477.
7. Cai YD, Ricardo PW, Jen CH, Chou KC. 2004. Application of SVM to predict membrane protein types. J Theor Biol 226:373-376.
8. 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.
9. Caspi J, Barak Y, Haimovitz R, Irwin D, Lamed R, Wilson DB, Bayer EA. 2009. Effect of linker length and dockerin position on conversion of a Thermobifida fusca endoglucanase to the cellulosomal mode. Appl Environ Microbiol 75:7335-7342.
10. Cavaletti L, Monciardini P, Bamonte R, Schumann P, Rohde M, Sosio M, Donadio S. 2006. New lineage of filamentous, spore-forming, gram-positive bacteria from soil. Appl Environ Microbiol 72:4360-4369.
11. Chang JJ, Ho FJ, Ho CY, Wu YC, Hou YH, Huang CC, Shih MC, Li WH. 2013. Assembling a cellulase cocktail and a cellodextrin transporter into a yeast host for CBP ethanol production. Biotechnology for Biofuels 6:19.
12. Chang YJ, Land M, Hauser L, Chertkov O, Del Rio TG, Nolan M, Copeland A, Tice H, Cheng JF, Lucas S, Han C, Goodwin L, Pitluck S, Ivanova N, Ovchinikova G, Pati A, Chen A, Palaniappan K, Mavromatis K, Liolios K, Brettin T, Fiebig A, Rohde M, Abt B, Goker M, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Lapidus A. 2011. Non-contiguous finished genome sequence and contextual data of the filamentous soil bacterium Ktedonobacter racemifer type strain (SOSP1-21). Stand Genomic Sci 5:97-111.
13. Chaudet MM, Allen JL, Rose DR. 2012. Expression and purification of two Family GH31 alpha-glucosidases from Bacteroides thetaiotaomicron. Protein Expr Purif 86:135-141.
14. Chelius MK, Triplett EW. 2000. Dyadobacter fermentans gen. nov., sp. nov., a novel gram-negative bacterium isolated from surface-sterilized Zea mays stems. Int J Syst Evol Microbiol 50(Pt 2):751-758.
15. Chen S, Dong X. 2005. Proteiniphilum acetatigenes gen. nov., sp. nov., from a UASB reactor treating brewery wastewater. Int J Syst Evol Microbiol 55:2257-2261.
16. Cho KH, Salyers AA. 2001. Biochemical analysis of interactions between outer membrane proteins that contribute to starch utilization by Bacteroides thetaiotaomicron. J Bacteriol 183:7224-7230.
17. Copeland A, Zhang X, Misra M, Lapidus A, Nolan M, Lucas S, Deshpande S, Cheng JF, Tapia R, Goodwin LA, Pitluck S, Liolios K, Pagani I, Ivanova N, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Pan C, Jeffries CD, Detter JC, Brambilla EM, Rohde M, Djao OD, Goker M, Sikorski J, Tindall BJ, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Mavromatis K. 2012. Complete genome sequence of the aquatic bacterium Runella slithyformis type strain (LSU 4(T)). Stand Genomic Sci 6:145-154.
18. Dashtban M, Maki M, Leung KT, Mao C, Qin W. 2010. Cellulase activities in biomass conversion: Measurement methods and comparison. Crit Rev Biotechnol 30:302-309.
19. de Lima Morais DA, Fang H, Rackham OJ, Wilson D, Pethica R, Chothia C, Gough J. 2011. SUPERFAMILY 1.75 including a domain-centric gene ontology method. Nucleic Acids Res 39:D427-D434.
20. Elkins JG, Lochner A, Hamilton-Brehm SD, Davenport KW, Podar M, Brown SD, Land ML, Hauser LJ, Klingeman DM, Raman B, Goodwin LA, Tapia R, Meincke LJ, Detter JC, Bruce DC, Han CS, Palumbo AV, Cottingham RW, Keller M, Graham DE. 2010. Complete genome sequence of the cellulolytic thermophile Caldicellulosiruptor obsidiansis OB47T. J Bacteriol 192:6099-6100.
21. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953-971.
22. Endo K, Hakamada Y, Takizawa S, Kubota H, Sumitomo N, Kobayashi T, Ito S. 2001. A novel alkaline endoglucanase from an alkaliphilic Bacillus isolate: Enzymatic properties, and nucleotide and deduced amino acid sequences. Appl Microbiol Biotechnol 57:109-116.
23. Erdin S, Lisewski AM, Lichtarge O. 2011. Protein function prediction: Towards integration of similarity metrics. Curr Opin Struct Biol 21:180-188.
24. Fox JM, Jess P, Jambusaria RB, Moo GM, Liphardt J, Clark DS, Blanch HW. 2013. A single-molecule analysis reveals morphological targets for cellulase synergy. Nat Chem Biol 9:356-361.
25. Foyle T, Jennings L, Mulcahy P. 2007. Compositional analysis of lignocellulosic materials: Evaluation of methods used for sugar analysis of waste paper and straw. Bioresour Technol 98:3026-3036.
26. Futagami T, Mori K, Yamashita A, Wada S, Kajiwara Y, Takashita H, Omori T, Takegawa K, Tashiro K, Kuhara S, Goto M. 2011. Genome sequence of the white koji mold Aspergillus kawachii IFO 4308, used for brewing the Japanese distilled spirit shochu. Eukaryot Cell 10:1586-1587.
27. Gal L, Pages S, Gaudin C, Belaich A, Reverbel-Leroy C, Tardif C, Belaich JP. 1997. Characterization of the cellulolytic complex (cellulosome) produced by Clostridium cellulolyticum. Appl Environ Microbiol 63:903-909.
28. Gold ND, Martin VJ. 2007. Global view of the Clostridium thermocellum cellulosome revealed by quantitative proteomic analysis. J Bacteriol 189:6787-6795.
29. Guo FB, Xiong L, Teng JL, Yuen KY, Lau SK, Woo PC. 2013. Re-annotation of protein-coding genes in 10 complete genomes of Neisseriaceae family by combining similarity-based and composition-based methods. DNA Res 20:273-286.
30. Hakamada Y, Hatada Y, Koike K, Yoshimatsu T, Kawai S, Kobayashi T, Ito S. 2000. Deduced amino acid sequence and possible catalytic residues of a thermostable, alkaline cellulase from an Alkaliphilic bacillus strain. Biosci Biotechnol Biochem 64:2281-2289.
31. Harris D, DeBolt S. 2010. Synthesis, regulation and utilization of lignocellulosic biomass. Plant Biotechnol J 8:244-262.
32. Harris PV, Welner D, McFarland KC, Re E, Navarro Poulsen JC, Brown K, Salbo R, Ding H, Vlasenko E, Merino S, Xu F, Cherry J, Larsen S, Lo Leggio L. 2010. Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: Structure and function of a large, enigmatic family. Biochemistry 49:3305-3316.
33. Hayashi H, Shibata K, Sakamoto M, Tomita S, Benno Y. 2007. Prevotella copri sp. nov. and Prevotella stercorea sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 57:941-946.
34. Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G. 2010. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908-912.
35. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM. 2011. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463-467.
36. Isanapong J, Goodwin L, Bruce D, Chen A, Detter C, Han J, Han CS, Held B, Huntemann M, Ivanova N, Land ML, Mavromatis K, Nolan M, Pati A, Pennacchio L, Pitluck S, Szeto E, Tapia R, Woyke T, Rodrigues JL. 2012. High-quality draft genome sequence of the Opitutaceae bacterium strain TAV1, a symbiont of the wood-feeding termite Reticulitermes flavipes. J Bacteriol 194:2744-2745.
37. Jager G, Wu Z, Garschhammer K, Engel P, Klement T, Rinaldi R, Spiess AC, Buchs J. 2010. Practical screening of purified cellobiohydrolases and endoglucanases with alpha-cellulose and specification of hydrodynamics. Biotechnol Biofuels 3:18.
38. Jagtap SS, Dhiman SS, Kim TS, Kim IW, Lee JK. 2014. Characterization of a novel endo-beta-1, 4-glucanase from Armillaria gemina and its application in biomass hydrolysis. Appl Microbiol Biotechnol 98:661-669.
39. Kahsay RY, Gao G, Liao L. 2005. An improved hidden Markov model for transmembrane protein detection and topology prediction and its applications to complete genomes. Bioinformatics 21:1853-1858.
40. Koropatkin N, Martens EC, Gordon JI, Smith TJ. 2009. Structure of a SusD homologue, BT1043, involved in mucin O-glycan utilization in a prominent human gut symbiont. Biochemistry 48:1532-1542.
41. Lail K, Sikorski J, Saunders E, Lapidus A, Glavina Del Rio T, Copeland A, Tice H, Cheng JF, Lucas S, Nolan M, Bruce D, Goodwin L, Pitluck S, Ivanova N, Mavromatis K, Ovchinnikova G, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Chain P, Brettin T, Detter JC, Schutze A, Rohde M, Tindall BJ, Goker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Chen F. 2010. Complete genome sequence of Spirosoma linguale type strain (1). Stand Genomic Sci 2:176-185.
42. Lang E, Lapidus A, Chertkov O, Brettin T, Detter JC, Han C, Copeland A, Glavina Del Rio T, Nolan M, Chen F, Lucas S, Tice H, Cheng JF, Land M, Hauser L, Chang YJ, Jeffries CD, Kopitz M, Bruce D, Goodwin L, Pitluck S, Ovchinnikova G, Pati A, Ivanova N, Mavrommatis K, Chen A, Palaniappan K, Chain P, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Goker M, Rohde M, Kyrpides NC, Klenk HP. 2009. Complete genome sequence of Dyadobacter fermentans type strain (NS114). Stand Genomic Sci 1:133-140.
43. Larkin JM, Williams PM. 1978. Runella slithyformis gen. nov., sp. nov., a curved, nonflexible, pink bacterium. Int J Syst Evol Microbiol 28:32-36.
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. Lee M, Woo SG, Park J, Yoo SA. 2010. Dyadobacter soli sp. nov., a starch-degrading bacterium isolated from farm soil. Int J Syst Evol Microbiol 60:2577-2582.
46. Le Crom S, Schackwitz W, Pennacchio L, Magnuson JK, Culley DE, Collett JR, Martin J, Druzhinina IS, Mathis H, Monot F, Seiboth B, Cherry B, Rey M, Berka R, Kubicek CP, Baker SE, Margeot A. 2009. Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing. Proc Natl Acad Sci 106:16151-16156.
47. Lee SJ, Lee KS, Kim SR, Gui ZZ, Kim YS, Yoon HJ, Kim I, Kang PD, Sohn HD, Jin BR. 2005. A novel cellulase gene from the mulberry longicorn beetle, Apriona germari: Gene structure, expression, and enzymatic activity. Comp Biochem Physiol B Biochem Mol Biol 140:551-560.
48. Madera M, Gough J. 2002. A comparison of profile hidden Markov model procedures for remote homology detection. Nucleic Acids Res 30:4321-4328.
49. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH. 2013. CDD: Conserved domains and protein three-dimensional structure. Nucleic Acids Res 41:D348-D352.
50. Marjamaa K, Toth K, Bromann PA, Szakacs G, Kruus K. 2013. Novel Penicillium cellulases for total hydrolysis of lignocellulosics. Enzyme Microb Technol 52:358-369.
51. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Anderson I, Lykidis A, Mavromatis K, Ivanova NN, Kyrpides NC. 2010. The integrated microbial genomes system: An expanding comparative analysis resource. Nucleic Acids Res 38:D382-D390.
52. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC. 2012. IMG: The Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 40:D115-D122.
53. Matsushika A, Inoue H, Kodaki T, Sawayama S. 2009. Ethanol production from xylose in engineered Saccharomyces cerevisiae strains: Current state and perspectives. Appl Microbiol Biotechnol 84:37-53.
54. Mavromatis K, Chu K, Ivanova N, Hooper SD, Markowitz VM, Kyrpides NC. 2009. Gene context analysis in the Integrated Microbial Genomes (IMG) data management system. PLoS ONE 4:e7979.
55. Mirande C, Mosoni P, Bera-Maillet C, Bernalier-Donadille A, Forano E. 2010. Characterization of Xyn10A, a highly active xylanase from the human gut bacterium Bacteroides xylanisolvens XB1A. Appl Microbiol Biotechnol 87:2097-2105.
56. Nakamura T, Mine S, Hagihara Y, Ishikawa K, Ikegami T, Uegaki K. 2008. Tertiary structure and carbohydrate recognition by the chitin-binding domain of a hyperthermophilic chitinase from Pyrococcus furiosus. J Mol Biol 381:670-680.
57. Park J, Karplus K, Barrett C, Hughey R, Haussler D, Hubbard T, Chothia C. 1998. Sequence comparisons using multiple sequences detect three times as many remote homologues as pairwise methods. J Mol Biol 284:1201-1210.
58. Pauly M, Keegstra K. 2008. Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J 54:559-568.
59. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JA, van den Berg M, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EG, Debets AJ, Dekker P, van Dijck PW, van Dijk A, Dijkhuizen L, Driessen AJ, d'Enfert C, Geysens S, Goosen C, Groot GS, de Groot PW, Guillemette T, Henrissat B, Herweijer M, van den Hombergh JP, van den Hondel CA, van der Heijden RT, van der Kaaij RM, Klis FM, Kools HJ, Kubicek CP, van Kuyk PA, Lauber J, Lu X, van der Maarel MJ, Meulenberg R, Menke H, Mortimer MA, Nielsen J, Oliver SG, Olsthoorn M, Pal K, van Peij NN, Ram AF, Rinas U, Roubos JA, Sagt CM, Schmoll M, Sun J, Ussery D, Varga J, Vervecken W, van de Vondervoort PJ, Wedler H, Wosten HA, Zeng AP, van Ooyen AJ, Visser J, Stam H. 2007. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25:221-231.
60. Posta K, Beki E, Wilson DB, Kukolya J, Hornok L. 2004. Cloning, characterization and phylogenetic relationships of cel5B, a new endoglucanase encoding gene from Thermobifida fusca. J Basic Microbiol 44:383-399.
61. 2+-ATPase-mediated carbonate dissolution among cyanobacterial euendoliths. Appl Environ Microb 78:7-13.
62. Rebuffet E, Groisillier A, Thompson A, Jeudy A, Barbeyron T, Czjzek M, Michel G. 2011. Discovery and structural characterization of a novel glycosidase family of marine origin. Environ Microbiol 13:1253-1270.
63. Robert C, Chassard C, Lawson PA, Bernalier-Donadille A. 2007. Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community. Int J Syst Evol Microbiol 57:1516-1520.
64. Rubin EM. 2008. Genomics of cellulosic biofuels. Nature 454:841-845.
65. Sabathe F, Belaich A, Soucaille P. 2002. Characterization of the cellulolytic complex (cellulosome) of Clostridium acetobutylicum. FEMS Microbiol Lett 217:15-22.
66. Sakamoto M, Kitahara M, Benno Y. 2007. Parabacteroides johnsonii sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 57:293-296.
67. Salgado H, Moreno-Hagelsieb G, Smith TF, Collado-Vides J. 2000. Operons in Escherichia coli: Genomic analyses and predictions. P Natl Acad Sci USA 97:6652-6657.
68. Simpson PJ, Xie H, Bolam DN, Gilbert HJ, Williamson MP. 2000. The structural basis for the ligand specificity of family 2 carbohydrate-binding modules. J Biol Chem 275:41137-41142.
69. Sonnhammer EL, Eddy SR, Birney E, Bateman A, Durbin R. 1998. Pfam: Multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res 26:320-322.
70. Sonnhammer EL, Eddy SR, Durbin R. 1997. Pfam: A comprehensive database of protein domain families based on seed alignments. Proteins 28:405-420.
71. Tamaru Y, Miyake H, Kuroda K, Nakanishi A, Kawade Y, Yamamoto K, Uemura M, Fujita Y, Doi RH, Ueda M. 2010. Genome sequence of the cellulosome-producing mesophilic organism Clostridium cellulovorans 743B. J Bacteriol 192:901-902.
72. Tatusov RL, Koonin EV, Lipman DJ. 1997. A genomic perspective on protein families. Science 278:631-637.
73. Ten LN, Xu JL, Jin FX, Im WT, Oh HM, Lee ST. 2009. Spirosoma panaciterrae sp. nov., isolated from soil. Int J Syst Evol Microbiol 59:331-335.
74. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G. 2011. Environmental and gut Bacteroidetes: The food connection. Front Microbiol 2:93.
75. Tsuji A, Sato S, Kondo A, Tominaga K, Yuasa K. 2012. Purification and characterization of cellulase from North Pacific krill (Euphausia pacifica). Analysis of cleavage specificity of the enzyme. Comp Biochem Phys B 163:324-333.
76. Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sorlie M, Eijsink VG. 2010. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219-222.
77. Vapnik VN. 1999. An overview of statistical learning theory. IEEE Trans Neural Netw 10:988-999.
78. Wang Y, Xue Z, Shen G, Xu J. 2008. PRINTR: Prediction of RNA binding sites in proteins using SVM and profiles. Amino Acids 35:295-302.
79. Weon HY, Kim BY, Kwon SW, Park IC, Cha IB, Tindall BJ, Stackebrandt E, Truper HG, Go SJ. 2005. Leadbetterella byssophila gen. nov., sp. nov., isolated from cotton-waste composts for the cultivation of oyster mushroom. Int J Syst Evol Microbiol 55:2297-2302.
80. Weon HY, Kim BY, Yoo SH, Lee SY, Kwon SW, Go SJ, Stackebrandt E. 2006. Niastella koreensis gen. nov., sp. nov. and Niastella yeongjuensis sp. nov., novel members of the phylum Bacteroidetes, isolated from soil cultivated with Korean ginseng. Int J Syst Evol Microbiol 56:1777-1782.
81. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D'Haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng JF, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk HP, Eisen JA. 2009. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056-1060.
82. Wu I, Arnold FH. 2013. Engineered thermostable fungal Cel6A and Cel7A cellobiohydrolases hydrolyze cellulose efficiently at elevated temperatures. Biotechnol Bioeng 110:1874-1883.
83. Xia D, Wei Y, Zhang G, Zhao Q, Zhang Y, Xiang Z, Lu C. 2013. cDNA cloning, expression, and enzymatic activity of a novel endogenous cellulase from the beetle Batocera horsfieldi. Gene 514:62-68.
84. Xie CH, Yokota A. 2006. Reclassification of [Flavobacterium] ferrugineum as Terrimonas ferruginea gen. nov., comb. nov., and description of Terrimonas lutea sp. nov., isolated from soil. Int J Syst Evol Microbiol 56:1117-1121.
85. Xie F, Cheng G, Xu H, Wang Z, Lei L, Li Y. 2011. Identification of a novel gene for biosynthesis of a bacteroid-specific electron carrier menaquinone. PLoS ONE 6:e28995.
86. Xie G, Bruce DC, Challacombe JF, Chertkov O, Detter JC, Gilna P, Han CS, Lucas S, Misra M, Myers GL, Richardson P, Tapia R, Thayer N, Thompson LS, Brettin TS, Henrissat B, Wilson DB, McBride MJ. 2007. Genome sequence of the cellulolytic gliding bacterium Cytophaga hutchinsonii. Appl Environ Microbiol 73:3536-3546.
87. Zhang PYH, Himmel ME, Mielenz JR. 2006. Outlook for cellulase improvement: Screening and selection strategies. Biotechnol Adv 24:452-481.
88. Zhang YH, Hong J, Ye X. 2009. Cellulase assays. Methods Mol Biol 581:213-231.
89. Zinzen RP, Girardot C, Gagneur J, Braun M, Furlong EEM. 2009. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 462:U65-U72.