The cellulosomes: Multienzyme machines for degradation of plant cell wall polysaccharides

Annual Review of Microbiology

Volumn 58, Issue , 2004, Pages 521-554

  Bayer, Edward A ^a   Belaich, Jean Pierre ^b,c   Shoham, Yuval ^d   Lamed, Raphael ^e  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e TEL AVIV UNIVERSITY   (Israel)

Author keywords

Cellulases; Cohesin dockerin interaction; Hemicellulases; Multiprotein complexes; Protein protein interactions; Scaffoldin

Indexed keywords

AMINO ACID; CELLULOSE; CELLULOSOME; COHESIN; DIMER; DOCKERIN; HEMICELLULOSE; HETERODIMER; MULTIENZYME COMPLEX; POLYSACCHARIDE; SCAFFOLDIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

BACTERIUM; BINDING AFFINITY; CARBOHYDRATE METABOLISM; CELL WALL; CELLULOLYTIC BACTERIA; CELLULOSOMAL GENE; CELLULOSOME RELATED GENE; CIPA GENE; CLOSTRIDIUM CELLULOLYTICUM; CLOSTRIDIUM CELLULOVORANS; CLOSTRIDIUM JOSUI; CLUSTER ANALYSIS; CRYSTAL STRUCTURE; DOCKERIN DOMAIN; ENZYME SPECIFICITY; GENE CLUSTER; GENE CONTROL; GENOME; HYDROLYSIS; NONHUMAN; PHYLOGENY; PLANT CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REVIEW; SUPRAMOLECULAR CHEMISTRY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL WALL; CELLULOSOMES; CHROMOSOMAL PROTEINS, NON-HISTONE; CLOSTRIDIUM CELLULOLYTICUM; CLOSTRIDIUM CELLULOVORANS; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PLANTS; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM CELLULOLYTICUM; CLOSTRIDIUM CELLULOVORANS; CLOSTRIDIUM JOSUI; POSIBACTERIA;

EID: 4143139469     PISSN: 00664227     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.micro.57.030502.091022     Document Type: Review

References (150)

1. Ahsan MM, Kimura T, Karita S, Sakka K, Ohmiya K. 1996. Cloning, DNA sequencing, and expression of the gene encoding Clostridium thermocellum cellulase CelJ, the largest catalytic component of the cellulosome. J. Bacteriol. 178:5732-40
2. Ahsan MM, Matsumoto M, Karita S, Kimura T, Sakka K, Ohmiya K. 1997. Purification and characterization of the family J catalytic domain derived from the Clostridium thermocellum endoglucanase CelJ. Biosci. Biotechnol. Biochem. 61:427-31
3. a. Aubert J-P, Béguin P, Millet J, eds. 1988. Biochemistry and Genetics of Cellulose Degradation. London: Academic. 428 pp.
4. Bagnara-Tardif C, Gaudin C, Belaich A, Hoest P, Citard T, Belaich J-P. 1992. Sequence analysis of a gene cluster encoding cellulases from Clostridium cellulolyticum. Gene 119:17-28
5. Bayer EA, Chanzy H, Lamed R, Shoham Y. 1998. Cellulose, cellulases and cellulosomes. Curr. Opin. Struct. Biol. 8:548-57
6. Bayer EA, Coutinho PM, Henrissat B. 1999. Cellulosome-like sequences in Archaeoglobus fulgidus: an enigmatic vestige of cohesin and dockerin domains. FEBS Lett. 463:277-80
7. Bayer EA, Ding S-Y, Mechaly A, Shoham Y, Lamed R. 1999. Emerging phylogenetics of cellulosome structure. See Ref. 59a, pp. 189-201
8. Bayer EA, Ding S-Y, Shoham Y, Lamed R. 1999. New perspectives in the structure of cellulosome-related domains from different species. See Ref. 105a, pp. 428-36
9. Bayer EA, Kenig R, Lamed R. 1983. Adherence of Clostridium thermocellum to cellulose. J. Bacteriol. 156:818-27
10. Bayer EA, Morag E, Lamed R. 1994. The cellulosome: a treasure-trove for biotechnology. Trends Biotechnol. 12:378-86
11. Bayer EA, Morag E, Lamed R, Yaron S, Shoham Y. 1998. Cellulosome structure: four-pronged attack using biochemistry, molecular biology, crystallography and bioinformatics. In Carbohydrases from Trichoderma reesei and Other Microorganisms, ed. M Claeyssens, W Nerinckx, K Piens, pp. 39-65. London: R. Soc. Chem.
12. Bayer EA, Morag E, Shoham Y, Tormo J, Lamed R. 1996. The cellulosome: a cell-surface organelle for the adhesion to and degradation of cellulose. In Bacterial Adhesion: Molecular and Ecological Diversity, ed. M Reicher, pp. 155-82. New York: Wiley-Liss
13. Bayer EA, Nakar D, Handelsman T, Mechaly A, Fierobe H-P, et al. 2004. Probing the cohesin-dockerin interaction by rational mutagenesis. See Ref. 105b, pp. 155-66
14. Bayer EA, Setter E, Lamed R. 1985. Organization and distribution of the cellulosome in Clostridium thermocellum. J. Bacteriol. 163:552-59
15. Bayer EA, Shimon LJW, Lamed R, Shoham Y. 1998. Cellulosomes: structure and ultrastructure. J. Struct. Biol. 124:221-34
16. Bayer EA, Shoham Y, Lamed R. 2000. Cellulose-decomposing prokaryotes and their enzyme systems. In The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, ed. M Dworkin, S Falkow, E Rosenberg, K-H Schleifer, E Stackebrandt. New York: Springer-Verlag. 3rd ed. http://link.springer.de/link/service/books/10125/index.htm
17. Bayer EA, Shoham Y, Lamed R. 2000. The cellulosome: an exocellular organelle for degrading plant cell wall polysaccharides. In Glycomicrobiology, ed. RJ Doyle, pp. 387-439. New York: Kluwer/Plenum
18. Béguin P. 1990. Molecular biology of cellulose degradation. Annu. Rev. Microbiol. 44:219-48
19. Béguin P, Alzari PM. 1998. The cellulosome of Clostridium thermocellum. Biochem. Soc. Trans. 26:178-85
20. Béguin P, Aubert J-P. 1994. The biological degradation of cellulose. FEMS Microbiol. Lett. 13:25-58
21. Béguin P, Chauvaux S, Guglielmi G, Matuschek M, Leibovitz E, et al. 1999. The Clostridium thermocellum cellulosome: organization and mode of attachment to the cell. See Ref. 105a, pp. 437-43
22. Béguin P, Lemaire M. 1996. The cellulosome: an exocellular, multiprotein complex specialized in cellulose degradation. Crit. Rev. Biochem. Mol. Biol. 31:201-36
23. Béguin P, Millet J, Aubert J-P. 1992. Cellulose degradation by Clostridium thermocellum: from manure to molecular biology. FEMS Microbiol. Lett. 100:523-28
24. Beguin P, Millet J, Chauvaux S, Salamitou S, Tokatlidis K, et al. 1992. Bacterial cellulases. Biochem. Soc. Trans. 20:42-46
25. Béguin P, Millet J, Grépinet O, Navarre A, Juy M, et al. 1988. The cel (cellulose degradation) genes of Clostridium thermocellum. See Ref. 2a, pp. 267-82
26. Belaich J-P, Belaich A, Fierobe H-P, Gal L, Gaudin C, et al. 1999. The cellulolytic system of Clostridium cellulolyticum. See Ref. 105a, pp. 479-87
27. Belaich J-P, Tardif C, Belaich A, Gaudin C. 1997. The cellulolytic system of Clostridium cellulolyticum. J. Biotechnol. 57:3-14
28. Bhat KM, Goodenough PW, Owen E, Wood TM. 1993. Cellobiose: a true inducer of cellulosome in different strains of Clostridium thermocellum. FEMS Microbiol. Lett. 111:73-78
29. Bhat S, Hutson RA, Owen E, Bhat MK. 1997. Determination of immunological homology between cellulosome subunits and cloned endoglucanases and xylanases of Clostridium thermocellum. Anaerobe 3:347-52
30. Bhat S, Kennedy JF, Goodenough PW, Owen E, Bhat MK. 1997. Effect of D-glucono-1,4-lactone on the production of CMCase, pNPCase and true cellulase by Clostridium thermocellum. Carbohydr. Polym. 34:95-99
31. Blum DL, Kataeva IA, Li XL, Ljungdahl LG. 2000. Feruloyl esterase activity of the Clostridium thermocellum cellulosome can be attributed to previously unknown domains of XynY and XynZ. J. Bacteriol. 182:1346-51
32. Boraston AB, McLean BW, Kormos JM, Alam M, Gilkes NR, et al. 1999. Carbohydrate-binding modules: diversity of structure and function. See Ref. 59a, pp. 202-11
33. Carvalho AL, Dias FM, Prates JA, Nagy T, Gilbert HJ, et al. 2003. Cellulosome assembly revealed by the crystal structure of the cohesin-dockerin complex. Proc. Natl. Acad. Sci. USA 100:13809-14
34. Chauvaux S, Béguin P, Aubert J-P, Bhat KM, Gow LA, et al. 1990. Calcium-binding affinity and calcium-enhanced activity of Clostridium thermocellum endoglucanase D. Biochem. J. 265:261-65
35. Choi SK, Ljungdahl LG. 1996. Structural role of calcium for the organization of the cellulosome of Clostridium thermocellum. Biochemistry 35:4906-10
36. Ciruela A, Gilbert HJ, Ali BRS, Hazlewood GP. 1998. Synergistic interaction of the cellulosome integrating protein (CipA) from Clostridium thermocellum with a cellulosomal endoglucanase. FEBS Lett. 422:221-24
37. Coutinho PM, Henrissat B. 1999. Carbohydrate-active enzymes: an integrated database approach. See Ref. 59a, pp. 3-12
38. Coutinho PM, Henrissat B. 1999. The modular structure of cellulases and other carbohydrate-active enzymes: an integrated database approach. See Ref. 105a, pp. 15-23
39. Davies G, Henrissat B. 1995. Structures and mechanisms of glycosyl hydrolases. Structure 3:853-59
40. Devillard E, Goodheart DE, Karnati SK, Bayer EA, Lamed R, et al. 2004. Ruminococcus albus 8 mutants defective in cellulose degradation are deficient in two processive endocellulases, Cel48A and Cel9B, both of which possess a novel modular architecture. J. Bacteriol. 186:136-45
41. Ding S-Y, Bayer EA, Steiner D, Shoham Y, Lamed R. 1999. A novel cellulosomal scaffoldin from Acetivibrio cellulolyticus that contains a family-9 glycosyl hydrolase. J. Bacteriol. 181:6720-29
42. Ding S-Y, Bayer EA, Steiner D, Shoham Y, Lamed R. 2000. A scaffoldin of the Bacteroides cellulosolvens cellulosome that contains 11 type II cohesins. J. Bacteriol. 182:4915-25
43. Ding S-Y, Lamed R, Bayer EA, Himmel ME. 2003. The bacterial scaffoldin: structure, function and potential applications in nanoscience. In Genetic Engineering: Principles and Methods, ed. JK Setlow, 25:209-26. New York: Kluwer Acad.
44. Ding S-Y, Rincon MT, Lamed R, Martin JC, McCrae SI, et al. 2001. Cellulosomal scaffoldin-like proteins from Ruminococcusflavefaciens. J. Bacteriol. 183:1945-53
45. Doi RH, Goldstein M, Hashida S, Park JS, Takagi M. 1994. The Clostridium cellulovorans cellulosome. Crit. Rev. Microbiol. 20:87-93
46. Doi RH, Kosugi A, Murasnima K, Tamaru Y, Han SO. 2003. Cellulosomes from mesophilic bacteria. J. Bacteriol. 185:5907-14
47. Doi RH, Park JS, Liu CC, Malburg LM, Tamaru Y, et al. 1998. Cellulosome and noncellulosomal cellulases of Clostridium cellulovorans. Extremophiles 2:53-60
48. Doi RH, Tamura Y. 2001. The Clostridium cellulovorans cellulosome: an enzyme complex with plant cell wall degrading activity. Chem. Rec. 1:24-32
49. Dror TW, Morag E, Rolider A, Bayer EA, Lamed R, Shoham Y. 2003. Regulation of the cellulosomal celS (cel4SA) gene of Clostridium thermocellum is growth-rate dependent. J. Bacteriol. 185:3042-48
50. Dror TW, Rolider A, Bayer EA, Lamed R, Shoham Y. 2003. Regulation of expression of scaffoldin-related genes in Clostridium thermocellum. J. Bacteriol. 185:5109-16
51. Felix CR, Ljungdahl LG. 1993. The cellulosome: the exocellular organelle of Clostridium. Annu. Rev. Microbiol. 47:791-819
52. Fernandes AC, Fontes CM, Gilbert HJ, Hazlewood GP, Fernandes TH, Ferreira LMA. 1999. Homologous xylanases from Clostridium thermocellum: evidence for bi-functional activity, synergism between xylanase catalytic modules and the presence of xylan-binding domains in enzyme complexes. Biochem. J. 342:105-10
53. Fierobe H-P, Bayer EA, Tardif C, Czyzek M, Mechaly A, et al. 2002. Degradation of cellulose substrates by cellulosome chimeras: substrate targeting versus proximity of enzyme components. J. Biol. Chem. 277:49621-30
54. Fierobe H-P, Mechaly A, Tardif C, Belaich A, Lamed R, et al. 2001. Design and production of active cellulosome chimeras: selective incorporation of dockerin-containing enzymes into defined functional complexes. J. Bacteriol. 276:21257-61
55. Fierobe H-P, Mechaly A, Tardif C, Belaich A, Lamed R, et al. 2002. Designer nanosomes: selective engineering of dockerin-containing enzymes into chimeric scaffoldins to form defined nanoreactors. In Carbohydrate Bioengineering: Interdisciplinary Approaches, ed. TT Teeri, B Svensson, HJ Gilbert, T Feizi, pp. 113-23. Cambridge, UK: R. Soc. Chem.
56. Fierobe H-P, Pagès S, Belaich A, Champ S, Lexa D, Belaich J-P. 1999. Cellulosome from Clostridium cellulolyticum: molecular study of the dockerin/cohesin interaction. Biochemistry 38:12822-32
57. Fraser CM, Eisen JA, Nelson KE, Paulsen IT, Salzberg SL. 2002. The value of complete microbial genome sequencing (you get what you pay for). J. Bacteriol. 184:6403-5
58. Fujino T, Béguin P, Aubert J-P. 1993. Organization of a Clostridium thermocellum gene cluster encoding the cellulosomal scaffolding protein CipA and a protein possibly involved in attachment of the cellulosome to the cell surface. J. Bacteriol. 175:1891-99
59. Gal L, Gaudin C, Belaich A, Pagès S, Tardif C, Belaich J-P. 1997. CelG from Clostridium cellulolyticum: a multidomain endoglucanase acting efficiently on crystalline cellulose. J. Bacteriol. 179:6595-601
60. L-protein reveals an unusual degree of internal homology. Mol. Microbiol. 8:325-34
61. a. Gilbert HJ, Davies GJ, Henrissat B, Svensson B, eds. 1999. Recent Advances in Carbohydrate Bioengineering. Cambridge, UK: R. Soc. Chem.
62. Guglielmi G, Béguin P. 1998. Cellulase and hemicellulase genes of Clostridium thermocellum from five independent collections contain few overlaps and are widely scattered across the chromosome. FEMS Microbiol. Lett. 161:209-15
63. Han SO, Yukawa H, Inui M, Doi RH. 2003. Transcription of Clostridium cellulovorans cellulosomal cellulase and hemicellulase genes. J. Bacteriol. 185:2520-27
64. ed. B Sahah, K Hayashi. Washington, DC: Am. Chem. Soc. In press. Handelsman T, Mechaly A, Barak Y, Nakar D, Lamed R, et al. 2004. Effect of rational mutagenesis of selected cohesin residues on the high-affinity cohesin-dockerin interaction. In Lignocellulose Biodegradation, ed. B Sahah, K Hayashi. Washington, DC: Am. Chem. Soc. In press
65. Hayashi H, Takehara M, Hattori T, Kimura T, Karita S, et al. 1999. Nucleotide sequences of two contiguous and highly homologous xylanase genes xynA and xynB and characterization of XynA from Clostridium thermocellum. Appl. Microbiol. Biotechnol. 51:348-57
66. Hazlewood GP, Romaniec MPM, Davidson K, Grépinet O, Béguin P, et al. 1988. A catalogue of Clostridium thermocellum endoglucanase, β-glucosidase and xylanase genes cloned in Escherichia coli. FEMS Microbiol. Lett. 51:231-36
67. Irwin D, Shin D-H, Zhang S, Barr BK, Sakon J, et al. 1998. Roles of the catalytic domain and two cellulose binding domains of Thermomonospora fusca E4 in cellulose hydrolysis. J. Bacteriol. 180:1709-14
68. Jennert KCB,Tardif C, Young DI, Young M. 2000. Gene transfer to Clostridium cellulolyticum ATCC 35319. Microbiology 146:3071-80
69. Jindou S, Souda A, Karita S, Kajino T, Beguin P, et al. 2004. Cohesin/ dockerin interactions within and between Clostridium josui and Clostridium thermocellum: binding selectivity between cognate dockerin and cohesin domains and species specificity. J. Biol. Chem. 279:9867-74
70. Johnson EA, Bouchot F, Demain AL. 1985. Regulation of cellulase formation in Clostridium thermocellum. J. Gen. Microbiol. 131:223-32
71. Kakiuchi M, Isui A, Suzuki K, Fujino T, Fujino E, et al. 1998. Cloning and DNA sequencing of the genes encoding Clostridium josui scaffolding protein CipA and cellulase CelD and identification of their gene products as major components of the cellulosome. J. Bacteriol. 180:4303-8
72. Karita S, Kimura T, Sakka K, Ohmiya K. 1997. Purification of the Ruminococcus albus endoglucanase IV using a cellulose-binding domain as an affinity tag. J. Ferment. Bioeng. 84:354-57
73. Kataeva I, Guglielmi G, Béguin P. 1997. Interaction between Clostridium thermocellum endoglucanase CelD and polypeptides derived from the cellulosome-integrating protein CipA: stoichiometry and cellulolytic activity of the complexes. Biochem. J. 326:617-24
74. Kataeva IA, Seidel RD III, Shah A, West LT, Li X-L, Ljungdahl LG. 2002. The fibronectin type 3-like repeat from the Clostridium thermocellum cellobio-hydrolase CbhA promotes hydrolysis of cellulose by modifying its surface. Appl. Environ. Microbiol. 68:4292-300
75. Kosugi A, Murashima K, Doi RH. 2001. Characterization of xylanolytic enzymes in Clostridium cellulovorans: expression of xylanase activity dependent on growth substrates. J. Bacteriol. 183:7037-43
76. Kosugi A, Murashima K, Tamaru Y, Doi RH. 2002. Cell-surface-anchoring role of N-terminal surface layer homology domains of Clostridium cellulovorans EngE. J. Bacteriol. 184:884-88
77. Krispin O, Allmansberger R. 1998. The Bacillus subtilis AraE protein displays a broad substrate specificity for several substrates. J. Bacteriol. 180:3250-52
78. Lamed R, Bayer EA. 1988. The cellulosome concept: exocellular/ extracellular enzyme reactor centers for efficient binding and cellulolysis. See Ref. 2a, pp. 101-16
79. Lamed R, Bayer EA. 1988. The cellulosome of Clostridium thermocellum. Adv. Appl. Microbiol. 33:1-46
80. Lamed R, Bayer EA. 1993. The cellulosome concept - a decade later! See Ref. 121a, pp. 1-12
81. Lamed R, Kenig R, Setter E, Bayer EA. 1985. Major characteristics of the cellulolytic system of Clostridium thermocellum coincide with those of the purified cellulosome. Enzyme Microb. Technol. 7:37-41
82. Lamed R, Setter E, Bayer EA. 1983. Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum. J. Bacteriol. 156:828-36
83. Lamed R, Setter E, Kenig R, Bayer EA. 1983. The cellulosome: a discrete cell surface organelle of Clostridium thermocellum which exhibits separate antigenic, cellulose-binding and various cellulolytic activities. Biotechnol. Bioeng. Symp. 13:163-81
84. Lehtio J, Sugiyama J, Gustavsson M, Fransson L, Linder M, Teeri TT. 2003. The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules. Proc. Natl. Acad. Sci. USA 100:484-89
85. Leibovitz E, Béguin P. 1996. A new type of cohesin domain that specifically binds the dockerin domain of the Clostridium thermocellum cellulosome-integrating protein CipA. J. Bacteriol. 178:3077-84
86. Leibovitz E, Béguin P. 1998. Comparison of two scaffolding polypeptides for the integration of different proteins in synthetic complexes derived from the Clostridium thermocellum cellulosome. Enzyme Microb. Technol. 22:588-93
87. Lemaire M, Ohayon H, Gounon P, Fujino T, Béguin P. 1995. OlpB, a new outer layer protein of Clostridium thermocellum, and binding of its S-layer-like domains to components of the cell envelope. J. Bacteriol. 177:2451-59
88. Lytle B, Wu JHD. 1998. Involvement of both dockerin subdomains in assembly of the Clostridium thermocellum cellulosome. J. Bacteriol. 180:6581-85
89. Lytle BL, Volkman BF, Westler WM, Heckman MP, Wu JHD. 2001. Solution structure of a type 1 dockerin domain, a novel prokaryotic, extracellular calcium-binding domain. J. Mol. Biol. 307:745-53
90. Maamar H, de Philip P, Belaich JP, Tardif C. 2003. ISCce1 and ISCce2, two novel insertion sequences in Clostridium cellulolyticum. J. Bacteriol. 185:714-25
91. Mechaly A, Fierobe H-P, Belaich A, Belaich J-P, Lamed R, et al. 2001. Cohesin-dockerin interaction in cellulosome assembly: A single hydroxyl group of a dockerin domain distinguishes between non-recognition and high-affinity recognition. J. Biol. Chem. 276:9883-88
92. Mechaly A, Yaron S, Lamed R, Fierobe H-P, Belaich A, et al. 2000. Cohesin-dockerin recognition in cellulosome assembly: experiment versus hypothesis. Proteins 39:170-77
93. Millet J, Petre D, Béguin P, Raynaud O, Aubert J-P. 1985. Cloning of ten distinct DNA fragments of Clostridium thermocellum coding for cellulases. FEBS Lett. 29:145-49
94. Miras I, Schaeffer F, Béguin P, Alzari PM. 2002. Mapping by site-directed mutagenesis of the region responsible for cohesin-dockerin interaction on the surface of the seventh cohesin domain of Clostridium thermocellum CipA. Biochemistry 41:2115-19
95. Mishra S, Béguin P, Aubert J. 1991. Transcription of Clostridium thermocellum endoglucanase genes celF and celD. J. Bacteriol. 173:80-85
96. Mohand-Oussaid O, Payot S, Guedon E, Gelhaye E, Youyou A, Petitdemange H. 1999. The extracellular xylan degradative system in Clostridium cellulolyticum cultivated on xylan: evidence for cell-free cellulosome production. J. Bacteriol. 181:4035-40
97. Morag E, Bayer EA, Lamed R. 1990. Relationship of cellulosomal and noncellulosomal xylanases of Clostridium thermocellum to cellulose-degrading enzymes. J. Bacteriol. 172:6098-105
98. Morris DD, Gibbs MD, Ford M, Thomas J, Bergquist PL. 1999. Family 10 and 11 xylanase genes from Caldicellulosiruptor sp. strain Rt69B.1. Extremophiles 3:103-11
99. Morrison M, Miron J. 2000. Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and Pil-proteins? FEMS Microbiol. Lett. 185:109-15
100. Mosbah A, Belaich A, Bornet O, Belaich JP, Henrissat B, Darbon H. 2000. Solution structure of the module X2 1 of unknown function of the cellulosomal scaffolding protein CipC of Clostridium cellulolyticum. J. Mol. Biol. 304:201-17
101. Murashima K, Chen CL, Kosugi A, Tamaru Y, Doi RH, Wong SL. 2002. Heterologous production of Clostridium cellulovorans engB, using protease-deficient Bacillus subtilis, and preparation of active recombinant cellulosomes. J. Bacteriol. 184:76-81
102. Murashima K, Kosugi A, Doi RH. 2002. Determination of subunit composition of Clostndium cellulovorans cellulosomes that degrade plant cell walls. Appl. Environ. Microbiol. 68:1610-15
103. Murashima K, Kosugi A, Doi RH. 2003. Synergistic effects of cellulosomal xylanase and cellulases from Clostridium cellulovorans on plant cell wall degradation. J. Bacteriol. 185:1518-24
104. Murashima K, Kosugi A, Doi RH. 2003. Synergistic effects on crystalline cellulose degradation between cellulosomal cellulases from Clostridium cellulovorans. J. Bacteriol. 184:5088-95
105. Noach I, Lamed R, Xu Q, Kenig R, Bayer EA, Frolow F. 2003. Preliminary X-ray characterization and phasing of a type II cohesin domain from the cellulosome of Acetivibrio cellulolyticus. Acta Crystallogr. D D59:1610-13
106. Moiling J, Breton G, Omelchenko MV, Makarova KS, Zeng Q, et al. 2001. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183:4823-38
107. Ohara H, Noguchi J, Karita S, Kimura T, Sakka K, Ohmiya K. 2000. Sequence of egV and properties of EgV, a Ruminococcus albus endoglucanase containing a dockerin domain. Biosci. Biotechnol. Biochem. 64:80-88
108. a. Ohmiya K, Hayashi K, Sakka K, Kobayashi Y, Karita S, Kimura T, eds. 1999. Genetics, Biochemistry and Ecology of Cellulose Degradation. Tokyo: Uni Publ.
109. b. Ohmiya K, Sakka K, Karita S, Kimura T, Sakka M, Onishi Y, eds. 2004. Genetics, Biotechnology of Lignocellulose Degradation and Biomass Utilization. Tokyo: Uni Publ.
110. Ohmiya K, Sakka K, Karita S, Kimura T. 1997. Structure of cellulases and their applications. Biotechnol. Genet. Eng. Rev. 14:365-414
111. Pagès S, Belaich A, Belaich J-P, Morag E, Lamed R, et al. 1997. Species-specificity of the cohesin-dockerin interaction between Clostridium thermocellum and Clostridium cellulolyticum: prediction of specificity determinants of the dockerin domain. Proteins 29:517-27
112. Pagès S, Belaich A, Fierobe H-P, Tardif C, Gaudin C, Belaich J-P. 1999. Sequence analysis of scaffolding protein CipC and ORFXp, a new cohesin-containing protein in Clostridium cellulolyticum: comparison of various cohesin domains and subcellular localization of ORFXp. J. Bacteriol. 181:1801-10
113. Pages S, Valette O, Abdou L, Belaich A, Belaich J-P. 2003. A rhamnogalacturonan lyase in the Clostridium cellulolyticum cellulosome. J. Bacteriol. 185:4727-33
114. Perret S, Maamar H, Belaich J-P, Tardif C. 2004. Use of antisense RNA to modify the composition of cellulosomes produced by Clostridium cellulolyticum. Mol. Microbiol. 51:599-607
115. Rincon MT, Ding S-Y, Martin JC, McCrae SI, Aurilia V, et al. 2004. Protein: protein interactions involved in the assembly of lignocellulolytic enzyme complexes in Ruminococcus flavefaciens. See Ref. 105b, pp. 241-48
116. Rincon MT, Ding S-Y, McCrae SI, Martin JC, Aurilia V, et al. 2003. Novel organization and divergent dockerin specificities in the cellulosome system of Ruminococcus flavefaciens. J. Bacteriol. 185:703-13
117. Rincon MT, McCrae SI, Kirby J, Scott KP, Flint HJ. 2001. EndB, a multidomain family 44 cellulase from Ruminococcus flavefaciens 17, binds to cellulose via a novel cellulose-binding module and to another R. flavefaciens protein via a dockerin domain. Appl. Environ. Microbiol. 67:4426-31
118. Sabathe F, Belaich A, Soucaille P. 2002. Characterization of the cellulolytic complex (cellulosome) of Clostridium acetobutylicum. FEMS Microbiol. Lett. 217:15-22
119. Sakka K, Hayashi H, Ahsan MM, Kimura T, Karita S, Ohmiya K. 1999. Xylanase activities associated with the Clostridium thermocellum cellulosome. See Ref. 105a, pp. 461-67
120. Sakon J, Irwin D, Wilson DB, Karplus PA. 1997. Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. Nat. Struct. Biol. 4:810-18
121. Salamitou S, Raynaud O, Lemaire M, Coughlan M, Béguin P, Aubert J-P. 1994. Recognition specificity of the duplicated segments present in Clostridium thermocellum endoglucanase CelD and in the cellulosome-integrating protein CipA. J. Bacterial. 176:2822-27
122. Salamitou S, Tokatlidis K, Béguin P, Aubert J-P. 1992. Involvement of separate domains of the cellulosomal protein S1 of Clostridium thermocellum in binding to cellulose and in anchoring of catalytic subunits to the cellulosome. FEBS Lett. 304:89-92
123. Saul DJ, Williams LC, Grayling RA, Chamley LW, Love DR, Bergquist PL. 1990. celB, a gene coding for a bifunctional cellulase from the extreme thermophile "Caldocellum saccharolyticum". Appl. Environ. Microbiol. 56:3117-24
124. Schaeffer F, Matuschek M, Guglielmi G, Miras I, Alzari PM, Béguin P. 2002. Duplicated dockerin subdomains of Clostridium thermocellum endoglucanase CelD bind to a cohesin domain of the scaffolding protein CipA with distinct thermodynamic parameters and a negative cooperativity. Biochemistry 41:2106-14
125. Schwarz WH. 2001. The cellulosome and cellulose degradation by anaerobic bacteria. Appl. Microbiol. Biotechnol. 56:634-49
126. a. Shimada K, Hoshino S, Ohmiya K, Sakka K, Kobayashi Y, Karita S, eds. 1993. Genetics, Biochemistry and Ecology of Lignocellulose Degradation, Tokyo: Uni Publ.
127. Shimon LJ, Pages S, Belaich A, Belaich JP, Bayer EA, et al. 2000. Structure of a family IIIa scaffoldin CBD from the cellulosome of Clostridium cellulolyticum at 2.2 Å resolution. Acta. Crystallogr. D Biol. Crystallogr. 56:1560-68
128. Shimon LJW, Bayer EA, Morag E, Lamed R, Yaron S, et al. 1997. A cohesin domain from Clostridium thermocellum: the crystal structure provides new insights into cellulosome assembly. Structure 5:381-90
129. Shoham Y, Lamed R, Bayer EA. 1999. The cellulosome concept as an efficient microbial strategy for the degradation of insoluble polysaccharides. Trends Microbiol. 7:275-81
130. Shoseyov O, Takagi M, Goldstein MA, Doi RH. 1992. Primary sequence analysis of Clostridium cellulovorans cellulose binding protein A. Proc. Natl. Acad. Sci. USA 89:3483-87
131. 15N NMR sequence-specific resonance assignment of a Clostridium thermocellum type II cohesin module. J. Biomol. NMR 23:73-74
132. Spinelli S, Fierobe HP, Belaich A, Belaich JP, Henrissat B, Cambillau C. 2000. Crystal structure of a cohesin module from Clostridium cellulolyticum: implications for dockerin recognition. J. Mol. Biol. 304:189-200
133. Steenbakkers PJM, Arts J, Dijkerman R, Harhangi HR, Op den Camp HJM, et al. 1999. The cellulosome-like complex of the anaerobic fungus Piromyces E2. See Ref. 105a, pp. 507-10
134. Stulk J, Hillen W. 2002. Regulation of carbon catabolism in Bacillus species. Annu. Rev. Microbiol. 54:849-80
135. Tamaru Y, Doi RH. 1999. Three surface layer homology domains at the N terminus of the Clostridium cellulovorans major cellulosomal subunit EngE. J. Bacteriol. 181:3270-76
136. Tamaru Y, Doi RH. 2001. Pectate lyase A, an enzymatic subunit of the Clostridium cellulovorans cellulosome. Proc. Nad. Acad. Sci. USA 20:4125-29
137. Tamaru Y, Karita S, Ibrahim A, Chan H, Doi RH. 2000. A large gene cluster for the Clostridium cellulovorans cellulosome. J. Bacteriol. 182:5906-10
138. Tavares GA, Béguin P, Alzari PM. 1997. The crystal structure of a type I cohesin domain at 1.7 A resolution. J. Mol. Biol. 273:701-13
139. Titgemeyer F, Hillen W. 2002. Global control of sugar metabolism: a grampositive solution. Antonie Van Leeuwenhoek 82:59-71
140. Tokatlidis K, Salamitou S, Béguin P, Dhurjati P, Aubert J-P. 1991. Interaction of the duplicated segment carried by Clostridium thermocellum cellulases with cellulosome components. FEBS Lett. 291:185-88
141. Tomme P, Warren RAJ, Miller RC, Kilburn DG, Gilkes NR. 1995. Cellulose-binding domains: classification and properties. In Enzymatic Degradation of Insoluble Polysaccharides, ed. JM Saddler, MH Penner, pp. 142-61. Washington, DC: Am. Chem. Soc.
142. Tormo J, Lamed R, Chirino AJ, Morag E, Bayer EA, et al. 1996. Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. EMBO J. 15:5739-51
143. Wu JHD, Demain AL. 1988. Proteins of the Clostridium thermocellum cellulase complex responsible for degradation of crystalline cellulose. See Ref. 2a, pp. 117-31
144. Xu Q, Bayer EA, Goldman M, Kenig R, Shoham Y, Lamed R. 2004. Architecture of the Bacteroides cellulosolvens cellulosome: description of a cell surface-anchoring scaffoldin and a family 48 cellulase. J. Bacteriol. 186:968-77
145. Xu Q, Gao W, Ding S-Y, Kenig R, Shoham Y, et al. 2003. The cellulosome system of Acetivibrio cellulolyticus includes a novel type of adaptor protein and a cell-surface anchoring protein. J. Bacteriol. 185:4548-57
146. Yaron S, Morag E, Bayer EA, Lamed R, Shoham Y 1995. Expression, purification and subunit-binding properties of cohesins 2 and 3 of the Clostridium thermocellum cellulosome. FEBS Lett. 360:121-24
147. Zverlov VV, Fuchs K-P, Schwarz WH. 2002. Chi18A, the endochitinase in the cellulosome of the thermophilic, cellulolytic bacterium Clostridium thermocellum. Appl. Environ. Microbiol. 68:3176-79
148. Zverlov VV, Velikodvorskaya GA, Schwarz WH. 2003. Two new cellulosome components encoded downstream of cell in the genome of Clostridium thermocellum: the non-processive endoglucanase CelN and the possibly structural protein CseP. Microbiology 149:515-24
149. Zverlov VV, Velikodvorskaya GV, Schwarz WH, Kellermann J, Staudenbauer WL. 1999. Duplicated Clostridium thermocellum cellobiohydrolase gene encoding cellulosomal subunits S3 and S5. Appl. Microbiol. Biotechnol. 51:852-59
150. Perret S, Casalot L, Fierobe H-P, Tardif C, Sabathe F, et al. 2004. Production of heterologous and chimeric scaffolds by Clostridium acetobutylicum A824. J. Bacteriol. 186:253-57