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

Journal of Bacteriology

Volumn 186, Issue 1, 2004, Pages 136-145

  Devillard, Estelle ^a   Goodheart, Dara B ^a   Karnati, Sanjay K R ^a   Bayer, Edward A ^b   Lamed, Raphael ^c   Miron, Joshua ^d   Nelson, Karen E ^e,f   Morrison, Mark ^a,f  

^a OHIO STATE UNIVERSITY   (United States)

^b Weizmann Research Institute   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

^d VOLCANI CENTER   (Israel)

^e J CRAIG VENTER INSTITUTE   (United States)

^f N American Consortium for Genomics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULASE; CELLULOSE; FIBRONECTIN; GLYCOSIDASE; PROTEIN CE148A; PROTEIN CE19B; PROTEIN CELF; PROTEIN CELS; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM MUTANT; CLOSTRIDIUM CELLULOLYTICUM; CLOSTRIDIUM THERMOCELLUM; CYTOLYSIS; GENE SEQUENCE; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN STRUCTURE; RUMINOCOCCUS; RUMINOCOCCUS ALBUS; TWO DIMENSIONAL GEL ELECTROPHORESIS; WILD TYPE;

AMINO ACID SEQUENCE; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; CELLULASES; CELLULOSE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PROTEOME; RUMINOCOCCUS; SEQUENCE ANALYSIS, DNA;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM; CLOSTRIDIUM CELLULOLYTICUM; CLOSTRIDIUM THERMOCELLUM; POSIBACTERIA; RUMINOCOCCUS; RUMINOCOCCUS ALBUS 8;

EID: 0345730809     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.1.136-145.2004     Document Type: Article

References (51)

1. Aurilia, V., J. C. Martin, S. I. McCrae, K. P. Scott, M. T. Rincon, and H. J. Flint. 2000. Three multidomain esterases from the cellulolytic rumen anaerobe Ruminococcus flavefaciens 17 that carry divergent dockerin sequences. Microbiology 146:1391-1397.
2. Bayer, E. A., R. Kenig, and R. Lamed. 1983. Adherence of Clostridium thermocellum to cellulose. J. Bacteriol. 156:818-827.
3. Bayer, E. A., L. J. Shimon, Y. Shoham, and R. Lamed. 1998. Cellulosomes-structure and ultrastructure. J. Struct. Biol. 124:221-234.
4. Bayer, E. A., H. Chanzy, R. Lamed, and Y. Shoham. 1998. Cellulose, cellulases and cellulosomes. Curr. Opin. Struct. Biol. 8:548-557.
5. Bayer, E. A., Y. Shoham, and R. Lamed. 2 November 2001, release date. Cellulose-decomposing bacteria and their enzyme systems. In M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (ed.) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd ed., release 3.7. Springer-Verlag, New York, N.Y. [Online.] http: //141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=297.
6. Beguin, P., and M. Lemaire. 1996. The cellulosome: an exocellular, multiprotein complex specialized in cellulose degradation. Crit. Rev. Biochem. Mol. Biol. 31:201-236.
7. Belaich, A., G. Parsiegla, L. Gal, C. Villard, R. Haser, and J.-P. Belaich. 2002. Cel9M, a new family 9 cellulase of the Clostridium cellulolyticum cellulosome. J. Bacteriol. 184:1378-1384.
8. Bourne, Y., and B. Henrissat. 2001. Glycoside hydrolases and glycosyltransferases: families and functional modules. Curr. Opin. Struct. Biol. 11:593-600.
9. Bradford, M. M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Champion, K. M., C. T. Helaszek, and B. A. White. 1988. Analysis of antibiotic susceptibility and extrachromosomal DNA content of Ruminococcus albus and Ruminococcus flavefaciens. Can. J. Microbiol. 34:1109-1115.
11. Ding, S. Y., E. A. Bayer, D. Steiner, Y. Shoham, and R. Lamed. 1999. A novel cellulsomal scaffoldin from Acetivibrio cellulolyticus that contains a family 9 glycosyl hydrolase. J. Bacteriol. 181:6720-6729.
12. Ding, S. Y., M. T. Rincon, R. Lamed, J. C. Martin, S. I. McCrae, V. Aurilla, Y. Shoham, E. A. Bayer, and H. J. Flint. 2001. Cellulosomal scaffoldin-like proteins from Ruminococcus flavefaciens. J. Bacteriol. 183:1945-1953.
13. 14C]-labeled cellulose. Biotechnol. Lett. 8:581-589.
14. Gaudin, C., A. Belaich, S. Champ, and J.-P. Belaich. 2000. CelE, a multidomain cellulase from Clostridium cellulolyticum: a key enzyme in the cellulosome? J. Bacteriol. 182:1910-1915.
15. Gong, J., and C. W. Forsberg. 1989. Factors affecting adhesion of Fibrobacter succinogenes subsp. succinogenes S85 and adherence-defective mutants to cellulose. Appl. Environ. Microbiol. 55:3039-3044.
16. Henrissat, B., T. T. Teeri, and R. A. J. Warren. 1998. A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett. 425:352-354.
17. Henrissat, B., and P. M. Coutinho. 2001. Classification of glycoside hydrolases and glycosyltransferases from hyperthermophiles. Methods Enzymol. 330:183-201.
18. Hermann, T., M. Finkemeier, W. Pfefferle, G. Wersch, R. Kramer, and A. Burkovski. 2000. Two-dimensional electrophoresis analysis of Corynebacterium glutamicum membrane fraction and surface proteins. Electrophoresis 21:654-659.
19. Jee, J. G., T. Ikegami, M. Hashimoto, T. Kawabata, M. Ikeguchi, T. Watanabe, and M. Shirakawa. 2002. Solution structure of the fibronectin type III domain from Bacillus circulans WI-12 chitinase Al. J. Biol. Chem. 277:1388-1397.
20. Karita, S., K. Sakka, and K. Ohmiya. 1998. Cellulososmes and cellulose complexes of anaerobic microbes: their structure, models and function, p. 44-57. In R. Onodera, H. Itabashi, K. Ushida, H. Yano, and Y. Sasaki (ed.), Rumen microbes and digestive physiology in ruminants. Japan Scientific Societies Press, Tokyo, Japan.
21. Kataeva, I., X.-L. Li, H. Chen, H. Choi, and L. G. Ljungdahl. 1999. Cloning and sequence analysis of a new cellulase gene encoding CelK, a major cellulosome component of Clostridium thermocellum: evidence for gene duplication and recombination. J. Bacteriol. 181:5288-5295.
22. Kataeva, I. A., R. D. Seidel III, A. Shah, L. T. West, X.-L. Li, and L. G. Ljungdahl. 2002. The fibronectin type 3-like repeat from the Clostridium thermocellum cellobiohydrolase CbhA promotes hydrolysis of cellulose by modifying its surface. Appl. Environ. Microbiol. 68:4292-4300.
23. Kim, Y. S., S. G. Wi, and K. H. Myung. 1998. Ultrastructural studies of Ruminococcus albus surface structures involved in lignocellulose degradation, p. 119. In Proceedings of the Mie Bioforum on Cellulose Degradation. Mie University Press, Mie, Japan.
24. Kirby, J., J. C. Martin, A. S. Daniel, and H. J. Flint. 1997. Dockerin-like sequences in cellulases and xylanases from the rumen cellulolytic bacterium Ruminococcus flavefaciens. FEMS Microbiol. Lett. 149:213-219.
25. Kruus, K., A. Andreacchi, W. K. Wang, and J. H. Wu. 1995. Product inhibition of the recombinant CelS, an exoglucanase component of the Clostridium thermocellum cellulosome. Appl. Microbiol. Biotechnol. 44:399-404.
26. Lamed, R., E. Setter, and E. A. Bayer. 1983. Characterization of cellulose-binding, cellulase-containing complex in Clostridium thermocellum. J. Bacteriol. 156:828-836.
27. Lamed, R., J. Naimark, E. Morgenstern, and E. A. Bayer. 1987. Specialized cell surface structures in cellulolytic bacteria. J. Bacteriol. 169:3792-3800.
28. Lynd, L. R., P. J. Weimer, W. H. van Zyl, and I. S. Pretorius. 2002. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 66:506-577.
29. Miron, J., and C. W. Forsberg. 1998. Features of Fibrobacter intestinalis DR7 mutant which is impaired with its ability to adhere to cellulose. Anaerobe 4:35-43.
30. Miron, J., E. Morag, E. A. Bayer, R. Lamed, R., and D. Ben-Ghedalia. 1998. An adhesion defective mutant of Ruminococcus albus SY3 is impaired in its capacity to degrade cellulose. J. Appl. Microbiol. 84:249-254.
31. Miron, J., J. Jacobovitch, E. A. Bayer, R. Lamed, M. Morrison, and D. Ben-Ghedalia. 2001. Subcellular distribution of glycanases and related components in Ruminococcus albus SY3 and their role in cell adhesion to cellulose. J. Appl. Microbiol. 91:677-685.
32. Morag, E., I. Halevy, E. A. Bayer, and R. Lamed. 1991. Isolation and properties of a major cellobiohydrolase from the cellulosome of Clostridium thermocellum. J. Bacteriol. 173:4155-4162.
33. Morrison, M., and J. Miron. 2000. Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and Pil-proteins? FEMS Microbiol. Lett. 185:109-115.
34. Mosoni, P., and B. Gaillard-Martinie. 2001. Characterization of a spontaneous adhesion-defective mutant of Rumnicoccus albus strain 20. Arch. Microbiol. 176:52-61.
35. Ohara, H., S. Karita, T. Kimura, K. Sakka, and K. Ohmiya. 2000. Characterization of the cellulolytic complex (cellulosome) from Ruminococcus albus. Biosci. Biotechnol. Biochem. 64:254-260.
36. Ohara, H., J. Noguchi, S. Karita, T. Kimura, K. Sakka, and K. Ohmiya. 2000. Sequence of egV and properties of EgV, a Ruminococcus albus endoglucanase containing a dockerin domain. Biosci. Biotechnol. Biochem. 64:80-88.
37. Parsiegla, G., C. Reverbel-Leroy, C. Tardiff, J.-P. Belaich, H. Driguez, and R. Haser. 2000. Crystal structures of the cellulase Cel48F in complex with inhibitors and substrates give insights into its processive action. Biochemistry 39:11238-11246.
38. Pegden, R. S., M. A. Larson, R. J. Grant, and M. Morrison. 1998. Adherence of the gram-positive bacterium Ruminococcus albus to cellulose and identification of a novel form of cellulose-binding protein which belongs to the Pil family of proteins. J. Bacteriol. 180:5921-5927.
39. Perrakis, A., I. Tews, Z. Dauter, A. B. Oppenheim, I. Chet, K. S. Wilson, and C. E. Vorgias. 1994. Crystal structure of a bacterial chitinase at 2.3 Å resolution. Structure 2:1169-1180.
40. Perrakis, A., C. Ouzounis, and K. S. Wilson. 1997. Evolution of immunoglobulin-like modules in chitinases: their structural flexibility and functional implications. Fold Des. 2:291-294.
41. Rainey, F. A., and P. H. Janssen. 1995. Phylogenetic analysis by 16S ribosomal DNA sequence comparison reveals two unrelated groups of species within the genus Ruminococcus. FEMS Microbiol. Lett. 129:69-73.
42. Rakotoarivonina, H., G. Jubelin, M. Hebraud, B. Gaillard-Martinie, E. Forano, and P. Mosoni. 2002. Adhesion to cellulose of the Gram-positive bacterium Ruminococcus albus involves type IV pili. Microbiology 148:1871-1880.
43. Reverbel-Leroy, C., S. Pages, A. Belaich, J.-P. Belaich, and C. Tardif. 1997. The processive endocellulase CelF, a major component of the Clostridium cellulolyticum cellulosome: purification and characterization of the recombinant form. J. Bacteriol. 179:46-52.
44. Rincon, M. T., S. I. McCrae, J. Kirby, K. P. Scott, and H. J. Flint. 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. 67:4426-4431.
45. Rincon, M. T., S. Y. Ding, S. I. McCrae, J. C. Martin, V. Aurillia, R. Lamed, Y. Shoham, E. A. Bayer, and H. J. Flint. 2003. Novel organization and divergent dockerin specificities in the cellulososme system of Ruminococcus flavefaciens. J. Bacteriol. 185:703-713.
46. Shoham, Y., R. Lamed, and E. A. Bayer. 1999. The cellulosome concept as an efficient microbial strategy for the degradation of insoluble polysaccharides. Trends Microbiol. 7:275-281.
47. Stack, R. J., R. E. Hungate, and W. P. Opsahl. 1983. Phenylacetic acid stimulation of cellulose digestion by Ruminococcus albus 8. Appl. Environ. Microbiol. 46:539-544.
48. Stack, R. J., and R. E. Hungate. 1984. Effect of the 3-phenylpropanoic acid on capsule and cellulases of Ruminococcus albus 8. Appl. Environ. Microbiol. 48:218-223.
49. Tomme, P., R. A. Warren, and N. R. Gilkes. 1995. Cellulose hydrolysis by bacteria and fungi. Adv. Microb. Physiol. 37:1-81.
50. Tomme, P., E. Kwan, N. R. Gilkes, D. G. Kilburn, and R. A. Warren. 1996. Characterization of CenC, an enzyme from Cellulomonas fimi with both endo-and exoglucanase activities. J. Bacteriol. 178:4216-4223.
51. Zverlov, V. V., G. V. Velikodvorskaya, W. H. Schwarz, K. Bronnenmeier, J. Kellermann, and W. L. Staudenbauer. 1998. Multidomain structure and cellulosmal localization of the Clostridium thermocellum cellobiohydrolase CbhA. J. Bacteriol. 180:3091-3099.