Outer membrane proteins of Fibrobacter succinogenes with potential roles in adhesion to cellulose and in cellulose digestion

Journal of Bacteriology

Volumn 189, Issue 19, 2007, Pages 6806-6815

  Jun, Hyun Sik ^a,b   Qi, Meng ^a   Gong, Joshua ^a,c   Egbosimba, Emmanuel E ^a,d   Forsberg, Cecil W ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^d UNIVERSITY OF WINDSOR   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE; GLUCOSE; OUTER MEMBRANE PROTEIN; PILIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM MUTANT; COMPARATIVE STUDY; FIBROBACTER SUCCINOGENES; MEMBRANE BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TWO DIMENSIONAL ELECTROPHORESIS;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, WESTERN; CELLULOSE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FIBROBACTER; GLUCOSE; GLYCOSIDE HYDROLASES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

FIBROBACTER SUCCINOGENES;

EID: 34948911454     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00560-07     Document Type: Article

References (52)

1. Arai, T., R. Araki, A. Tanaka, S. Karita, T. Kimura, K. Sakka, and K. Ohmiya. 2003. Characterization of a cellulase containing a family 30 carbohydrate-binding module (CBM) derived from Clostridium thermocellum CelJ: importance of the CBM to cellulose hydrolysis. J. Bacteriol. 185:504-512.
2. Bera-Maillet, C., Y. Ribot, and E. Forano. 2004. Fiber-degrading systems of different strains of the genus Fibrobacter. Appl. Environ. Microbiol. 70:2172-2179.
3. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram amounts of protein using the principle of protein-dye binding. Anal. Biochem. 72:248-254.
4. Chevallet, M., V. Santoni, A. Poinas, D. Rouquié, A. Fuchs, S. Kieffer, M. Rossignol, J. Lunardi, J. Garin, and T. Rabilloud. 1998. New zwitterionic detergents improve the analysis of membrane proteins by two-dimensional electrophoresis. Electrophoresis 19:1901-1909.
5. Das, A. K., P. W. Cohen, and D. Barford. 1998. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17:1192-1199.
6. Dubois, M., K. A. Gilles, K. Hamilton, P. A. Rebers, and F. Smith. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350-356.
7. Eichinger, L., et al. 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435:43-57.
8. Fischer, E. H., H. Charbonneau, and N. K. Tonks. 1991. Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes. Science 253:401-406.
9. Freudl, R., M. Klose, and U. Henning. 1990. Export and sorting of the Escherichia coli outer membrane protein OmpA. J. Bioenerg. Biomembr. 22:441-449.
10. Goebl, M., and M. Yanagida. 1991. The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biochem. Sci. 16:173-177.
11. Gong, J., E. E. Egbosimba, and C. W. Forsberg. 1996. Cellulose-binding proteins of Fibrobacter succinogenes and the possible role of a 180 kDa cellulose-binding glycoprotein in adhesion to cellulose. Can. J. Microbiol. 42:453-460.
12. 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.
13. Gong, J., and C. W. Forsberg. 1993. Separation of outer and cytoplasmic membranes of Fibrobacter succinogenes and membrane and glycogen granule locations of glycanase and cellobiase. J. Bacteriol. 175:6810-6821.
14. Herbert, B. 1999. Advances in protein solubilisation for two-dimensional electrophoresis. Electrophoresis 20:660-663.
15. Huang, L., and C. W. Forsberg. 1988. Purification and comparison of the periplasmic and extracellular forms of the cellodextrinase from Bacteroides succinogenes. Appl. Environ. Microbiol. 54:1488-1493.
16. Huang, L., and C. W. Forsberg. 1990. Cellulose digestion and cellulase regulation and distribution in Fibrobacter succinogenes subsp. succinogenes S85. Appl. Environ. Microbiol. 56:1221-1228.
17. Huang, L., C. W. Forsberg, and D. Y. Thomas. 1988. Purification and characterization of a chloride-stimulated cellobiosidase from Bacteroides succinogenes S85. J. Bacteriol. 170:2923-2932.
18. Huang, L., M. McGavin, C. W. Forsberg, J. S. Lam, and K. J. Cheng. 1990. Antigenic nature of the chloride-stimulated cellobiosidase and other cellulases of Fibrobacter succinogenes subsp. succinogenes S85 and related fresh isolates. Appl. Environ. Microbiol. 56:1229-1234.
19. Jenkins, J., O. Mayans, and R. Pickersgill. 1998. Structure and evolution of parallel β-helix proteins. J. Struct. Biol. 122:236-246.
20. Johnson, J. M., and G. M. Church. 1999. Alignment and structure prediction of divergent protein families: periplasmic and outer membrane proteins of bacterial efflux pumps. J. Mol. Biol. 287:695-715.
21. Jun, H. S., J. K. Ha, L. M. Malburg, Jr., G. A. Verrinder, and C. W. Forsberg. 2003. Characteristics of a cluster of xylanase genes in Fibrobacter succinogenes S85. Can. J. Microbiol. 49:171-180.
22. Kam, D. K., H. S. Jun, J. Ha, G. D. Inglis, and C. W. Forsberg. 2005. Characteristics of adjacent family 6 acetylxylan esterases from Fibrobacter succinogenes and the interaction with the XynE xylanase in hydrolysis of acetylated xylan. Can. J. Microbiol. 51:821-832.
23. 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.
24. Koike, S., S. Yoshitani, Y. Kobayashi, and K. Tanaka. 2003. Phylogenetic analysis of fiber-associated rumen bacterial community and PCR detection of uncultured bacteria. FEMS Microbiol. Lett. 229:23-30.
25. Kudo, H, K. J. Cheng, and J. W. Costerton. 1987. Electron microscopic study of the methylcellulose-mediated detachment of cellulolytic rumen bacteria from cellulose fibers. Can. J. Microbiol. 33:267-272.
26. Kuwahara, T., A. Yamashita, H. Hirakawa, H. Nakayama, H. Toh, N. Okada, S. Kuhara, M. Hattori, T. Hayashi, and Y. Ohnishi. 2004. Genomic analysis of Bacteroides fragilis reveals extensive DNA inversions regulating cell surface adaptation. Proc. Natl. Acad. Sci. USA 101:14919-14924.
27. Lamb, J. R., S. Tugendreich, and P. Hieter. 1995. Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem. Sci. 20:257-259.
28. Lawler, J., and R. O. Hynes. 1986. The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. J. Cell. Biol. 103:1635- 1648.
29. Liu, Y., J. Zhang, Q. Liu, C. Zhang, and Q. Ma. 2004. Molecular cloning of novel cellulase genes cel9A and cel12A from Bacillus licheniformis GXN151 and synergism of their encoded polypeptides. Curr. Microbiol. 49:234-238.
30. 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, table.
31. Malburg, L. M., A. H. Iyo, and C. W. Forsberg. 1996. A novel family 9 endoglucanase gene (celD), whose product cleaves substrates mainly to glucose, and its adjacent upstream homolog (celE) from Fibrobacter succinogenes S85. Appl. Environ. Microbiol. 62:898-906.
32. Malburg, S. R. C., L. M. Malburg, T. Liu, A. H. Iyo, and C. W. Forsberg. 1997. Catalytic properties of the cellulose-binding endoglucanase F from Fibrobacter succinogenes S85. Appl. Environ. Microbiol. 63:2449-2453.
33. McGavin, M., and C. W. Forsberg. 1988. Isolation and characterization of endoglucanases 1 and 2 from Bacteroides succinogenes S85. J. Bacteriol. 170:2914-2922.
34. McGavin, M., and C. W. Forsberg. 1989. Catalytic and substrate-binding domains of endoglucanase 2 from Bacteroides succinogenes. J. Bacteriol. 171:3310-3315.
35. McGavin, M. J., C. W. Forsberg, B. Crosby, A. W. Bell, D. Dignard, and D. Y. Thomas. 1989. Structure of the cel-3 gene from Fibrobacter succinogenes S85 and characteristics of the encoded gene product, endoglucanase 3. J. Bacteriol. 171:5587-5595.
36. Nelles, L. P., and J. R. Bamburg. 1976. Rapid visualization of protein - dodecyl sulfate complexes in Polyacrylamide gels. Anal. Biochem. 73:522-531.
37. Neuhoff, V., N. Arold, D. Taube, and W. Ehrhardt. 1988. Improved staining of proteins in Polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255-262.
38. Neuwald, A. F., L. Aravind, J. L. Spouge, and E. V. Koonin. 1999. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9:27-43.
39. Pell, A. N., and P. Schofield. 1993. Microbial adhesion and degradation of plant cell walls, p. 397-423. In H. G. Jung, D. R. Buxton, R. D. Hatfield, and J. Ralph (ed.), Forage cell wall structure and digestibility. American Society of Agronomy, Inc., Madison, WI.
40. Qi, M., H.-S. Jun, and C. W. Forsberg. July 2007, posting date. Characterization and synergistic interactions of Fibrobacter succinogenes glycoside hydrolases. Appl. Environ. Microbiol., in press.
41. Qi, M., K. E. Nelson, S. C. Daugherty, W. C. Nelson, I. R. Hance, M. Morrison, and C. W. Forsberg. 2005. Novel molecular features of the fibrolytic intestinal bacterium Fibrobacter intestinalis not shared with Fibrobacter succinogenes as determined by suppressive subtractive hybridization. J. Bacteriol. 187:3739-3751.
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. Scott, H. W., and B. A. Dehority. 1965. Vitamin requirements of several cellulolytic bacteria. J. Bacteriol. 89:1169-1175.
44. Shoseyov, O., T. Hamamoto, F. Foong, and R. H. Doi. 1990. Cloning of Clostridium cellulovorans endo-1,4-b-glucanase genes. Biochem. Biophys. Res. Commun. 169:667-672.
45. Smith, P. K., R. I. Krohn, G. T. Hermanson, A. K. Mallia, F. H. Gartner, M. D. Provenzano, E. K. Fujimoto, N. M. Goeke, B. J. Olson, and D. C. Klenk. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:76-85.
46. Stalbrand, H., S. D. Mansfield, J. N. Saddler, D. G. Kilburn, R. A. Warren, and N. R. Gilkes. 1998. Analysis of molecular size distributions of cellulose molecules during hydrolysis of cellulose by recombinant Cellulomonas fimi β-1,4-glucanases. Appl. Environ. Microbiol. 64:2374-2379.
47. Suerbaum, S., C. Josenhans, T. Sterzenbach, B. Drescher, P. Brandt, M. Bell, M. Droge, B. Fartmann, H. P. Fischer, Z. Ge, A. Horster, R. Holland, K. Klein, J. Konig, L. Macko, G. L. Mendz, G. Nyakatura, D. B. Schauer, Z. Shen, J. Weber, M. Frosch, and J. G. Fox. 2003. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc. Natl. Acad. Sci. USA 100:7901-7906.
48. Tamara, Y., S. Karita, A. Ibrahim, H. Chan, and R. H. Doi. 2000. A large gene cluster for the Clostridium cellulovorans cellulosome. J. Bacteriol. 182:5906-5910.
49. Updegraff, D. M. 1969. Semimicro determination of cellulose in biological materials. Anal. Biochem. 32:420-424.
50. von Heijne, G. 1989. The structure of signal peptides from bacterial lipoproteins. Protein Eng. 2:531-534.
51. Wood, T. M. 1988. Preparation of crystalline, amorphous and dyed cellulose substrates. Methods Enzymol. 160:19-25.
52. Zhu, H., F. W. Paradis, P. J. Krell, J. P. Phillips, and C. W. Forsberg. 1994. Enzymatic specificities and modes of action of the two catalytic domains of the XynC xylanase from Fibrobacter succinogenes S85. J. Bacteriol. 176:3885-3894.