Complete cellulase system in the marine bacterium Saccharophagus degradans strain 2-40T

Journal of Bacteriology

Volumn 188, Issue 11, 2006, Pages 3849-3861

  Taylor II, Larry E ^a   Henrissat, Bernard ^b   Coutinho, Pedro M ^b   Ekborg, Nathan A ^c   Hutcheson, Steven W ^c   Weiner, Ronald M ^a,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b AIX MARSEILLE UNIVERSITY   (France)

^c Bldg 142   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULASE; CELLULOSE; GLYCOSIDASE; HEMICELLULOSE; LIGNIN; PECTIN; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BACTERIOPLANKTON; BACTERIUM; BIODEGRADATION; CELL WALL; ENZYME ACTIVITY; ENZYME ASSAY; MARINE ENVIRONMENT; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PLANT CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEOMICS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SACCHAROPHAGUS DEGRADANS; STRAIN IDENTIFICATION; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; BASE SEQUENCE; CELLULASE; GAMMAPROTEOBACTERIA; GENOME, BACTERIAL; PROTEOME; RESTRICTION MAPPING; SEAWATER;

ALGAE; BACTERIA (MICROORGANISMS); INVERTEBRATA; SACCHAROPHAGUS; SACCHAROPHAGUS DEGRADANS; SACCHAROPHAGUS DEGRADANS 2-40;

EID: 33744771680     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01348-05     Document Type: Article

References (62)

1. Adelsberger, H., C. Hertel, E. Glawischnig, V. V. Zverlov, and W. H. Schwarz. 2004. Enzyme system of Clostridium stercorarium for hydrolysis of arabinoxylan: reconstitution of the in vivo system from recombinant enzymes. Microbiology 150:2257-2266.
2. Andrykovitch, G., and I. Marx. 1988. Isolation of a new polysaccharide-digesting bacterium from a salt marsh. Appl. Environ. Microbiol. 54:3-4.
3. Barr, B. K., Y. L. Hsieh, B. Ganem, and D. B. Wilson. 1996. Identification of two functionally different classes of exocellulases. Biochemistry 35:586-592.
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., and R. Lamed. 1986. Ultrastructure of the cell surface cellulosome of Clostridium thermocellum and its interaction with cellulose. J. Bacteriol. 167:828-836.
6. Beguin, P., and J. P. Aubert. 1994. The biological degradation of cellulose. FEMS Microbiol. Rev. 13:25-58.
7. Boraston, A. B., D. N. Bolam, H. J. Gilbert, and G. J. Davies. 2004. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382:769-781.
8. Boraston, A. B., V. Notenboom, R. A. Warren, D. G. Kilburn, D. R. Rose, and G. Davies. 2003. Structure and ligand binding of carbohydrate-binding module CsCBM6-3 reveals similarities with fucose-specific lectins and "galactose-binding" domains. J. Mol. Biol. 327:659-669.
9. Carpita, N. C. 1996. Structure and biogenesis of the cell walls of grasses. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:445-476.
10. Cosgrove, D. J., L. C. Li, H.-T. Cho, S. Hoffmann-Benning, R. C. Moore, and D. Blecker. 2002. The growing world of expansins. Plant Cell Physiol. 43: 1436-1444.
11. Coutinho, P. M., and B. Henrissat. 1999. The modular structure of cellulases and other carbohydrate-active enzymes: an integrated database approach, p. 15-23. In K. Ohmiya, K. Hayashi, K. Sakka, C. Kobayashi, S. Karita, and T. Kimura (ed.), Genetics, biochemistry, and ecology of cellulose degradation. Uni Publishers, Tokyo, Japan.
12. Coutinho, P. M., M. Stam, E. Blanc, and B. Henrissat. 2003. Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci. 8:563-565.
13. d'Enfert, C., A. Ryter, and A. P. Pugsley. 1987. Cloning and expression in Escherichia coli of the Klebsiella pneumoniae genes for production, surface localization and secretion of the lipoprotein pullulanase. EMBO J. 6:3531-3538.
14. Distel, D. L., W. Morrill, N. MacLaren-Toussaint, D. Franks, and J. Waterbury. 2002. Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic gamma-proteobacterium isolated from the gills of wood-boring molluscs (Bivalvia: Teredinidae). Int. J. Syst. Evol. Microbiol. 52:2261-2269.
15. Ducret, A., I. Van-Oostveen, J. E. Eng, J. R. Yates III, and R. Aebersold. 1998. High throughput protein characterization by automated reverse-phase chromatography/electrospray tandem mass spectrometry. Protein Sci. 7:706-719.
16. Ekborg, N. A., J. M. Gonzalez, M. B. Howard, L. E. Taylor, S. W. Hutcheson, and R. M. Weiner. 2005. Saccharophagus degradans gen. nov., sp. nov., a versatile marine degrader of complex polysaccharides. Int. J. Syst. Evol. Microbiol. 55:1545-1549.
17. Ensor, L., S. K. Stotz, and R. M. Weiner. 1999. Expression of multiple insoluble complex polysaccharide degrading enzyme systems by a marine bacterium. J. Ind. Microbiol. Biotechnol. 23:123-126.
18. Foreman, P. K., D. Brown, L. Dankmeyer, R. Dean, S. Diener, N. S. Dunn-Coleman, F. Goedegebuur, T. D. Houfek, G. J. England, A. S. Kelley, H. J. Meerman, T. Mitchell, C. Mitchinson, H. A. Olivares, P. J. M. Teunissen, J. Yao, and M. Ward. 2003. Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei. J. Biol. Chem. 278: 31988-31997.
19. Gilkes, N. R., B. Henrissat, D. G. Kilburn, R. C. Miller, Jr., and R. A. Warren. 1991. Domains in microbial β-1,4-glycanases: sequence conservation, function, and enzyme families. Microbiol. Rev. 55:303-315.
20. Gonzalez, J., and R. M. Weiner. 2000. Phylogenetic characterization of marine bacterium strain 2-40, a degrader of complex polysaccharides. Int. J. Syst. Evol. Microbiol. 50:831-834.
21. Green, F., III, C. A. Clausen, and T. L. Highley. 1989. Adaptation of the Nelson-Somogyi reducing-sugar assay to a microassay using microtiter plates. Anal. Biochem. 182:197-199.
22. Hazlewood, G. P., and H. J. Gilbert. 1998. Structure and function analysis of Pseudomonas plant cell wall hydrolases. Prog. Nucleic Acid. Res. Mol. Biol. 61:211-241.
23. Henrissat, B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280((Pt. 2):309-316.
24. Henrissat, B., P. M. Coutinho, E. Deleury, and G. J. Davies. 2003. Sequence families and modular organisation of carbohydrate-active enzymes, p. 15-34. In A. Svendsen (ed.), Enzyme functionality: design, engineering, and screening. Marcel Dekker, New York, N.Y.
25. Henrissat, B., T. T. Teeri, and R. A. Warren. 1998. A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett. 425:352-354.
26. Howard, M. B., N. A. Ekborg, L. E. Taylor, S. W. Hutcheson, and R. M. Weiner. 2004. Identification and analysis of polyserine linker domains in prokaryotic proteins with emphasis on the marine bacterium Microbulbifer degradans. Protein Sci. 13:1422-1425.
27. Howard, M. B., N. A. Ekborg, L. E. Taylor, R. M. Weiner, and S. W. Hutcheson. 2004. Chitinase B of "Microbulbifer degradans" 2-40 contains two catalytic domains with different chitinolytic activities. J. Bacteriol. 186:1297-1303.
28. Howard, M. B., N. A. Ekborg, L. E. Taylor, R. M. Weiner, and S. W. Hutcheson. 2003. Genomic analysis and initial characterization of the chitinolytic system of Microbulbifer degradans strain 2-40. J. Bacteriol. 185:3352-3360.
29. Irwin, D. C., S. Zhang, and D. B. Wilson. 2000. Cloning, expression and characterization of a family 48 exocellulase, Cel48A, from Thermobifida fusca. Eur. J. Biochem. 267:4988-4997.
30. Juncker, A. S., H. Willenbrock, G. Von Heijne, S. Brunak, H. Nielsen, and A. Krogh. 2003. Prediction of lipoprotein signal peptides in gram-negative bacteria. Protein Sci. 12:1652-1662.
31. Jung, H. C., J. M. Lebeault, and J. G. Pan. 1998. Surface display of Zymomonas mobilis levansucrase by using the ice-nucleation protein of Pseudomonas syringae. Nat. Biotechnol. 16:576-580.
32. Kosugi, A., K. Murashima, and R. H. Doi. 2002. Characterization of two noncellulosomal subunits, ArfA and BgaA, from Clostridium cellulovorans that cooperate with the cellulosome in plant cell wall degradation. J. Bacteriol. 184:6859-6865.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 277:680-685.
34. Ljungdahl, L. G., and K. E. Eriksson. 1985. Ecology of microbial cellulose degradation. Adv. Microb. Ecol. 8:237-299.
35. 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.
36. McBride, M. J., and S. A. Baker. 1996. Development of techniques to genetically manipulate members of the genera Cytophaga, Flavobacterium, Flexibacter, and Sporocytophaga. Appl. Environ. Microbiol. 62:3017-3022.
37. 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.
38. Notenboom, V., A. B. Boraston, S. J. Williams, D. G. Kilburn, and D. R. Rose. 2002. High-resolution crystal structures of the lectin-like xylan binding domain from Streptomyces lividans xylanase 10A with bound substrates reveal a novel mode of xylan binding. Biochemistry 41:4246-4254.
39. Perkins, D. N., D. J. Pappin, D. M. Creasy, and J. S. Cottrell. 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551-3567.
40. Pugsley, A. P., C. Chapon, and M. Schwartz. 1986. Extracellular pullulanase of Klebsiella pneumoniae is a lipoprotein. J. Bacteriol. 166:1083-1088.
41. Reverbel-Leroy, C., A. Belaich, A. Bernadac, C. Gaudin, J. Belaich, and C. Tardif. 1996. Molecular study and overexpression of the Clostridium cellulolyticum celF cellulase gene in Escherichia coli. Microbiology 142:1013-1023.
42. Reverbel-Leroy, C., S. Pages, A. Belaich, J. 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.
43. Roberts, A. W., E. M. Roberts, and D. P. Delmer. 2002. Cellulose synthase (CesA) genes in the green alga Mesotaenium caldariorum. Eukaryot. Cell 1:847-855.
44. Saloheimo, M., M. Paloheimo, S. Hakola, J. Pere, B. Swanson, E. Nyyssonen, A. Bhatia, M. Ward, and M. Penttila. 2002. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on celluiosic materials. Eur. J. Biochem. 269:4202-4211.
45. Salyers, A. A., A. Reeves, and J. D'Ella. 1996. Solving the problem of how to eat something as big as yourself: diverse bacterial strategies for degrading polysaccharides. J. Ind. Microbiol. 17:470-476.
46. Schwarz, W. H. 2001. The cellulosome and cellulose degradation by anaerobic bacteria. Appl. Microbiol. Biotechnol. 56:634-649.
47. Schwarz, W. H., V. V. Zverlov, and H. Bahl. 2004. Extracellular glycosyl hydrolases from clostridia. Adv. Appl. Microbiol. 56:215-261.
48. Seydel, A., P. Gounon, and A. P. Pugsley. 1999. Testing the "+2 rule" for lipoprotein sorting in the Escherichia coli cell envelope with a new genetic selection. Mol. Microbiol. 34:810-821.
49. Simpson, P. J., H. Xie, D. N. Bolam, H. J. Gilbert, and M. P. Williamson. 2000. The structural basis for the ligand specificity of family 2 carbohydrate-binding modules. J. Biol. Chem. 275:41137-41142.
50. 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.
51. Tamm, L. K., A. Arora, and J. H. Kleinschmidt. 2001. Structure and assembly of beta-barrel membrane proteins. J. Biol. Chem. 276:32399-32402.
52. Taylor, L. E. 2005. Degradation of plant cell wall polysaccharides by Saccharophagus degradans. Ph.D. thesis. University of Maryland, College Park.
53. Tomme, P., R. A. Warren, and N. R. Gilkes. 1995. Cellulose hydrolysis by bacteria and fungi. Adv. Microb. Physiol. 37:1-81.
54. Vaaje-Kolstad, G., D. R. Houston, A. H. Riemen, V. G. Eijsink, and D. M. van Aalten. 2005. Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J. Biol. Chem. 280:11313-11319.
55. Warren, R. A. 1996. Microbial hydrolysis of polysaccharides. Annu. Rev. Microbiol. 50:183-212.
56. Wood, T. M. 1988. Preparation of crystalline, amorphous, and dyed cellulase substrates. Methods Enzymol. 160:19-25.
57. Zhang, S., D. C. Irwin, and D. B. Wilson. 2000. Site-directed mutation of noncatalytic residues of Thermobifida fusca exocellulase Cel6B. Eur. J. Biochem. 267:3101-3115.
58. Zhang, Y.-H. P., and L. R. Lynd, 2005. Cellulose utilization by Clostridium themocellum: bioenergetics and hydrolysis product assimilation. Proc. Natl. Acad. Sci. USA 102:7321-7325.
59. Zverlov, V. V., J. Kellermann, and W. H. Schwarz. 2005. Functional subgenomics of Clostridium thermocellum cellulosomal genes: identification of the major catalytic components in the extracellular complex and detection of three new enzymes. Proteomics 5:3646-3653.
60. Zverlov, V. V., N. Schantz, and W. H. Schwarz. 2005. A major new component in the cellulosome of Clostridium thermocellum is a processive endo-β-1,4-glucanase producing cellotetraose. FEMS Microbiol. Lett. 249:353-358.
61. Zverlov, V. V., G. A. Velikodvorskaya, and W. H. Schwarz. 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 149:515-524.
62. Zverlov, V. V., G. V. Velikodvorskaya, W. H. Schwarz, K. Bronnenmeier, J. Kellermann, and W. L. Staudenbauer. 1998. Multidomain structure and cellulosomal localization of the Clostridium thermocellum cellobiohydrolase CbhA. J. Bacteriol. 180:3091-3099.