An extra peptide within the catalytic module of a β-agarase affects the agarose degradation pattern

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 9519-9531

  Han, Wen Jun ^a   Gu, Jing Yan ^a   Liu, Hui Hui ^a   Li, Fu Chuan ^a   Wu, Zhi Hong ^a   Li, Yue Zhong ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE RESIDUES; BIOINFORMATIC ANALYSIS; DEGRADATION PATTERNS; DEGRADATION PRODUCTS; ENZYMATIC ACTIVITIES; ENZYMATIC FUNCTIONS; GLYCOSIDE HYDROLASES; OPTIMAL TEMPERATURE;

AMINO ACIDS; BIOINFORMATICS; DEGRADATION; ENZYME ACTIVITY; PEPTIDES;

CLONING;

AGAG4 ENZYME; AGAROSE; ASPARAGINE; BACTERIAL ENZYME; GENOMIC DNA; GLYCINE; MUTANT PROTEIN; NEOAGAROHEXAOSE; NEOAGAROOCTAOSE; NEOAGAROOOLIGOSACCHARIDE; NEOAGAROTETRAOSE; OLIGOSACCHARIDE; PROTEIN DEGRADATION END PRODUCT; TYROSINE; UNCLASSIFIED DRUG;

AGAG4 GENE; ARTICLE; BACTERIAL GENE; BACTERIUM; BIOINFORMATICS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DEGRADATION KINETICS; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME DEGRADATION; ENZYME STABILITY; FLAMMEOVIRGA; GENE SEQUENCE; HETEROLOGOUS EXPRESSION; MOLECULAR PHYLOGENY; MOLECULAR WEIGHT; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN REFOLDING; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BACTERIA; CATALYSIS; CATALYTIC DOMAIN; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DNA PRIMERS; GENETIC VECTORS; GLYCOSIDE HYDROLASES; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; OLIGOSACCHARIDES; PEPTIDES; PHYLOGENY; PROTEIN BINDING; SEPHAROSE; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TEMPERATURE;

FLAMMEOVIRGA;

EID: 84875967731     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.412247     Document Type: Article

References (41)

1. Rees, D. A. (1969) Structure, conformation, and mechanism in the formation of polysaccharide gels and networks. Adv. Carbohydr. Chem. Biochem. 24, 267-332
2. Rochas, C., Potin, P., and Kloareg, B. (1994) NMR spectroscopic investigation of agarose oligomers produced by an α-agarase. Carbohydr. Res. 253, 69-77
3. Morrice, L. M., McLean, M. W., Long, W. F., and Williamson, F. B. (1983) β-Agarases I and II from Pseudomonas atlantica. Substrate and specificities. Eur. J. Biochem. 137, 149-154
4. Morrice, L. M., McLean, M. W., Williamson, F. B., and Long, W. F. (1983) β-Agarases I and II from Pseudomonas atlantica. Purifications and some properties. Eur. J. Biochem. 135, 553-558
5. Michel, G., Nyval-Collen, P., Barbeyron, T., Czjzek, M., and Helbert, W. (2006) Bioconversion of red seaweed galactans. A focus on bacterial agarases and carrageenases. Appl. Microbiol. Biotechnol. 71, 23-33
6. Fu, X. T., and Kim, S. M. (2010) Agarases. Review of major sources, categories, purification method, enzyme characteristics and applications. Mar. Drugs. 8, 200-218
7. Chi, W. J., Chang, Y. K., and Hong, S. K. (2012) Agar degradation by microorganisms and agar-degrading enzymes. Appl. Microbiol. Biotechnol. 94, 917-930
8. Potin, P., Richard, C., Rochas, C., and Kloareg, B. (1993) Purification and characterization of the α-agarase from Alteromonas agarlyticus (Cataldi) comb. nov., strain GJ1B. Eur. J. Biochem. 214, 599-607
9. Ohta, Y., Hatada, Y., Miyazaki, M., Nogi, Y., Ito, S., and Horikoshi, K. (2005) Purification and characterization of a novel α-agarase from a Thalassomonas sp. Curr. Microbiol. 50, 212-216
10. Allouch, J., Jam, M., Helbert, W., Barbeyron, T., Kloareg, B., Henrissat, B., and Czjzek, M. (2003) The three-dimensional structures of two β-agarases. J. Biol. Chem. 278, 47171-47180
11. Michel, G., Barbeyron, T., Kloareg, B., and Czjzek M. (2009) The family 6 carbohydrate-binding modules have coevolved with their appended catalytic modules toward similar substrate specifity. Glycobiology. 19, 615-623
12. Henrissat, B., and Davies, G. (1997) Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637-644
13. Flament, D., Barbeyron, T., Jam, M., Potin, P., Czjzek, M., Kloareg, B., and Michel G. (2007) α-agarases define a new family of glycoside hydrolases distinct from β-agarase families. Appl. Environ. Microbiol. 73, 4691-4694
14. Ma, C., Lu, X., Shi, C., Li, J., Gu, Y., Ma, Y., Chu, Y., Han, F., Gong, Q., and Yu, W. (2007) Molecular cloning and characterization of a novel -agarase, AgaB, from marine Pseudoalteromonas sp. CY24. J. Biol. Chem. 282, 3747-3754
15. Dong, J., Hashikawa, S., Konishi, T., Tamaru, Y., and Araki, T. (2006) Cloning of the novel gene encoding β-agarase C from a marine bacterium, Vibrio sp. strain PO-303, and characterization of the gene product. Appl. Environ. Microbiol. 72, 6399-6401
16. Hehemann, J. H., Michel, G., Barbeyron, T., and Czjzek, M. (2010) Expression, purification and preliminary x-ray diffraction analysis of the catalytic module of a β-agarase from the flavobacterium Zobellia galactanivorans. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 413-417
17. Ren, A., Xia, Z. X., Yu, W., and Zhou, J. (2010) Expression, crystallization and preliminary x-ray analysis of an anomeric inverting agarase from Pseudoalteromonas sp. CY24. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 1635-1639
18. Jam, M., Flament, D., Allouch, J., Potin, P., Thion, L., Kloareg, B., Czjzek, M., Helbert, W., Michel, G., and Barbeyron, T. (2005) The endo-β-agarase AgaA and AgaB from the marine bacterium Zobellia galactanivorans. Two paralogue enzymes with different molecular organizations and catalytic behaviours. Biochem. J. 385, 703-713
19. Shi, C., Lu, X., Ma, C., Ma, Y., Fu, X., and Yu, W. (2008) Enhancing the thermostability of a novel β-agarase AgaB through directed evolution. Appl. Biochem. Biotechnol. 151, 51-59
20. Jang, M. K., Lee, S. W., Lee, D. G., Kim, N. Y., Yu, K. H., Jang, H. J., Kim, S., Kim, A., and Lee, S. H. (2010) Enhancement of the thermostability of a recombinant β-agarase, AgaB, from Zobellia galactanivorans by random mutagenesis. Biotechnol. Lett. 32, 943-949
21. Lee, S., Lee, D. G., Jang, M. K., Jeon, M. J., Jang, H. J., and Lee, S. H. (2011) Improvement in the catalytic activity of β-agarase AgaA from Zobellia galactanivorans by site-directed mutagenesis. J. Microbiol. Biotechnol. 21, 1116-1122
22. Nakagawa, Y., Hamana, K., Sakane, T., and Yamasato, K. (1997) Reclassification of Cytophaga aprica (Lewin 1969) Reichenbach 1989 in Flammeovirga gen. nov. as Flammeovirga aprica comb. nov., and of Cytophaga diffluens (ex Stanier 1940; emend. Lewin 1969) Reichenbach 1989 in Persicobacter gen. nov. as Persicobacter diffluens comb. nov. Int. J. Syst. Evol. Microbiol. 47, 220-223
23. Takahashi, M., Suzuki, K., and Nakagawa, Y. (2006) Emendation of the genus Flammeovirga and Flammeovirga aprica with the proposal of Flammeovirga arenaria nom. rev., comb. nov., and Flammeovirga yaeyamensis sp. nov. Int. J. Syst. Evol. Microbiol. 56, 2095-2100
24. Hosoya, S., and Yokota, A. (2007) Flammeovirga kamogawensis sp. nov., isolated from coastal seawater in Japan. Int. J. Syst. Evol. Microbiol. 57, 1327-1330
25. Xu, H., Fu, Y., Yang, N., Ding, Z., Lai, Q., and Zeng, R. (2012) Flammeovirga pacifica sp. nov., isolated from deep-sea sediment. Int. J. Syst. Evol. Microbiol. 62, 937-941
26. Han, W. J., Gu, J. Y., Yan, Q. J., Li, J. G., Wu, Z. H., Gu, Q. Q., and Li, Y. Z. (2012) A polysaccharide-degrading marine bacterium Flammeovirga sp. MY04 and its extracellular agarase system. J. Ocean Univ. China 11, 375-382
27. Sambrook, J., and Russel, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd Ed, pp. A8.40-A8.47, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
28. Birnboim, H. C., and Doly, J. (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7, 1513-1523
29. Suzuki, H., Sawai, Y., Suzuki, T., and Kawai, K. (2002) Purification and characterization of an extracellular β-agarase from Bacillus sp. MK03. J. Biosci. Bioeng. 93, 456-463
30. Hall, T. A. (1999) BioEdit. A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98
31. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5. Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739
32. Miller, G. L. (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31, 426-428
33. Wang, S. Y., Hu, W., Lin, X. Y., Wu, Z. H., and Li, Y. Z. (2012) A novel cold-active xylanase from the cellulolytic myxobacterium Sorangium cellulosum So9733-1. Gene cloning, expression, and enzymatic characterization. Appl. Microbiol. Biotechnol. 93, 1503-1512
34. Bigge, J. C., Patel, T. P., Bruce, J. A., Goulding, P. N., Charles, S. M., and Parekh, R. B. (1995) Nonselective and efficient fluorescent labelling of glycans using 2-amino benzamide and anthranilic acid. Anal. Biochem. 230, 229-238
35. Nielsen, M., Lundegaard, C., Lund, O., and Petersen, T. N. (2010) CPHmodels-3.0. Remote homology modelling using structure guided sequence profiles. Nucleic Acids Res. 38, W576-W581
36. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb-Viewer. An environment for comparative protein modelling. Electrophoresis. 18, 2714-2723
37. Yang, J. I., Chen, L. C., Shih, Y. Y., Hsieh, C., Chen, C. Y., Chen, W. M., and Chen, C. C. (2011) Cloning and characterization of -agarase AgaYT from Flammeovirga yaeyamensis strain YT. J. Biosci. Bioeng. 112, 225-232
38. Zhong, Z., Toukdarian, A., Helinski, D., Knauf, V., Sykes, S., Wilkinson, J. E., O'Bryne, C., Shea, T., DeLoughery, C., and Caspi, R. (2001) Sequence analysis of a 101-kilobase plasmid required for agar degradation by a Microscilla isolate. Appl. Environ. Microbiol. 67, 5771-5779
39. Hehemann, J. H., Correc, G., Thomas, F., Bernard, T., Barbeyron, T., Jam, M., Helbert, W., Michel, G., and Czjzek M. (2012) Biochemical and structural characterization of the complex agarolytic enzyme system from the marine bacterium Zobellia galactanivorans. J. Biol. Chem. 287, 30571-30584
40. Hehemann, J. H., Correc, G., Barbeyron, T., Helbert, W., Czjzek, M., and Michel, G. (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908-912
41. Rochas, C., Lahaye, M., Yaphe, W., and Phan Viet, M. T. (1986) 13C-NMR spectroscopic investigation of agarose oligomers. Carbohydr. Res. 148, 199-207