A novel unsaturated β-glucuronyl hydrolase involved in ulvan degradation unveils the versatility of stereochemistry requirements in family GH105

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 6199-6211

  Collén, Pi Nyvall ^a,e   Jeudy, Alexandra ^a   Sassi, Jean François ^b   Groisillier, Agnès ^a   Czjzek, Mirjam ^a   Coutinho, Pedro M ^c   Helbert, William ^a,d  

^a CNRS   (France)

^b Centre d'Etudes et de Valorisation des Algues   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^e Pôle Biotechnologique du Haut du Bois   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE STRUCTURE; ENZYMATIC DEGRADATION; GLYCOSIDE HYDROLASES; GLYCOSIDIC LINKAGES; SEQUENCE SIMILARITY; SUBSTRATE BINDING; SUBSTRATE SPECIFICITY; THREE-DIMENSIONAL CRYSTALS;

ALGAE; CLONING; ESCHERICHIA COLI; GENES; HYDROLYSIS; SUGARS;

HYDROLASES;

BETA GLUCURONIDASE; FUNGAL POLYSACCHARIDE; GLUCURONIC ACID; IDURONIC ACID; RHAMNOSE; ULVAN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; ESCHERICHIA COLI; MOLECULAR CLONING; NONHUMAN; NONLABENS ULVANIVORANS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STEREOCHEMISTRY; ULVA;

BIODEGRADATION; CRYSTAL STRUCTURE; ENZYME CATALYSIS; GH105; GLYCOSIDE HYDROLASES; POLYSACCHARIDE; ULVAN;

BACTERIAL PROTEINS; FLAVOBACTERIACEAE; GLYCOSIDE HYDROLASES; HYDROLYSIS; KINETICS; POLYSACCHARIDES; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84896852946     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.537480     Document Type: Article

References (40)

1. Gao, S., Chen, X., Yi, Q., Wang, G., Pan, G., Lin, A., and Peng, G. (2010) A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. Plos ONE 5, 1-7
2. Lahaye, M., and Robic, A. (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8, 1765-1774 (Pubitemid 47017986)
3. Percival, E., and McDowell, R. H. (1967) Chemistry and enzymology of marine algal polysaccharides, Academic Press Inc., London
4. Quemener, B., Lahaye, M., and Bobin-Dubigeon, C. (1997) Sugar determination in ulvans by a chemical-enzymatic method coupled to high performance anion exchange chromatography. J. Appl. Phycol. 9, 179-188 (Pubitemid 27372454)
5. Ray, B., and Lahaye, M. (1995) Cell wall polysaccharides from the marine green alga Ulva "rigida" (Ulvales, Chlorophyta). Extraction and chemical composition. Carbohydr. Res. 274, 313-318
6. Lahaye, M., Brunel, M., and Bonnin, E. (1997) Fine chemical structure analysis of oligosaccharides produced by an ulvan-lyase degradation of the water-soluble cell-wall polysaccharides from Ulva sp. (Ulvales, Chlorophyta). Carbohydr. Res. 304, 325-333 (Pubitemid 28015100)
7. Robic, A., Rondeau-Mouro, C., Sassi, J. F., Lerat, Y., and Lahaye, M. (2009) Structure and interactions of ulvan in the cell wall of the marine green algae Ulva rotundata (Ulvales, Chlorophyta). Carbohydr. Polym. 77, 206-216
8. Robic, A., Sassi J. F., Dion, P., Lerat, Y., and Lahaye, M. (2009) Seasonal variability of physicochemical and rheological properties of ulvan in two Ulva species from the Brittany coast. J. Phycol. 45, 962-973
9. Robic, A., Sassi, J.-F., and Lahaye, M. (2008) Impact of stabilization treatments of the green seaweed Ulva rotundata (Chlorophyta) on the extraction yield, the physic-chemical and rheological properties of ulvan. Carbohydr. Polym. 74, 344-352
10. Barbeyron, T., Lerat, Y., Sassi, J.-F., Le Panse, S., Helbert, W., and Collén, P. N. (2011) Persicivirga ulvanivorans sp. nov., a marine member of the family Flavobacteriaceae that degrades ulvan from green algae. Int. J. Syst. Evol. Microbiol. 61, 1899-1905
11. Nyvall Collén, P., Sassi, J.-F., Rogniaux, H., Marfaing, H., and Helbert, W. (2011) Ulvan lyases isolated from the Flavobacteria Persicivirga ulvanivorans are the first members of a new polysaccharide lyase family. J. Biol. Chem. 286, 42063-42071
12. Yi, H., and Chun, J. (2012) Unification of the genera Nonlabens, Persicivirga, Sandarakinotalea, and Stenothermobacter into a single emended genus, Nonlabens, and description of Nonlabens agnitus sp. nov. Syst. Appl. Microbiol. 35, 150-155
13. Boutachfaiti, R., Pheulpin, P., Courtois, B., and Courtois-Sambourg, J. (2009) Method for enzyme cleavage of polysaccharides derived from algae. WO 2009/016275 A2
14. Garron, M.-L., and Cygler, M. (2010) Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology 20, 1547-1573
15. Yip, V. L., and Withers, S. G. (2006) Breakdown of oligosaccharides by the process of elimination. Curr. Opin. Chem. Biol. 10, 147-155
16. Itoh, T., Akao, S., Hashimoto, W., Mikami, B., and Murata, K. (2004) Crystal structure of unsaturated glucuronyl hydrolase, responsible for the degradation of glycosaminoglycan, from Bacillus sp. GL1 at 1.8 Å resolution. J. Biol. Chem. 279, 31804-31812 (Pubitemid 39037853)
17. Maruyama, Y., Nakamichi, Y., Itoh, T., Mikami, B., Hashimoto, W., and Murata, K. (2009) Substrate specificity of streptococcal unsaturated glucuronyl hydrolases for sulfated glycosaminoglycan. J. Biol. Chem. 284, 18059-18069
18. Cantarel B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The carbohydrate-active EnZymes database (CAZy). An expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
19. Itoh, T., Ochiai, A., Mikami, B., Hashimoto, W., and Murata, K. (2006) Structure of unsaturated rhamnogalacturonyl hydrolase complexed with substrate. Biochem. Biophys. Res. Commun. 347, 1021-1029 (Pubitemid 44118218)
20. Itoh, T., Ochiai, A., Mikami, B., Hashimoto, W., and Murata, K. (2006) A novel glycoside hydrolase family 105. The structure of family 105 unsaturated rhamnogalacturonyl hydrolase complexed with a disaccharide in comparison with family 88 enzyme complexed with the disaccharide. J. Mol. Biol. 360, 573-585 (Pubitemid 43975105)
21. Jongkees, S. A., and Withers, S. G. (2011) Glycoside cleavage by a new mechanism in unsaturated glucuronyl hydrolases. J. Am. Chem. Soc. 133, 19334-19337
22. Liu, Y. G., and Whittier, R. F. (1995) Thermal asymmetric interlaced PCR. Automatable amplification and sequencing of insert end fragments from PI and YAC Clones for chromosome walking. Genomics 25, 674-681
23. Liu, Y. G., Mitsukawa, N., Oosumi, T., and Whittier, R. F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457-463
24. Korf, U., Kohl, T., van der Zandt, H., Zahn, R., Schleeger, S., Ueberle, B., Wandschneider, S., Bechtel, S., Schnölzer, M., Ottleben, H., Wiemann, S., and Poustka, A. (2005) Large scale protein expression for proteome research. Proteomics 5, 3571-3580 (Pubitemid 41393290)
25. Studier, F. W. (2005) Protein production by auto-induction in high-density shaking cultures. Protein Expr. Purif. 41, 207-234
26. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
27. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
28. Zhang K. Y., Cowtan, K., Main, P. (1997) Combining constraints for electron-density modification. Methods Enzymol. 277, 53-64 (Pubitemid 27390916)
29. Perrakis, A., Sixma, T. K., Wilson, K. S., and Lamzin, V. S. (1997) wARP. Improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models. Acta Crystallogr. D Biol. Crystallogr. 53, 448-455 (Pubitemid 27340643)
30. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
31. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
32. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992) The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282
33. Ward, J. H., Jr. (1963) Hierarchical grouping to optimize an objective function. J. Am. Statist. Assoc. 58, 236-244
34. Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., and Madden, T. L. (2008) NCBI BLAST. A better web interface. Nucleic Acids Res. 36, W5-W9
35. Lahaye, M., Inizan F., and Vigouroux, J. (1998)NMRanalysis of the chemical structure of ulvan and of ulvan-boron complex formation. Carbohydr. Polym. 36, 239-249 (Pubitemid 128399596)
36. Holm, L., and Rosenström, P. (2010) Dali server. Conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
37. Hashimoto, W., Itoh, T., Maruyama, Y., Mikami, B., and Murata, K. (2007) Hydration of vinyl ether groups by unsaturated glycoside hydrolases and their role in bacterial pathogenesis. Int. Microbiol. 10, 233-243 (Pubitemid 351214577)
38. Derrien, M., Vaughan E. E., Plugge, C. M., and de Vos, W. M. (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 54, 1469-1476 (Pubitemid 39359958)
39. Han, C., Spring, S., Lapidus, A., Del Rio, T. G., Tice, H., Copeland, A., Cheng, J. F., Lucas, S., Chen, F., Nolan, M., Bruce, D., Goodwin, L., Pitluck, S., Ivanova, N., Mavromatis, K., Mikhailova, N., Pati, A., Chen, A., Palaniappan, K., Land, M., Hauser, L., Chang, Y. J., Jeffries, C. C., Saunders, E., Chertkov, O., Brettin, T., Göker, M., Rohde, M., Bristow, J., Eisen, J. A., Markowitz, V., Hugenholtz, P., Kyrpides, N. C., Klenk, H. P., Detter, J. C. (2009) Complete genome sequence of Pedobacter heparinus type strain (HIM 762-3). Stand. Genomic Sci. 1, 54-62
40. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript. Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31, 3320-3323