The β-glucanase ZgLamA from zobellia galactanivorans evolved a bent active site adapted for efficient degradation of algal laminarin

Journal of Biological Chemistry

Volumn 289, Issue 4, 2014, Pages 2027-2042

  Labourel, Aurore ^a,b   Jam, Murielle ^a,b   Jeudy, Alexandra ^a,b   Hehemann, Jan Hendrik ^a,b,c   Czjzek, Mirjam ^a,b   Michel, Gurvan ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c Massachusetts Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A-CARBON; ACTIVE SITE; GLUCANASE; LAMINARINS; MARINE BACTERIUM;

BIOCHEMISTRY; BIOLOGY;

ENZYME ACTIVITY;

BACTERIAL ENZYME; BETA GLUCONASE ZOBELLIA GALACTANIVORANS LAMA; ENDO 1,3 BETA GLUCANASE; GLUCAN; LAMINARAN; MIXED LINKED GLUCAN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; BETA SHEET; BIOCHEMICAL COMPOSITION; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; HYDROLYSIS; MARINE BACTERIUM; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; ZOBELLIA GALACTANIVORANS;

1,3-BETA-GLUCAN; ALGAE; CARBOHYDRATE METABOLISM; CRYSTAL STRUCTURE; FAMILY GH16; GLYCOSIDE HYDROLASES; LAMINARINASE; MARINE BACTERIA; OLIGOSACCHARIDE;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; FLAVOBACTERIACEAE; GLUCAN 1,3-BETA-GLUCOSIDASE; POLYSACCHARIDES; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84893104437     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.538843     Document Type: Article

References (57)

1. Stone, B. A. (2009) Chemistry of β-glucans. In Chemistry, Biochemistry and Biology of (1->3)- β-Glucans and Related Polysaccharides (Bacic, A., Fincher, G. B., and Stone, B. A., eds) pp. 5-46, Academic Press, Orlando, FL
2. Michel, G., Tonon, T., Scornet, D., Cock, J. M., and Kloareg, B. (2010) Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus. Insights into the origin and evolution of storage carbohydrates in eukaryotes. New Phytol. 188, 67-81
3. Clarke, A. E., and Stone, B. A. (1960) Structure of the paramylon from Euglena gracilis. Biochim. Biophys. Acta 44, 161-163
4. Janse, I., van Rijssel, M., van Hall, P. J., Gerwig, G. J., Gottschal, J. G., and Prius, R. A. (1996) The storage glucan of Phaeocystis globosa (Prymnesiophyceae) cells. J. Phycol. 32, 382-387
5. Hirokawa, Y., Fujiwara, S., Suzuki, M., Akiyama, T., Sakamoto, M., Kobayashi, S., and Tsuzuki, M. (2008) Structural and physiological studies on the storage β-polyglucan of haptophyte Pleurochrysis haptonemofera. Planta 227, 589-599
6. Beattie, A., Hirst, E. L., and Percival, E. (1961) Studies on the metabolism of the Chrysophyceae. Comparative structural investigations on leucosin (chrysolaminarin) separated from diatoms and laminarin from the brown algae. Biochem. J. 79, 531-537
7. Wang, M. C., and Bartnicki-Garcia, S. (1974) Mycolaminarans. Storage (1,3)- β-D-glucans from the cytoplasm of the fungus Phytophthora palmivora. Carbohydr. Res. 37, 331-338
8. Percival, E. G., and Ross, A. G. (1951) The constitution of laminarin. Part II. The soluble laminarin of Laminaria digitata. J. Chem. Soc. 720-726
9. Read, S. M., Currie, G., and Bacic, A. (1996) Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydr. Res. 281, 187-201
10. Michel, G., Tonon, T., Scornet, D., Cock, J. M., and Kloareg, B. (2010) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in eukaryotes. New Phytol. 188, 82-97
11. Smith, S. V. (1981) Marine Macrophytes as a Global Carbon Sink. Science 211, 838-840
12. Duarte, C. M., Middelburg, J. J., and Caraco, N. (2005) Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2, 1-8
13. Siegel, D. A., Doney, S. C., and Yoder, J. A. (2002) The North Atlantic spring phytoplankton bloom and Sverdrup's critical depth hypothesis. Science 296, 730-733
14. Cloern, J. E. (1996) Phytoplankton bloom dynamics in coastal ecosystems. A review with some general lessons from sustained investigation of San Francisco Bay, California. Rev. Geophys. 34, 127-168
15. DiTullio, G. R., Grebmeier, J. M., Arrigo, K. R., Lizotte, M. P., Robinson, D. H., Leventer, A., Barry, J. P., VanWoert, M. L., and Dunbar, R. B. (2000) Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica. Nature 404, 595-598
16. Alderkamp, A. C., van Rijssel, M., and Bolhuis, H. (2007) Characterization of marine bacteria and the activity of their enzyme systems involved in degradation of the algal storage glucan laminarin. FEMS Microbiol. Ecol. 59, 108-117
17. Arnosti, C., Fuchs, B. M., Amann, R., and Passow, U. (2012) Contrasting extracellular enzyme activities of particle-associated bacteria from distinct provinces of the North Atlantic Ocean. Front. Microbiol. 3, 425
18. Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., Kassabgy, M., Huang, S., Mann, A. J., Waldmann, J., Weber, M., Klindworth, A., Otto, A., Lange, J., Bernhardt, J., Reinsch, C., Hecker, M., Peplies, J., Bockelmann, F. D., Callies, U., Gerdts, G., Wichels, A., Wiltshire, K. H., Glöckner, F. O., Schweder, T., and Amann, R. (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608-611
19. Thomas, F., Hehemann, J. H., Rebuffet, E., Czjzek, M., and Michel, G. (2011) Environmental and gut bacteroidetes. The food connection. Front. Microbiol. 2, 93
20. Barbeyron, T., L'Haridon, S., Corre, E., Kloareg, B., and Potin, P. (2001) Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of. Int. J. Syst. Evol. Microbiol. 51, 985-997
21. 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
22. Rebuffet, E., Groisillier, A., Thompson, A., Jeudy, A., Barbeyron, T., Czjzek, M., and Michel, G. (2011) Discovery and structural characterization of a novel glycosidase family of marine origin. Environ. Microbiol. 13, 1253-1270
23. 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
24. Barbeyron, T., Michel, G., Potin, P., Henrissat, B., and Kloareg, B. (2000) -Carrageenases constitute a novel family of glycoside hydrolases, unrelated to that of-carrageenases. J. Biol. Chem. 275, 35499-35505
25. Rebuffet, E., Barbeyron, T., Jeudy, A., Jam, M., Czjzek, M., and Michel, G. (2010) Identification of catalytic residues and mechanistic analysis of family GH82-carrageenases. Biochemistry 49, 7590-7599
26. Thomas, F., Barbeyron, T., Tonon, T., Génicot, S., Czjzek, M., and Michel, G. (2012) Characterization of the first alginolytic operons in a marine bacterium. From their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides. Environ. Microbiol. 14, 2379-2394
27. Thomas, F., Lundqvist, L. C., Jam, M., Jeudy, A., Barbeyron, T., Sandström, C., Michel, G., and Czjzek, M. (2013) Comparative characterization of two marine alginate lyases from Zobellia galactanivorans reveals distinct modes of action and exquisite adaptation to their natural substrate. J. Biol. Chem. 288, 23021-23037
28. Groisillier, A., Hervé, C., Jeudy, A., Rebuffet, E., Pluchon, P. F., Chevolot, Y., Flament, D., Geslin, C., Morgado, I. M., Power, D., Branno, M., Moreau, H., Michel, G., Boyen, C., and Czjzek, M. (2010) MARINE-EXPRESS. Taking advantage of high throughput cloning and expression strategies for the post-genomic analysis of marine organisms. Microb. Cell Fact. 9, 45
29. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein. Expr. Purif. 41, 207-234
30. Kidby, D. K., and Davidson, D. J. (1973) A convenient ferricyanide estimation of reducing sugars in the nanomole range. Anal. Biochem. 55, 321-325
31. Jackson, P. (1990) The use of polyacrylamide-gel electrophoresis for the high-resolution separation of reducing saccharides labelled with the fluorophore 8-aminonaphthalene-1,3,6-trisulphonic acid. Detection of picomolar quantities by an imaging system based on a cooled charge-coupled device. Biochem. J. 270, 705-713
32. Leslie, A. G. (2006) The integration of macromolecular diffraction data. Acta Crystallogr. D 62, 48-57
33. Weiss, M. S., Sicker, T., Djinovic-Carugo, K., and Hilgenfeld, R. (2001) On the routine use of soft x-rays in macromolecular crystallography. Acta Crystallogr. D 57, 689-695
34. Vagin, A., and Teplyakov, A. (1997) MOLREP. An automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025
35. Bleicher, L., Prates, E. T., Gomes, T. C., Silveira, R. L., Nascimento, A. S., Rojas, A. L., Golubev, A., Martínez, L., Skaf, M. S., and Polikarpov, I. (2011) Molecular basis of the thermostability and thermophilicity of laminarinases. X-ray structure of the hyperthermostable laminarinase from Rhodothermus marinus and molecular dynamics simulations. J. Phys. Chem. B 115, 7940-7949
36. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D 66, 486-501
37. Vagin, A. A., Steiner, R. A., Lebedev, A. A., Potterton, L., McNicholas, S., Long, F., and Murshudov, G. N. (2004) REFMAC5 dictionary. Organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D 60, 2184-2195
38. 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
39. Katoh, K., and Standley, D. M. (2013) MAFFT multiple sequence alignment software version 7. Improvements in performance and usability. Mol. Biol. Evol. 30, 772-780
40. Vasur, J., Kawai, R., Andersson, E., Igarashi, K., Sandgren, M., Samejima, M., and Ståhlberg, J. (2009) X-ray crystal structures of Phanerochaete chrysosporium Laminarinase 16A in complex with products from lichenin and laminarin hydrolysis. FEBS J. 276, 3858-3869
41. Tsai, L. C., Shyur, L. F., Cheng, Y. S., and Lee, S. H. (2005) Crystal structure of truncated Fibrobacter succinogenes 1,3-1,4-β-D-glucanase in complex with β-1,3-1,4-cellotriose. J. Mol. Biol. 354, 642-651
42. Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002) MAFFT. A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066
43. 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
44. Wang, Y. K., Zhao, G. Y., Li, Y., Chen, X. L., Xie, B. B., Su, H. N., Lv, Y. H., He, H. L., Liu, H., Hu, J., Zhou, B. C., and Zhang, Y. Z. (2010) Mechanistic insight into the function of the C-terminal PKD domain of the collagenolytic serine protease deseasin MCP-01 from deep sea Pseudoalteromonas sp. SM9913. Binding of the PKD domain to collagen results in collagen swelling but does not unwind the collagen triple helix. J. Biol. Chem. 285, 14285-14291
45. Viladot, J. L., de Ramon, E., Durany, O., and Planas, A. (1998) Probing the mechanism of Bacillus 1,3-1,4-β-D-glucan 4-glucanohydrolases by chemical rescue of inactive mutants at catalytically essential residues. Biochemistry 37, 11332-11342
46. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559
47. Johansson, P., Brumer, H., 3rd, Baumann, M. J., Kallas, A. M., Henriksson, H., Denman, S. E., Teeri, T. T., and Jones, T. A. (2004) Crystal structures of a poplar xyloglucan endotransglycosylase reveal details of transglycosylation acceptor binding. Plant Cell 16, 874-886
48. Baumann, M. J., Eklöf, J. M., Michel, G., Kallas, A. M., Teeri, T. T., Czjzek, M., and Brumer, H., 3rd (2007) Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases. Biological implications for cell wall metabolism. Plant Cell 19, 1947-1963
49. Michel, G., Chantalat, L., Duee, E., Barbeyron, T., Henrissat, B., Kloareg, B., and Dideberg, O. (2001) The-carrageenase of P. carrageenovora features a tunnel-shaped active site.Anovel insight in the evolution of Clan-B glycoside hydrolases. Structure 9, 513-525
50. Keitel, T., Meldgaard, M., and Heinemann, U. (1994) Cation binding to a Bacillus (1,3-1,4)- β-glucanase. Geometry, affinity and effect on protein stability. Eur. J. Biochem. 222, 203-214
51. Sulzenbacher, G., Driguez, H., Henrissat, B., Schülein, M., and Davies, G. J. (1996) Structure of the Fusarium oxysporum endoglucanase I with a nonhydrolyzable substrate analogue. Substrate distortion gives rise to the preferred axial orientation for the leaving group. Biochemistry 35, 15280-15287
52. Krah, M., Misselwitz, R., Politz, O., Thomsen, K. K., Welfle, H., and Borriss, R. (1998) The laminarinase from thermophilic eubacterium Rhodothermus marinus. Conformation, stability, and identification of active site carboxylic residues by site-directed mutagenesis. Eur. J. Biochem. 257, 101-111
53. Woodward, J. R., Fincher, G. B., and Stone, B. A. (1983) Water-soluble (1→3), (1→4)- β-D-giucans from barley (Hordeum vulgate) endosperm. II. Fine structure. Carbohydr. Polym. 3, 207-225
54. Kawai, R., Igarashi, K., Yoshida, M., Kitaoka, M., and Samejima, M. (2006) Hydrolysis of β-1,3/1,6-glucan by glycoside hydrolase family 16 endo-1,3(4)- β-glucanase from the basidiomycete Phanerochaete chrysosporium. Appl. Microbiol. Biotechnol. 71, 898-906
55. Barbeyron, T., Gerard, A., Potin, P., Henrissat, B., and Kloareg, B. (1998) The-carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol. Biol. Evol. 15, 528-537
56. Eklöf, J. M., Shojania, S., Okon, M., McIntosh, L. P., and Brumer, H. (2013) Structure-function analysis of a broad specificity Populus trichocarpa endo-β-glucanase reveals an evolutionary link between bacterial licheninases and plant XTH gene products. J. Biol. Chem. 288, 15786-15799
57. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript. Extracting and rendering sequence and three-dimensional information from atomic structures of proteins. Nucleic Acids Res. 31, 3320-3323