Discovery and structural characterization of a novel glycosidase family of marine origin

Environmental Microbiology

Volumn 13, Issue 5, 2011, Pages 1253-1270

  Rebuffet, Etienne ^a,b,d   Groisillier, Agnès ^a,b   Thompson, Andrew ^c   Jeudy, Alexandra ^a,b   Barbeyron, Tristan ^a,b   Czjzek, Mirjam ^a,b   Michel, Gurvan ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c SYNCHROTRON SOLEIL   (France)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; BACTERIAL PROTEIN; GALACTOSIDASE; GALACTOSIDE; ZINC;

ARTICLE; BIOLOGY; CHEMISTRY; ENZYMOLOGY; FLAVOBACTERIACEAE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN TERTIARY STRUCTURE;

AGAR; BACTERIAL PROTEINS; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; FLAVOBACTERIACEAE; GALACTOSIDASES; GALACTOSIDES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; ZINC;

ALGAE; BACTERIA (MICROORGANISMS); FUNGI; PISCES; ZOBELLIA GALACTANIVORANS;

EID: 79955037032     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02426.x     Document Type: Article

References (98)

1. Alberto, F., Bignon, C., Sulzenbacher, G., Henrissat, B., and Czjzek, M. (2004) The three-dimensional structure of invertase (beta-fructosidase) from Thermotoga maritima reveals a bimodular arrangement and an evolutionary relationship between retaining and inverting glycosidases. J Biol Chem 279: 18903-18910.
2. Allouch, J., Jam, M., Helbert, W., Barbeyron, T., Kloareg, B., Henrissat, B., and Czjzek, M. (2003) The three-dimensional structures of two beta-agarases. J Biol Chem 278: 47171-47180.
3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
4. Andrykovitch, G., and Marx, I. (1988) Isolation of a new polysaccharide-digesting bacterium from a salt marsh. Appl Environ Microbiol 54: 1061-1062.
5. Auld, D.S. (2001) Zinc coordination sphere in biochemical zinc sites. Biometals 14: 271-313.
6. Azam, F., and Malfatti, F. (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 782-791.
7. Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A., and Thingstad, F. (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10: 257-263.
8. Barbeyron, T., Michel, G., Potin, P., Henrissat, B., and Kloareg, B. (2000) Iota-carrageenases constitute a novel family of glycoside hydrolases, unrelated to that of kappa-carrageenases. J Biol Chem 275: 35499-35505.
9. 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 [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol 51: 985-997.
10. Bauer, M., Kube, M., Teeling, H., Richter, M., Lombardot, T., Allers, E., etal. (2006) Whole genome analysis of the marine Bacteroidetes 'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter. Environ Microbiol 8: 2201-2213.
11. Bibb, M.J., Jones, G.H., Joseph, R., Buttner, M.J., and Ward, J.M. (1987) The agarase gene (dag A) of Streptomyces coelicolor A3(2): affinity purification and characterization of the cloned gene product. J Gen Microbiol 133: 2089-2096.
12. Burkepile, D.E., and Hay, M.E. (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci USA 105: 16201-16206.
13. 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.
14. Clements, K.D., and Bullivant, S. (1991) An unusual symbiont from the gut of surgeonfishes may be the largest known prokaryote. J Bacteriol 173: 5359-5362.
15. Colin, S., Deniaud, E., Jam, M., Descamps, V., Chevolot, Y., Kervarec, N., etal. (2006) Cloning and biochemical characterization of the fucanase FcnA: definition of a novel glycoside hydrolase family specific for sulfated fucans. Glycobiology 16: 1021-1032.
16. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763.
17. Costa-Ramos, C., and Rowley, A.F. (2004) Effect of extracellular products of Pseudoalteromonas atlantica on the edible crab Cancer pagurus. Appl Environ Microbiol 70: 729-735.
18. Cowtan, K., and Main, P. (1998) Miscellaneous algorithms for density modification. Acta Crystallogr D 54: 487-493.
19. Crump, B.C., and Koch, E.W. (2008) Attached bacterial populations shared by four species of aquatic angiosperms. Appl Environ Microbiol 74: 5948-5957.
20. Dabin, J., Jam, M., Czjzek, M., and Michel, G. (2008) Expression, purification, crystallization and preliminary X-ray analysis of the polysaccharide lyase RB5312 from the marine planctomycete Rhodopirellula baltica. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 224-227.
21. Day, D.F., and Yaphe, W. (1975) Enzymatic hydrolysis of agar: purification and characterization of neoagarobiose hydrolase and p-nitrophenyl alpha-galactoside hydrolase. Can J Microbiol 21: 1512-1518.
22. DeLong, E.F., Franks, D.G., and Alldredge, A.L. (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38: 924-934.
23. Duckworth, M., and Yaphe, W. (1970) Thin-layer chromatographic analysis of enzymic hydrolysates of agar. J Chromatogr 49: 482-487.
24. van den Elsen, J.M., Kuntz, D.A., and Rose, D.R. (2001) Structure of Golgi alpha-mannosidase II: a target for inhibition of growth and metastasis of cancer cells. EMBO J 20: 3008-3017.
25. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60: 2126-2132.
26. Fandino, L.B., Riemann, L., Steward, G.F., Long, R.A., and Azam, F. (2003) Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquat Microb Ecol 23: 119-130.
27. Flament, D., Barbeyron, T., Jam, M., Potin, P., Czjzek, M., Kloareg, B., and Michel, G. (2007) Alpha-agarases define a new family of glycoside hydrolases, distinct from beta-agarase families. Appl Environ Microbiol 73: 4691-4694.
28. Fox, B.G., Goulding, C., Malkowski, M.G., Stewart, L., and Deacon, A. (2008) Structural genomics: from genes to structures with valuable materials and many questions in between. Nat Methods 5: 129-132.
29. Fuerst, J.A. (2005) Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 59: 299-328.
30. Gasparic, A., Martin, J., Daniel, A.S., and Flint, H.J. (1995) A xylan hydrolase gene cluster in Prevotella ruminicola B(1)4: sequence relationships, synergistic interactions, and oxygen sensitivity of a novel enzyme with exoxylanase and beta-(1, 4)-xylosidase activities. Appl Environ Microbiol 61: 2958-2964.
31. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D., and Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy Server. In The Proteomics Protocols Handbook. Walker, J.M. (ed.). Totowa, NJ, USA: Totowa, pp. 571-607.
32. Glöckner, F.O., and Joint, I. (2010) Marine microbial genomics in Europe: current status and perspectives. Microb Biotechnol 3: 523-530.
33. Glöckner, F.O., Kube, M., Bauer, M., Teeling, H., Lombardot, T., Ludwig, W., etal. (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100: 8298-8303.
34. Gomez-Pereira, P.R., Fuchs, B.M., Alonso, C., Oliver, M.J., van Beusekom, J.E., and Amann, R. (2010) Distinct flavobacterial communities in contrasting water masses of the north Atlantic Ocean. ISME J 4: 472-487.
35. 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.
36. Groisillier, A., Herve, C., Jeudy, A., Rebuffet, E., Pluchon, P.F., Chevolot, Y., etal. (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.
37. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
38. 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.
39. Hieu, C.X., Voigt, B., Albrecht, D., Becher, D., Lombardot, T., Glöckner, F.O., etal. (2008) Detailed proteome analysis of growing cells of the planctomycete Rhodopirellula baltica SH1T. Proteomics 8: 1608-1623.
40. Hoagland, K.D., Rosowski, J.R., Gretz, M.R., and Roemer, S.C. (1993) Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J Phycol 29: 537-566.
41. Jam, M., Flament, D., Allouch, J., Potin, P., Thion, L., Kloareg, B., etal. (2005) The endo-beta-agarases AgaA and AgaB from the marine bacterium Zobellia galactanivorans: two paralogue enzymes with different molecular organizations and catalytic behaviours. Biochem J 385: 703-713.
42. Juncker, A.S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H., and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12: 1652-1662.
43. Kabsch, W. (2010) Xds. Acta Crystallogr D 66: 125-132.
44. 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.
45. Kelley, L.A., and Sternberg, M.J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
46. Kidby, D.K., and Davidson, D.J. (1973) A convenient ferricyanide estimation of reducing sugars in the nanomole range. Anal Biochem 55: 321-325.
47. Kirchman, D.L. (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39: 91-100.
48. Kloareg, B., and Quatrano, R.S. (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 26: 259-315.
49. Kumar, S., Tamura, K., and Nei, M. (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150-163.
50. Kunin, V., Raes, J., Harris, J.K., Spear, J.R., Walker, J.J., Ivanova, N., etal. (2008) Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol Syst Biol 4: 198.
51. Kurokawa, K., Itoh, T., Kuwahara, T., Oshima, K., Toh, H., Toyoda, A., etal. (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14: 169-181.
52. de La Fortelle, E., and Bricogne, G. (1997) Maximum-likelihood heavy-atom parameter refinement in MIR and MAD methods. Methods Enzymol 276: 472-494.
53. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. (1993) PROCHECK. J Appl Crystallogr 26: 283-291.
54. Lee, S., Lee, J.Y., Ha, S.C., Jung, J., Shin, D.H., Kim, K.H., and Choi, I.G. (2009) Crystallization and preliminary X-ray analysis of neoagarobiose hydrolase from Saccharophagus degradans 2-40. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 1299-1301.
55. 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.
56. Manrique, J., and Jensen, H.H. (2001) Spanish household demand for seafood. J Agric Econ 52: 23-37.
57. Marianayagam, N.J., Sunde, M., and Matthews, J.M. (2004) The power of two: protein dimerization in biology. Trends Biochem Sci 29: 618-625.
58. Matthews, B.W. (1968) Solvent content of protein crystals. J Mol Biol 33: 491-497.
59. Medigue, C., Krin, E., Pascal, G., Barbe, V., Bernsel, A., Bertin, P.N., etal. (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15: 1325-1335.
60. Medina, F.X. (2005) Food Culture in Spain. Westport Connecticut, London: Greenwood Press.
61. Michel, G., Barbeyron, T., Flament, D., Vernet, T., Kloareg, B., and Dideberg, O. (1999) Expression, purification, crystallization and preliminary X-ray analysis of the kappa-carrageenase from Pseudoalteromonas carrageenovora. Acta Crystallogr D 55: 918-920.
62. Michel, G., Flament, D., Barbeyron, T., Vernet, T., Kloareg, B., and Dideberg, O. (2000) Expression, purification, crystallization and preliminary X-ray analysis of the iota-carrageenase from Alteromonas fortis. Acta Crystallogr D 56: 766-768.
63. 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.
64. Michel, G., Tonon, T., Scornet, D., Cock, J.M., and Kloareg, B. (2010a) 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.
65. Michel, G., Tonon, T., Scornet, D., Cock, J.M., and Kloareg, B. (2010b) 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.
66. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53: 240-255.
67. Navarro, D.A., and Stortz, C.A. (2005) Modeling ring puckering in strained systems: application to 3, 6-anhydroglycosides. Carbohydr Res 340: 2030-2038.
68. Nielsen, H., Brunak, S., and von Heijne, G. (1999) Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng 12: 3-9.
69. Nurizzo, D., Turkenburg, J.P., Charnock, S.J., Roberts, S.M., Dodson, E.J., McKie, V.A., etal. (2002) Cellvibrio japonicus alpha-l-arabinanase 43A has a novel five-blade beta-propeller fold. Nat Struct Biol 9: 665-668.
70. Pape, T., and Schneider, T.R. (2004) HKL2MAP: a graphical user interface for macromolecular phasing with shelx programs. J Appl Crystallogr 37: 843-844.
71. 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 53: 448-455.
72. Potin, P., Richard, C., Rochas, C., and Kloareg, B. (1993) Purification and characterization of the alpha-agarase from Alteromonas agarlyticus (Cataldi) comb. nov., strain GJ1B. Eur J Biochem 214: 599-607.
73. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., etal. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
74. Rebuffet, E., Barbeyron, T., Jeudy, A., Jam, M., Czjzek, M., and Michel, G. (2010) Identification of catalytic residues and mechanistic analysis of family GH82 iota-carrageenases. Biochemistry 49: 7590-7599.
75. Rochas, C., Potin, P., and Kloareg, B. (1994) NMR spectroscopic investigation of agarose oligomers produced by an alpha-agarase. Carbohydr Res 253: 69-77.
76. Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., etal. (2007) The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5: e77.
77. Seshadri, R., Kravitz, S.A., Smarr, L., Gilna, P., and Frazier, M. (2007) CAMERA: a community resource for metagenomics. PLoS Biol 5: e75.
78. Sheldrick, G.M. (2008) A short history of SHELX. Acta Crystallogr A 64: 112-122.
79. Stanier, R.Y. (1941) Studies on marine agar-digesting bacteria. J Bacteriol 42: 527-559.
80. Staufenberger, T., Thiel, V., Wiese, J., and Imhoff, J.F. (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64: 65-77.
81. Studier, F.W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
82. Sugano, Y., Kodama, H., Terada, I., Yamazaki, Y., and Noma, M. (1994) Purification and characterization of a novel enzyme, alpha-agarooligosaccharide hydrolase (alpha-NAOS hydrolase), from a marine bacterium, Vibrio sp. strain JT0107. J Bacteriol 176: 6812-6818.
83. Suzuki, H., Sawai, Y., Suzuki, T., and Kawai, K. (2002) Purification and characterization of an extracellular alpha-neoagarooligosaccharide hydrolase from Bacillus sp. MK03. J Biosci Bioeng 93: 456-463.
84. 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.
85. Thrash, J.C., Cho, J.C., Vergin, K.L., Morris, R.M., and Giovannoni, S.J. (2010) Genome sequence of Lentisphaera araneosa HTCC2155T, the type species of the order Lentisphaerales in the phylum Lentisphaerae. J Bacteriol 192: 2938-2939.
86. Tichelaar, G.M., and Vruggink, H. (1975) A survey of fungi and actinomycetes colonizing the newly reclaimed soil of the polder Zuidelijk Flevoland. Plant Soil 42: 241-253.
87. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., etal. (2009) A core gut microbiome in obese and lean twins. Nature 457: 480-485.
88. Van der Meulen, H.J., and Harder, W. (1976) Characterization of the neoagarotetra-ase and neoagarobiase of Cytophaga flevensis. Antonie Van Leeuwenhoek 42: 81-94.
89. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., etal. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74.
90. Vocadlo, D.J., and Davies, G.J. (2008) Mechanistic insights into glycosidase chemistry. Curr Opin Chem Biol 12: 539-555.
91. Voget, S., Leggewie, C., Uesbeck, A., Raasch, C., Jaeger, K.E., and Streit, W.R. (2003) Prospecting for novel biocatalysts in a soil metagenome. Appl Environ Microbiol 69: 6235-6242.
92. Wallner, S.R., Bauer, M., Würdemann, C., Wecker, P., Glöckner, F.O., and Faber, K. (2005) Highly enantioselective sec-Alkylsulfatase activity of the marine Planctomycete Rhodopirellula baltica shows retention of configuration. Angew Chem Int Ed Engl 44: 2-4.
93. Watson, J.D., Laskowski, R.A., and Thornton, J.M. (2005) Predicting protein function from sequence and structural data. Curr Opin Struct Biol 15: 275-284.
94. Wecker, P., Klockow, C., Ellrott, A., Quast, C., Langhammer, P., Harder, J., and Glöckner, F.O. (2009) Transcriptional response of the model planctomycete Rhodopirellula baltica SH 1T to changing environmental conditions. BMC Genomics 10: 410.
95. Wecker, P., Klockow, C., Schüler, M., Dabin, J., Michel, G., and Glöckner, F.O. (2010) Life cycle analysis of the model organism Rhodopirellula baltica SH 1T by transcriptome studies. Microb Biotechnol 3: 583-594.
96. Weinberger, F., Richard, C., Kloareg, B., Kashman, Y., Hoppe, H.-G., and Friedlander, M. (2001) Structure-activity relationships of oligoagar elicitors toward Gracilaria conferta (Rhodophyta). J Phycol 37: 418-426.
97. Yang, S., Cho, S.S., Levy, Y., Cheung, M.S., Levine, H., Wolynes, P.G., and Onuchic, J.N. (2004) Domain swapping is a consequence of minimal frustration. Proc Natl Acad Sci USA 101: 13786-13791.
98. Zhong, Z., Toukdarian, A., Helinski, D., Knauf, V., Sykes, S., Wilkinson, J.E., etal. (2001) Sequence analysis of a 101-kilobase plasmid required for agar degradation by a Microscilla isolate. Appl Environ Microbiol 67: 5771-5779.