Applied Microbiology and Biotechnology

, Volume 71, Issue 1, pp 23–33

Bioconversion of red seaweed galactans: a focus on bacterial agarases and carrageenases

  • Gurvan Michel
  • Pi Nyval-Collen
  • Tristan Barbeyron
  • Mirjam Czjzek
  • William Helbert
Mini-Review

Abstract

Agars and carrageenans are 1,3-α-1,4-β-galactans from the cell walls of red algae, substituted by zero (agarose), one (κ-), two (ι-), or three (λ-carrageenan) sulfate groups per disaccharidic monomer. Agars, κ-, and ι-carrageenans auto-associate into crystalline fibers and are well known for their gelling properties, used in a variety of laboratory and industrial applications. These sulfated galactans constitute a crucial carbon source for a number of marine bacteria. These microorganisms secrete glycoside hydrolases specific for these polyanionic, insoluble polysaccharides, agarases and carrageenases. This article reviews the microorganisms involved in the degradation of agars and carrageenans, in their environmental and taxonomic diversity. We also present an overview on the biochemistry of the different families of galactanases. The structure–function relationships of the family GH16 β-agarases and κ-caraggeenases and of the family GH82 ι-carrageenases are discussed in more details. In particular, we examine how the active site topologies of these glycoside hydrolases influence their mode of action in heterogeneous phase. Finally, we discuss the next challenges in the basic and applied field of the galactans of red algae and of their related degrading microorganisms.

References

  1. Allouch J, Jam M, Helbert W, Barbeyron T, Kloareg B, Henrissat B, Czjzek M (2003) The three-dimensional structures of two beta-agarases. J Biol Chem 278:47171–47180Google Scholar
  2. Allouch J, Helbert W, Henrissat B, Czjzek M (2004) Parallel substrate binding sites in a beta-agarase suggest a novel mode of action on double-helical agarose. Structure 12:623–632Google Scholar
  3. Anderson NS, Campbell JW, Harding MM, Rees DA, Samuel JW (1969) X-ray diffraction studies of polysaccharide sulphates: double helix models for k- and i-carrageenans. J Mol Biol 45:85–99Google Scholar
  4. Antonopoulos A, Favetta P, Helbert W, Lafosse M (2005a) On-line liquid chromatography electrospray ionization mass spectrometry for the characterization of kappa- and iota-carrageenans. Application to the hybrid iota-/nu-carrageenans. Anal Chem 77:4125–4136Google Scholar
  5. Antonopoulos A, Hardouin J, Favetta P, Helbert W, Delmas AF, Lafosse M (2005b) Matrix-assisted laser desorption/ionisation mass spectrometry for the direct analysis of enzymatically digested kappa- iota- and hybrid iota/nu-carrageenans. Rapid Commun Mass Spectrom 19:2217–2226Google Scholar
  6. Aoki T, Araki T, Kitamikado M (1990) Purification and characterization of a novel beta-agarase from Vibrio sp. AP-2. Eur J Biochem 187:461–465Google Scholar
  7. Araki T, Hayakawa M, Lu Z, Karita S, Morishita T (1998) Purification and characterization of agarases from a marine bacterium, Vibrio sp. PO-303. J Mar Biotechnol 6:260–265Google Scholar
  8. Arnott S, Fulmer A, Scott WE, Dea IC, Moorhouse R, Rees DA (1974) The agarose double helix and its function in agarose gel structure. J Mol Biol 90:269–284Google Scholar
  9. Barbeyron T, Henrissat B, Kloareg B (1994) The gene encoding the kappa-carrageenase of Alteromonas carrageenovora is related to beta-1,3-1,4-glucanases. Gene 139:105–109Google Scholar
  10. Barbeyron T, Gerard A, Potin P, Henrissat B, Kloareg B (1998) The kappa-carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol Biol Evol 15:528–537Google Scholar
  11. Barbeyron T, Michel G, Potin P, Henrissat B, Kloareg B (2000) iota-Carrageenases constitute a novel family of glycoside hydrolases, unrelated to that of kappa-carrageenases. J Biol Chem 275:35499–35505Google Scholar
  12. Barbeyron T, L’Haridon S, Corre E, Kloareg B, Potin P (2001) Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (Zo Bell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol 51:985–997Google Scholar
  13. Bayley ST (1955) X-ray and infrared studies on carrageenin. Biochim Biophys Acta 17:194–205Google Scholar
  14. Belas R (1989) Sequence analysis of the agrA gene encoding beta-agarase from Pseudomonas atlantica. J Bacteriol 171:602–605Google Scholar
  15. Bellion C, Hamer G, Yaphe W (1982) The degradation of Eucheuma spinosum and Eucheuma cottonii carrageenans by ι-carrageenases and k-carrageenases from marine bacteria. Can J Microbiol 28:874–880Google Scholar
  16. Bellion C, Brigand G, Prome J-C, Welti D, Bociek S (1983) Identification et caractérisation des précurseurs biologiques des carraghénanes par spectroscopie de R.M.N.-13C. Carbohydr Res 119:31–48Google Scholar
  17. Bixler H (1996) Recent developments in manufacturing and marketing carrageenan. Hydrobiologia 326/327:35–37Google Scholar
  18. Bongaerts K, Reynaers H, Zanetti F, Paoletti S (1999) Equilibrium and nonequilibrium association processes of kappa-carrageenan in aqueous salt solutions. Macromolecules 32:675–682Google Scholar
  19. Buttner MJ, Fernley IM, Bibb MJ (1987) The agarase gene (dagA) of Streptomyces coelicolor (A3)2: nucleotide sequence and transcriptionnal analysis. Mol Gen Genet 209:101–109Google Scholar
  20. Craigie J (1990) Cell walls. In: Cole K, Sheath R (eds) Biology of the red algae. Cambridge Univ. Press, Cambridge, pp 221–257Google Scholar
  21. Cuppo F, Reynaers H, Paoletti S (2002) Association of kappa-carrageenan induced by Cs+ ions in iodide aqueous solution: a light scattering study. Macromolecules 35:539–547Google Scholar
  22. Davies GJ, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859Google Scholar
  23. Day DF, Yaphe W (1975) Enzymatic hydrolysis of agar: purification and characterization of neoagarobiose hydrolase and p-nitrophenyl alpha-galactoside hydrolase. Can J Microbiol 21:1512–1518Google Scholar
  24. De Ruiter G, Rudolph B (1997) Carrageenan biotechnology. Trends Food Sci Technol 8:389–395Google Scholar
  25. Divne C, Stahlberg J, Reinikainen T, Ruohonen L, Pettersson G, Knowles JK, Teeri TT, Jones TA (1994) The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science 265:524–528Google Scholar
  26. Ekborg NA, Gonzalez JM, Howard MB, Taylor LE, Hutcheson SW, Weiner RM (2005) Saccharophagus degradans gen. nov., sp. nov., a versatile marine degrader of complex polysaccharides. Int J Syst Evol Microbiol 55:1545–1549Google Scholar
  27. Erasmus JH, Cook PA, Coyne VE (1997) The role of bacteria in the digestion of seaweed by the abalone Haliotis midae. Aquaculture 155:377–386Google Scholar
  28. Ford SA, Atkins EDT (1989) New X-ray diffraction results from agarose: extended single helix structures and implications for gelation mechanism. Biopolymers 28:1345–1365Google Scholar
  29. Gauthier G, Gauthier M, Christen R (1995) Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (emended) and Pseudoalteromonas gen. nov., and proposal of twelve new species combinations. Int J Syst Bacteriol 45:755–761Google Scholar
  30. Glöckner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, Gade D, Beck A, Borzym K, Heitmann K, Rabus R, Schlesner H, Amann R, Reinhardt R (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100:8298–8303Google Scholar
  31. Gran HH (1902) Studien über meerebakterien. II. Über die hydrolyse des agars-agars durch ein neues enzym, die gelase. Bergens Museums Arb 2:1–16Google Scholar
  32. Greer CW (1984) A study of carrageenases from marine bacteria. Thèse de Doctorat. McGill University, Montreal, CanadaGoogle Scholar
  33. Greer CW, Yaphe W (1984a) Hybrid (iota–nu–kappa) carrageenan from Eucheuma nudum (Rhodophyta, Solieriaceae), identified using iota- and kappa-carrageenases and 13C-nuclear magnetic resonance spectroscopy. Bot Mar 27:479–484CrossRefGoogle Scholar
  34. Greer CW, Yaphe W (1984b) Purification and properties of iota-carrageenase from a marine bacterium. Can J Microbiol 30:1500–1506Google Scholar
  35. Groleau D, Yaphe W (1977) Enzymatic hydrolysis of agar: purification and characterization of beta-neoagarotetraose hydrolase from Pseudomonas atlantica. Can J Microbiol 23:672–679CrossRefGoogle Scholar
  36. Guenet JM, Brulet A, Rochas C (1993) Agarose chain conformation in the sol state by neutron scattering. Int J Biol Macromol 15:131–132Google Scholar
  37. Ha JC, Kim GT, Kim SK, Oh TK, Yu JH, Kong IS (1997) Beta-Agarase from Pseudomonas sp. W7: purification of the recombinant enzyme from Escherichia coli and the effects of salt on its activity. Biotechnol Appl Biochem 26:1–6Google Scholar
  38. Hahn M, Olsen O, Politz O, Borriss R, Heinemann U (1995) Crystal structure and site-directed mutagenesis of Bacillus macerans endo-1,3-1,4-beta-glucanase. J Biol Chem 270:3081–3088Google Scholar
  39. Henrissat B, Bairoch A (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316:695–696Google Scholar
  40. Humm HJ (1946) Marine agar digesting bacteria of the South Atlantic coast. Duke Univ Mar Stn Bull 3:43–75Google Scholar
  41. Jam M, Flament D, Allouch J, Potin P, Thion L, Kloareg B, Czjzek M, Helbert W, Michel G, Barbeyron T (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 385:703–713Google Scholar
  42. Janaswamy S, Chandrasekaran R (2002) Effect of calcium ions on the organization of iota-carrageenan helices: an X-ray investigation. Carbohydr Res 337:523–535Google Scholar
  43. Johansson P, Brumer H 3rd, Baumann MJ, Kallas AM, Henriksson H, Denman SE, Teeri TT, Jones TA (2004) Crystal structures of a poplar xyloglucan endotransglycosylase reveal details of transglycosylation acceptor binding. Plant Cell 16:874–886Google Scholar
  44. Johnston K, McCandless E (1973) Enzymatic hydrolysis of potassium chloride soluble fraction of carrageenan: properties of “λ-carrageenases” from Pseudomonas carrageenovora. Can J Microbiol 19:779–788Google Scholar
  45. Keitel T, Simon O, Borriss R, Heinemann U (1993) Molecular and active-site structure of a Bacillus 1,3-1,4-beta-glucanase. Proc Natl Acad Sci USA 90:5287–5291Google Scholar
  46. Kimura K, Masuda N, Iwasaki Y, Nakagawa Y, Kobayashi R, Usami S (1999) Purification and characterization of a novel β-agarase from an alkalophylic bacterium, Alteromonas sp. E-1. J Biosci Bioeng 87:436–441Google Scholar
  47. Kleywegt GJ, Zou JY, Divne C, Davies GJ, Sinning I, Stahlberg J, Reinikainen T, Srisodsuk M, Teeri TT, Jones TA (1997) The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6 Å resolution, and a comparison with related enzymes. J Mol Biol 272:383–397Google Scholar
  48. Kloareg B, Quatrano R (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315Google Scholar
  49. Knutsen S, Myslabodski D, Larsen B, Usov A (1994) A modified system of nomenclature for red algal galactans. Bot Mar 37:163–169CrossRefGoogle Scholar
  50. Koshland DE (1953) Stereochemistry and the mechanism of enzymatic reactions. Biol Rev Camb Philos Soc 28:416–436Google Scholar
  51. Leon O, Quintana L, Peruzzo G, Slebe JC (1992) Purification and properties of an extracellular agarase from Alteromonas sp. Strain C-1. Appl Environ Microbiol 58:4060–4063Google Scholar
  52. Lewin RA (1969) A classification of flexibacteria. J Gen Microbiol 58:189–206Google Scholar
  53. Mc Hugh DJ (2003) A guide to seaweed industry. In: FAO (ed) FAO fisheries technical paper no 441. FAO, Rome, ItalyGoogle Scholar
  54. McLean MW, Williamson FB (1979a) Glycosulphatase from Pseudomonas carrageenovora. Purification and some properties. Eur J Biochem 101:497–505Google Scholar
  55. McLean MW, Williamson FB (1979b) Kappa-Carrageenase from Pseudomonas carrageenovora. Eur J Biochem 93:553–558Google Scholar
  56. McLean MW, Williamson FB (1981) Neocarratetraose 4-O-monosulphate beta-hydrolase from Pseudomonas carrageenovora. Eur J Biochem 113:447–456Google Scholar
  57. Michel G, Chantalat L, Duee E, Barbeyron T, Henrissat B, Kloareg B, Dideberg O (2001a) The kappa-carrageenase of P. carrageenovora features a tunnel-shaped active site: a novel insight in the evolution of Clan-B glycoside hydrolases. Structure 9:513–525Google Scholar
  58. Michel G, Chantalat L, Fanchon E, Henrissat B, Kloareg B, Dideberg O (2001b) The iota-carrageenase of Alteromonas fortis. A beta-helix fold-containing enzyme for the degradation of a highly polyanionic polysaccharide. J Biol Chem 276:40202–40209Google Scholar
  59. Michel G, Helbert W, Kahn R, Dideberg O, Kloareg B (2003) The structural bases of the processive degradation of iota-carrageenan, a main cell wall polysaccharide of red algae. J Mol Biol 334:421–433Google Scholar
  60. Michel G, Pojasek K, Li Y, Sulea T, Linhardt RJ, Raman R, Prabhakar V, Sasisekharan R, Cygler M (2004) The structure of chondroitin B lyase complexed with glycosaminoglycan oligosaccharides unravels a calcium-dependent catalytic machinery. J Biol Chem 279:32882–32896Google Scholar
  61. Millane RP, Chandrasekaran R, Arnott S, Dea ICM (1988) The molecular structure of kappa-carrageenan and comparison with iota-carrageenan. Carbohydr Res 182:1–17Google Scholar
  62. Mori T (1943) The enzyme catalyzing the decomposition of mucilage of Chondrus ocellatus. III. Purification, unit determination, and distribution of the enzyme. J Agric Chem Soc Jpn 19:740–742Google Scholar
  63. Morrice LM, McLean MW, Long WF, Williamson FB (1983a) Beta-agarases I and II from Pseudomonas atlantica. Substrate specificities. Eur J Biochem 137:149–154Google Scholar
  64. Morrice LM, McLean MW, Williamson FB, Long WF (1983b) beta-Agarases I and II from Pseudomonas atlantica. Purifications and some properties. Eur J Biochem 135:553–558Google Scholar
  65. Morris ER, Rees DA, Robinson G (1980) Cation-specific aggregation of carrageenan helices: domain model of polymer gel structure. J Mol Biol 138:349–362Google Scholar
  66. Ohta Y, Hatada Y, Nogi Y, Li Z, Ito S, Horikoshi K (2004a) Cloning, expression, and characterization of a glycoside hydrolase family 86 beta-agarase from a deep-sea Microbulbifer-like isolate. Appl Microbiol Biotechnol 66:266–275Google Scholar
  67. Ohta Y, Hatada Y, Nogi Y, Miyazaki M, Li Z, Akita M, Hidaka Y, Goda S, Ito S, Horikoshi K (2004b) Enzymatic properties and nucleotide and amino acid sequences of a thermostable beta-agarase from a novel species of deep-sea Microbulbifer. Appl Microbiol Biotechnol 64:505–514Google Scholar
  68. Ohta Y, Nogi Y, Miyazaki M, Li Z, Hatada Y, Ito S, Horikoshi K (2004c) Enzymatic properties and nucleotide and amino acid sequences of a thermostable beta-agarase from the novel marine isolate, JAMB-A94. Biosci Biotechnol Biochem 68:1073–1081Google Scholar
  69. Ohta Y, Hatada Y, Ito S, Horikoshi K (2005a) High-level expression of a neoagarobiose-producing beta-agarase gene from Agarivorans sp. JAMB-A11 in Bacillus subtilis and enzymic properties of the recombinant enzyme. Biotechnol Appl Biochem 41:183–191Google Scholar
  70. Ohta Y, Hatada Y, Miyazaki M, Nogi Y, Ito S, Horikoshi K (2005b) Purification and characterization of a novel alpha-agarase from a Thalassomonas sp. Curr Microbiol 50:212–216Google Scholar
  71. Parsiegla G, Juy M, Reverbel-Leroy C, Tardif C, Belaich JP, Driguez H, Haser R (1998) The crystal structure of the processive endocellulase CelF of Clostridium cellulolyticum in complex with a thiooligosaccharide inhibitor at 2.0 A resolution. EMBO J 17:5551–5562Google Scholar
  72. Petersen TN, Kauppinen S, Larsen S (1997) The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: a right-handed parallel beta helix. Structure 5:533–544Google Scholar
  73. Potin P (1992) Recherche, production, purification et caractérisation de galactane-hydrolases pour la préparation d’oligosaccharides des parois d’algues rouges. Thèse de Doctorat, Université de Bretagne Occidentale, Brest, Bretagne, FranceGoogle Scholar
  74. Potin P, Sanseau A, Le Gall Y, Rochas C, Kloareg B (1991) Purification and characterization of a new kappa-carrageenase from a marine Cytophaga-like bacterium. Eur J Biochem 201:241–247Google Scholar
  75. Potin P, Richard C, Rochas C, Kloareg B (1993) Purification and characterization of the alpha-agarase from Alteromonas agarlyticus (Cataldi) comb. nov., strain GJ1B. Eur J Biochem 214:599–607Google Scholar
  76. Potin P, Richard C, Barbeyron T, Henrissat B, Gey C, Petillot Y, Forest E, Dideberg O, Rochas C, Kloareg B (1995) Processing and hydrolytic mechanism of the cgkA-encoded kappa-carrageenase of Alteromonas carrageenovora. Eur J Biochem 228:971–975Google Scholar
  77. Rees D (1969) Structure, conformation, and mechanism in the formation of polysaccharide gels and networks. Adv Carbohydr Chem Biochem 24:267–332CrossRefGoogle Scholar
  78. Rees DA, Morris ER, Thom D, Madden J (1982) In: Aspinall GO (ed) The polysaccharides. Academic, New York, USA, pp 195–290Google Scholar
  79. Rochas C, Rinaudo M (1984) Mechanism of gel formation in k-carrageenan. Biopolymers 23:735–745Google Scholar
  80. Rouvinen J, Bergfors T, Teeri T, Knowles JK, Jones TA (1990) Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science 249:380–386Google Scholar
  81. Sakon J, Irwin D, Wilson DB, Karplus PA (1997) Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. Nat Struct Biol 4:810–818Google Scholar
  82. Sarwar G, Matayoshi S, Oda H (1987) Purification of a kappa-carrageenase from marine Cytophaga species. Microbiol Immunol 31:869–877Google Scholar
  83. Schroeder DC, Jaffer MA, Coyne VE (2003) Investigation of the role of a beta(1–4) agarase produced by Pseudoalteromonas gracilis B9 in eliciting disease symptoms in the red alga Gracilaria gracilis. Microbiology 149:2919–2929Google Scholar
  84. Shieh WY, Jean WD (1998) Alterococcus agarolyticus, gen.nov., sp.nov., a halophilic thermophilic bacterium capable of agar degradation. Can J Microbiol 44:637–645Google Scholar
  85. Sinnott ML (1990) Catalytic mechanisms of glycosyl transfer. Chem Rev 90:1171–1202Google Scholar
  86. Skea GL, Mountfort DO, Clements KD (2005) Gut carbohydrases from the New Zealand marine herbivorous fishes Kyphosus sydneyanus (Kyphosidae), Aplodactylus arctidens (Aplodactylidae) and Odax pullus (Labridae). Comp Biochem Physiol B 140:259–269Google Scholar
  87. Smidsrød O, Grasdalen H (1982) Some physical properties of carrageenan in solution and gel state. Carbohydr Polym 2:270–272Google Scholar
  88. Sorbotten A, Horn SJ, Eijsink VG, Varum KM (2005) Degradation of chitosans with chitinase B from Serratia marcescens. Production of chito-oligosaccharides and insight into enzyme processivity. FEBS J 272:538–549Google Scholar
  89. Stanier RY (1941) Studies on marine agar-digesting bacteria. J Bacteriol 42:527–559Google Scholar
  90. Stanier RY (1942) Agar-decomposing strains of the Actinomyces coelicolor species-group. J Bacteriol 1942:555–570Google Scholar
  91. Sugano Y, Matsumoto T, Kodama H, Noma M (1993a) Cloning and sequencing of agaA, a unique agarase 0107 gene from a marine bacterium, Vibrio sp. strain JT0107. Appl Environ Microbiol 59:3750–3756Google Scholar
  92. Sugano Y, Terada I, Arita M, Noma M, Matsumoto T (1993b) Purification and characterization of a new agarase from a marine bacterium, Vibrio sp. strain JT0107. Appl Environ Microbiol 59:1549–1554Google Scholar
  93. Sugano Y, Kodama H, Terada I, Yamazaki Y, Noma M (1994a) Purification and characterization of a novel enzyme, alpha-agarooligosaccharide hydrolase (alpha-NAOS hydrolase), from a marine bacterium, Vibrio sp. strain JT0107. J Bacteriol 176:6812–6818Google Scholar
  94. Sugano Y, Matsumoto T, Noma M (1994b) Sequence analysis of the agaB gene encoding a new beta-agarase from Vibrio sp. strain JT0107. Biochim Biophys Acta 1218:105–108Google Scholar
  95. Suzuki H, Sawai Y, Suzuki T, Kawai K (2003) Purification and characterization of an extracellular beta-agarase from Bacillus sp. MK03. J Biosci Bioeng 95:328–334Google Scholar
  96. Tempel W, Liu ZJ, Horanyi PS, Deng L, Lee D, Newton MG, Rose JP, Ashida H, Li SC, Li YT, Wang BC (2005) Three-dimensional structure of GlcNAcalpha1-4Gal releasing endo-beta-galactosidase from Clostridium perfringens. Proteins 59:141–144Google Scholar
  97. Turvey JR, Christison J (1967) The hydrolysis of algal galactans by enzymes from a Cytophaga species. Biochem J 105:311–321Google Scholar
  98. Usov AI, Miroshnikova LI (1975) Isolation of agarase from Littorina mandshurica by affinity chromatography on Biogel A. Carbohydr Res 43:204–207Google Scholar
  99. Van de Velde F, Peppelman H, Rollema H, Tromp R (2001) On the structure of kappa/iota-hybrid carrageenans. Carbohydr Res 331:271–283Google Scholar
  100. Van de Velde F, Rollema H, Grinberg N, Burova T, Grinberg V, Tromp R (2002) Coil–helix transition of ι-carrageenan as a function of chain regularity. Biopolymers 65:299–312Google Scholar
  101. Van der Meulen HJ, Harder W, Veldkamp H (1974) Isolation and characterization of Cytophaga flevensis sp. Nov., a new agarolytic flexibacterium. Antonie Van Leeuwenhoek 40:329–346Google Scholar
  102. Varrot A, Frandsen TP, von Ossowski I, Boyer V, Cottaz S, Driguez H, Schulein M, Davies GJ (2003) Structural basis for ligand binding and processivity in cellobiohydrolase Cel6A from Humicola insolens. Structure 11:855–864Google Scholar
  103. Vattuone MA, de Flores EA, Sampietro AR (1975) Isolation of neoagarobiose and neoagarotetraose from agarose digested by Pseudomonas elongata. Carbohydr Res 39:164–167Google Scholar
  104. Veldkamp H (1961) A study of two marine agar-degrading, facultatively anaerobic myxobacteria. J Gen Microbiol 26:331–342Google Scholar
  105. Vera J, Alvarez R, Murano E, Slebe JC, Leon O (1998) Identification of a marine agarolytic pseudoalteromonas isolate and characterization of its extracellular agarase. Appl Environ Microbiol 64:4378–4383Google Scholar
  106. Viebke C, Piculell L, Nilsson S (1994) On the mechanism of gelation of helix forming biopolymers. Macromolecules 27:4160–4166Google Scholar
  107. Voget S, Leggewie C, Uesbeck A, Raasch C, Jaeger KE, Streit WR (2003) Prospecting for novel biocatalysts in a soil metagenome. Appl Environ Microbiol 69:6235–6242Google Scholar
  108. Weigl J, Yaphe W (1966) The enzymic hydrolysis of carrageenan by Pseudomonas carrageenovora: purification of a kappa-carrageenase. Can J Microbiol 12:939–947Google Scholar
  109. Yaphe W (1957) The use of agarase from Pseudomonas atlantica in the identification of agar in marine algae (Rhodophyceae). Can J Microbiol 3:893–897CrossRefGoogle Scholar
  110. Yaphe W, Baxter B (1955) The enzymatic hydrolysis of carrageenin. Appl Microbiol 3:380–383Google Scholar
  111. Yoder MD, Keen NT, Jurnak F (1993) New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science 260:1503–1507Google Scholar
  112. Young KS, Hong KC, Duckworth M, Yaphe W (1971) Enzymic hydrolysis of agar and properties of bacterial agarases. Proc Int Seaweed Symp 7:15–22Google Scholar
  113. Zhong Z, Toukdarian A, Helinski D, Knauf V, Sykes S, Wilkinson JE, O’Bryne C, Shea T, DeLoughery C, Caspi R (2001) Sequence analysis of a 101-kilobase plasmid required for agar degradation by a Microscilla isolate. Appl Environ Microbiol 67:5771–5779Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Gurvan Michel
    • 1
  • Pi Nyval-Collen
    • 2
  • Tristan Barbeyron
    • 1
  • Mirjam Czjzek
    • 1
  • William Helbert
    • 2
  1. 1.Equipe Glycobiologie Marine, UMR7139 Végétaux Marins et Biomolécules (CNRS/UPMC)Roscoff, BretagneFrance
  2. 2.Equipe Structure des Polysaccharides Marins, UMR7139 Végétaux Marins et Biomolécules (CNRS/UPMC)Roscoff, BretagneFrance

Personalised recommendations