Skip to main content
Log in

Enzymes from marine phycophages that degrade cell walls of seaweeds

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Agarase, cellulase and alginate lyase activities from crude extracts of Aplysia dactylomela Rang, Haliotis coccinea canariensis Nordsieck, Littorina striata King et Broderip and Diadema antillarum Phillipi were measured in vitro to compare digestive efficiencies against several components of complex seaweed cell walls. Commercial abalone acetone powder (AAP, an extract from Haliotis sp.; Sigma, Ref. A-7514) and purified (Sigma, Ref. A-6306) and non-purified agarases from Pseudomonas atlantica were used with the same objective. Optimum conditions for agarase and cellulase activities were 40°C and pH 6.0. For alginate lyase, optimum temperature and pH were species-dependent. Highest reducing sugar release was shown by crude extracts from A. dactylomela. These crude extracts displayed high agarase activity compared with bacterial agarases at 40°C, and were significantly higher at 25°C. AAP and crude extracts from L. striata and D. antillarum exhibited high specific activities on all the substrates. Cold extract from Gracilaria spp. was the best substrate with which to measure agarase activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Benítez, L. V., Macaranas, J. M. (1979). Partial purification of a carrageenase from the tropical sea urchin Diadema setosum. Proc. int. Seaweed Symp. 9: 353–359 [Jensen, A., Stein, J. R. (eds.) Science Press, Princeton]

    Google Scholar 

  • Berliner, M. D. (1981). Protoplasts of eukaryotic algae. Int. Rev. Cytol. 73: 1–19

    Google Scholar 

  • Björk, M., Ekman, P., Wallin, A., Pedersén, M. (1990). Effects of growth rate and other factors on protoplast yield from four species of Gracilaria (Rhodophyta). Botanica mar. 33: 433–439

    Google Scholar 

  • Boyen, C., Kloareg, B., Polne-Fuller, M., Gibor, A. (1990). Preparation of alginate lyases from marine molluscs for protoplast isolation in brown algae. Phycologia 29: 173–181

    Google Scholar 

  • Brock, V., Kennedy, V. S., Brock, A. (1986). Temperature dependency of carbohydrase activity in the hepatopancreas of thirteen estuarine and coastal bivalve species from the North American east coast. J. exp. mar. Biol. Ecol. 103: 87–101

    Google Scholar 

  • Butler, D. M., Evans, L. V., Kloareg, B. (1990). Isolation of protoplasts from marine macroalgae. In: Akatsuka, I. (ed.) Introduction to applied phycology. SPB Academic Publishing, The Hague, p. 647–668

    Google Scholar 

  • Butler, D. M., Østgaard, K., Boyen, C., Evans, L. V., Jensen, A., Kloreg, B. (1989). Isolation conditions for high yields of protoplasts from Laminaria saccharina and L. digitata (Phaeophyceae). J. exp. Bot. 40: 1237–1246

    Google Scholar 

  • Chen, L. C.-M. (1987). Protoplast morphogenesis of Porphyra leucosticta in culture. Botanica mar. 30: 399–403

    Google Scholar 

  • Cheney, D. P., Mar, E., Saga, N., van der Meer, J. (1986). Protoplast isolation and cell division in the agar-producing seaweed Gracilaria (Rhodophyta). J. Phycol. 22: 238–243

    Google Scholar 

  • Cocking, E. (1972). Plant cell protoplasts. Isolation and development. A. Rev. Pl. Physiol. 23: 29–50

    Google Scholar 

  • Davison, I. R., Polne-Fuller, M. (1990). Photosynthesis in protoplasts of Macrocystis pyrifera (Phaeophyta). J. Phycol. 26: 384–387

    Google Scholar 

  • Duckworth, M., Turvey, J. R. (1969). An extracellular agarase from a Cytophaga species. Biochem. J. 113: 139–142

    Google Scholar 

  • Elyakova, L. A., Favorov, V. V. (1974). Isolation and certain properties of alginate lyase VI from the mollusk Littorina sp. Biochim. biophys. Acta 358: 341–354

    Google Scholar 

  • Eppley, R. W., Lasker, R. (1959). Alginase in the sea urchin Strongylocentrotus purpuratus. Science, N.Y. 129: 214–215

    Google Scholar 

  • Franssen, J., Jeuniaux, C. (1965). Digestion de l'acide alginique chez les invertebres. Cah. Biol. mar. 6: 1–21

    Google Scholar 

  • Friesen, J. A. (1980). The structure of the gut of Mysis stenolepis and the mechanism of cellulose digestion. M. Sc. thesis. Dalhousie University, Nova Scotia

    Google Scholar 

  • Galli, D. R., Giese, A. C. (1959). Carbohydrate digestion in a herbivorous snail, Tegula funebralis. J. exp. Zool. 140: 415–439

    Google Scholar 

  • Horiuchi, S., Lane, C. E. (1965). Digestive enzymes of the crystalline style of Strombus gigas Linne. I. Cellulase and some other carbohydrases. Biol. Bull. mar. biol. Lab., Woods Hole 129: 273–281

    Google Scholar 

  • Hylleberg Kristensen, J. (1972). Carbohydrases of some marine invertebrates with notes on their food and on the natural occurrence of the carbohydrates studies. Mar. Biol. 14: 130–142

    Google Scholar 

  • Jordan, P., Kloareg, B., Vilter, H. (1991). Detection of vanadate-dependent bromoperoxidases in protoplasts from the brown algae Laminaria digitata and L. saccharina. J. Pl. Physiol. 137: 520–524

    Google Scholar 

  • Kidby, D. K., Davidson, D. J. (1973). A convenient ferricyanide estimation of reducing sugars in the nanomole range. Analyt. Biochem. 55: 321–325

    Google Scholar 

  • Kloareg, B., Quatrano, R. S. (1988). Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr. mar. Biol. A. Rev. 26: 259–315

    Google Scholar 

  • Kreger, D. R. (1962). Cell walls. In: Lewin, R. D. (ed.) Physiology and biochemistry of algae. Academic Press, New York, p. 315–335

    Google Scholar 

  • Lahaye, M., Rochas, C., Yaphe, W. (1986). A new procedure for determining the heterogeneity of agar polymers in the cell wall of Gracilaria spp. (Gracilariaceae, Rhodophyta). Can. J. Bot. 64: 579–585

    Google Scholar 

  • Le Gall, Y., Braud, J. P., Kloareg, B. (1990). Protoplast production in Chondrus crispus gametophytes (Gigartinales, Rhodophyta). Pl. Cell Rep. 8: 582–585

    Google Scholar 

  • Lewis, J. B. (1964). Feeding and digestion in the tropical sea urchin Diadema antillarum Philippi. Can. J. Zool. 42: 549–557

    Google Scholar 

  • Liu, W. S., Tang, Y. L., Liu, X. W., Fang, T. C. (1984). Studies on the preparation and on the properties of sea snail enzymes. Hydrobiologia 116/117: 319–320

    Google Scholar 

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. biol. Chem. 193: 265–275

    Google Scholar 

  • Morrice, L. M., McLean, M., Williamson, F. B., Long, W. F. (1983). β-agarases I and II from Pseudomonas atlantica: purifications and some properties. Eur. J. Biochem. 135: 553–558

    Google Scholar 

  • Morrice, L. M., McLean, M., Williamson, F. B., Long, W. F. (1984). β-agarases from Pseudomonas atlantica. Hydrobiologia 116/117: 576–579

    Google Scholar 

  • Nakada, H. I., Sweeny, P. C. (1967). Alginic acid degradation by eliminases from abalone hepatopancreas. J. biol. Chem. 242: 845–851

    Google Scholar 

  • Nelson, N. (1944). A photometric adaptation of the Somogyi method for the determination of glucose. J. biol. Chem. 153: 375–380

    Google Scholar 

  • Nisizawa, K., Fujibayashi, S., Kashiwabara, Y. (1968). Alginate lyases in the hepatopancreas of a marine mollusc, Dolabella auricula Solander. J. Biochem. 64: 25–37

    Google Scholar 

  • Onishi, T., Suzuki, M., Kikuchi, R. (1985). The distribution of polysaccharide hydrolase activity in gastropods and bivalves. Bull. Jap. Soc. scient Fish. 51: 301–308

    Google Scholar 

  • Polne-Fuller, M. (1987). Preparation of enzymes. In: Indergaard, M., Østgaard, K., Guiry, M. D. (eds.) Seaweed protoplast and tissue culture. COST 48. European Economic Community, Brussels. Proceedings of Workshop on Biotechnical Methods in seaweed cultivation. E.E.C., Trondheim, p. 29–30

    Google Scholar 

  • Polne-Fuller, M., Biniaminov, M., Gibor, A. (1984). Vegetative propagation of Porphyra perforata. Hydrobiologia 116/117: 308–313

    Google Scholar 

  • Polne-Fuller, M., Gibor, A. (1987a) Microorganisms as digestors of seaweed cell walls. Hydrobiologia 151/152: 405–409

    Google Scholar 

  • Polne-Fuller, M., Gibor, A. (1987b). Tissue culture of seaweeds. In: Bird, K. T., Benson, P. H. (eds.) Seaweed cultivation for renewable resources. Vol. 16. Elsevier, Amsterdam, p. 219–239

    Google Scholar 

  • Preston, J. F., Romeo, T., Bromley, J. C., Robinson, R. W., Aldrich, H. C. (1985). Alginate lyase-secreting bacteria Underkofler, L. A. (ed.) Developments in industrial microbiology. Society for Industrial Microbiology, Arlington, Virginia, p. 727–740

    Google Scholar 

  • Saga, N., Polne-Fuller, M., Gibor, A. (1986). Protoplasts from seaweeds: production and fusion. In: Barclay, W. R., McIntosh, R. P. (eds.) Algal biomass technologies: an interdisciplinary perspective. Vol. 83. J. Cramer, Berlin, p. 37–43

    Google Scholar 

  • Saga, N., Sakai, Y. (1984). Isolation of protoplasts from Laminaria and Porphyra. Bull. Jap. Soc. scient. Fish. 50: p. 1085

    Google Scholar 

  • Smith, R. G., Bidwell, R. G. S. (1989). Inorganic carbon uptake by photosynthetically active protoplasts of the red macroalga Chondrus crispus. Mar. Biol. 102: 1–4

    Google Scholar 

  • Somogyi, M. (1952). Notes on sugar determination. J. biol. Chem. 195: 19–23

    Google Scholar 

  • Suzuki, M., Watanabe, Y., Tanaka, A., Ohnishi, T. (1986). The polysaccharide degradation activity in the apple snail. Bull. Tokai reg. Fish. Res. Lab. 120: 53–60

    Google Scholar 

  • Tokuda, H., Kawashima, Y. (1988). Protoplast isolation and culture of a brown alga, Undaria pinnatifida. In: Stadler, T., Mollion, J., Verdus, M.-C., Karamanos, Y., Morran, H., Christiaen, D. (eds.) Algal biotechnology. Elsevier Applied Science, London, p. 152–157

    Google Scholar 

  • Torzilli, A. P., Andrykovitch, G. (1980). Cell wall degrading enzymes produced by the salt marsh fungus Buergenerula spartinae. Botanica mar. 23: 645–650

    Google Scholar 

  • Van der Meulen, H. J. (1975). The enzymatic hydrolysis of agar by Cytophaga flevensis sp. nov. Ph. D. thesis. University of Groningen, The Netherlands

    Google Scholar 

  • Yaphe, W. (1966). The purification and properties of an agarase from a marine bacterium, Pseudomonas atlantica. Proc. 5th int. Seaweed Symp. 5: 333–335 [Young, E. G., McLachlan, J. L. (eds.) Pergamon Press, Oxford]

    Google Scholar 

  • Yokoe, Y., Yasumasu, I. (1964). The distribution of cellulase in invertebrates. Comp. Biochem. Physiol. 13: 323–338

    Google Scholar 

  • Zhu, R. (1983). A comparative study of marine algae cell-wall decomposition by the digestive enzymes isolated from three species of marine gastropods. Coll. ocean. Wks Qingdao (China) 6: 122–126

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J. M. Pérès, Marseille

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gómez-Pinchetti, J.L., García-Reina, G. Enzymes from marine phycophages that degrade cell walls of seaweeds. Marine Biology 116, 553–558 (1993). https://doi.org/10.1007/BF00355473

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00355473

Keywords

Navigation