Marine Biology

, Volume 108, Issue 1, pp 129–136 | Cite as

Glucose and glycerol uptake by isolated zooxanthellae fromCassiopea xamachana: Transport mechanisms and regulation by host homogenate fractions

  • A. Macon McDermott
  • R. S. Blanquet


We investigated the mechanisms by which glycerol and glucose enter freshly isolated zooxanthellae (FIZ),Symbiodinium microadriaticum Freudenthal, of the mangrove jellyfish,Cassiopea xamachana Bigelow, and the specific sites of host factor interaction. Glucose entry into FIZ is accomplished by a Na+-dependent symport system driven by an electrochemical gradient generated via a Na+-K+ ATPase. Inhibition of glucose uptake by a low molecular weight fraction of host homogenates [mol. wt<2 kilodaltons (kD)] occurs through the interaction of a putative host factor with the carrier protein and not the ATPase. Glycerol entry is apparently accomplished by simple or facilitated diffusion and is not affected by host homogenate fractions.


Glucose Molecular Weight Glycerol Glucose Uptake Transport Mechanism 
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Literature cited

  1. Barnett, R. E. (1965). Effect of monovalent cations on the ouabain inhibition of the sodium and potassium ion activated adenosine triphosphatase. J. Am. chem. Soc. 87: 4644–4648Google Scholar
  2. Battey, J. F., Patton, J. S. (1984). A reevaluation of the role of glycerol in carbon translocation in zooxanthellae-coelenterate symbiosis. Mar. Biol. 79: 27–38Google Scholar
  3. Battey, J. F., Patton, J. S. (1987). Glycerol translocation inCondylactis gigantea. Mar. Biol. 95: 37–46Google Scholar
  4. Blanquet, R. S., Emanuel, D., Murphy, T. A. (1988). Suppression of exogenous alanine uptake in isolated zooxanthellae by cnidarian host homogenate fractions: species and symbiosis specificity. J. exp. mar. Biol. Ecol. 117: 1–8Google Scholar
  5. Blanquet, R. S., Nevenzel, J. C., Benson, A. A. (1979). Acetate incorporation into the lipids of the anemoneAnthopleura elegantissima and its associated zooxanthellae. Mar. Biol. 54: 185–194Google Scholar
  6. Carroll, S. (1983). Alanine uptake by isolated zooxanthellae fromCassiopea xamachana (Cnidaria, Scyphozoa) and its suppression by an animal homogenate fraction. Ph. D. thesis, Georgetown University, Washington, D.C.Google Scholar
  7. Carroll, S., Blanquet, R. S. (1984a). Alanine uptake by isolated zooxanthellae of the mangrove jellyfish,Cassiopea xamachana. I. Transport mechanisms and utilization. Biol. Bull. mar. biol. Lab., Woods Hole 166: 409–418Google Scholar
  8. Carroll, S., Blanquet, R. S. (1984b). Alanine uptake by isolated zooxanthellae of the mangrove jellyfish,Cassiopea xamachana. II. Inhibition by host homogenate fraction. Biol. Bull. mar. biol. Lab., Woods Hole 166: 419–426Google Scholar
  9. Cavanaugh, G. M. (1964). Formulae and methods of the Marine Biological Laboratory Chemical Room, Chap. V. Mar. Biol. Lab., Woods Hole, Massachusetts, p. 83–84Google Scholar
  10. Cook, C. B. (1971). Transfer of35S-labeled material from food ingested byAiptasia sp. to its endosymbiotic zooxanthellae. In: Lenhoff, H. M., Muscatine, L., Davis, V. (eds.) Experimental coelenterate biology. Univ. of Hawaii Press, Honolulu, p. 218–224Google Scholar
  11. Cook, C. B. (1983). Metabolic interchanges in algae-invertebrate symbiosis. Int. Rev. Cytol. 14: 177–210Google Scholar
  12. Cook, C. B. (1985). Equilibrium populations and long term stability of mutualistic algal and invertebrate hosts. In: Boocher, D. B. (ed.) The biology of mutualism: ecology and evolution. Croom-Helm, Amsterdam, p. 171–191Google Scholar
  13. Crossland, C. J., Barnes, D. J., Borowitzka, M. A. (1980). Diurnal lipid and mucus production in the staghorn coralAcropora acuminata. Mar. Biol. 60: 81–90Google Scholar
  14. Deane, E. M., O'Brien, R. W. (1981). Uptake of sulphate, taurine, cysteine and methionine by symbiotic and free-living dinoflagellates. Archs Microbiol. 128: 311–319Google Scholar
  15. Douglas, A. E. (1988). Nutritional interactions as signals in the green hydra symbiosis. In: Scannerini, S., Smith, D., Bonfante-Fasolo, P., Gianinazii-Pearson, V. (eds.) Cell to cell signals in plant, animal and microbial symbiosis. Springer-Verlag, New York, p. 283–296Google Scholar
  16. Douglas, A. E., Smith, D. C. (1983). The cost of symbionts to the host in the green hydra symbiosis. In: Schwemmler, W., Schenk, H. E. A. (eds.) Endocytobiology, endosymbiosis and cell biology. Walter de Gruyter, Berlin, p. 631–648Google Scholar
  17. Emmelot, P., Bos, C. J., Van Hoeven, R. P., Van Blitterswijk, W. J. (1974). Isolation of plasma membranes from rat and mouse livers and hepatomas. In: Fleischer, S., Packer, L. (eds.) Methods in enzymology, Vol. 31. Biomembranes, Part A. Academic Press, New York, p. 75–91Google Scholar
  18. Glynn, P. W. (1983). Extensive ‘bleaching’ and death of reef corals on the Pacific coast of Panama. Envir. Conserv. 10: 149–154Google Scholar
  19. Glynn, P. W. (1984). Widespread coral mortality and the 1982/1983 El Nino warming event. Envir. Conserv. 11: 133–146Google Scholar
  20. Goreau, T. F. (1964). Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora. Science, N.Y. 145: 383–386Google Scholar
  21. Hinde, R. (1988). Factors produced by symbiotic marine invertebrates which affect translocation between the symbionts. In: Scannerini, S., Smith, D., Bonfante-Fasolo, P., Gianinazzi-Pearson, V. (eds.) Cell to cell signals in plant, animal and microbial symbiosis. Springer-Verlag, New York, p. 311–324Google Scholar
  22. Hoegh-Guldberg, O., Hinde, R. (1986). Studies on a nudibranch that contains zooxanthellae. I. Photosynthesis, respiration and the translocation of newly fixed carbon by zooxanthellae inPteraeolidia ianthina. Proc. R. Soc. (Ser. B) 228: 493–509Google Scholar
  23. Huntsberger, D. V., Billingsley, P. (1977). Elements of statistical inference. Allyn and Bacon, Inc., BostonGoogle Scholar
  24. Izawa, S., Good, N. E. (1972). Inhibition of photosynthetic electron transport and photophosphorylation. In: San Pietrol (ed.) Methods in enzymology, Vol. 24. Academic Press, New York, p. 335–377Google Scholar
  25. Jaap, W. C. (1979). Observations on zooxanthellae expulsion at Middle Sambo Reef, Florida Keys. Bull. mar. Sci. 29: 414–422Google Scholar
  26. Jeffrey, S. W., Haxo, F. T. (1968). Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol. Bull. mar. biol. Lab., Woods Hole 135: 149–165Google Scholar
  27. Jokiel, P., Coles, S. (1974). Effects of heated effluent on hermatypic corals at Kahe Point, Oahu. Pacif. Sci. 28: 1–18Google Scholar
  28. Katzen, H. M. (1967). The multiple forms of mammalian hexokinase and their significance to the action of insulin. In: Weber, G. (ed.) Advances in enzyme regulation, Vol. 5. Pergamon Press, New York, 335–356Google Scholar
  29. Kellogg, R. B., Patton, J. S. (1983). Lipid droplets, medium of energy exchange in the symbiotic anemoneCondylactis gigantea: a model coral polyp. Mar. Biol. 75: 137–149Google Scholar
  30. Kerkof, P. R., Abraham, S. (1974). Preparation of adipose cell-free suspensions of mammary gland parenchymal cells from lactating mice. Methods in Enzymology, Vol. 32. Biomembranes, Part B. Academic Press, New York, p. 693–706Google Scholar
  31. Komor, E., Tanner, W. (1974). Proton movement associated with hexose transport inChlorella vulgaris. In: Zimmerman, U., Dainty, J. (eds.) Membrane transport in plants. Springer-Verlag, Berlin, p. 209–215Google Scholar
  32. Leonard, R. T. (1982). The plasma membrane ATPase of plant cells: cation or proton pump? In: Martonosi, A. N. (ed.) Membranes and transport, Vol. 2. Plenum Press, New York, p. 633–637Google Scholar
  33. McAuley, P. J. (1985). The cell cycle of symbioticChlorella. I. The relationship between host feeding and algal cell growth and division. J. Cell Sci. 77: 225–239Google Scholar
  34. McAuley, P. J. (1986a). Uptake of amino acids by cultured and freshly isolated symbioticChlorella. New Phytol. 104: 415–427Google Scholar
  35. McAuley, P. J. (1987a). Quantitative estimation of movement of an amino acid from host toChlorella symbionts in green hydra. Biol. Bull. mar. biol. Lab., Woods Hole 173: 504–512Google Scholar
  36. McAuley, P. J. (1987b). Nitrogen limitation and amino acid metabolism ofChlorella symbiotic with green hydra. Planta 171: 532–538Google Scholar
  37. McCloskey, L. R., Muscatine, L. (1984). Production and respiration in the Red Sea coralStylophora pistillata as a function of depth. Proc. R. Soc. (Ser. B) 222: 215–230Google Scholar
  38. Muscatine, L. (1967). Glycerol excretion by symbiotic algae from corals andTridacna and its control by the host. Science, N.Y. 156: 516–519Google Scholar
  39. Muscatine, L. (1974). Endosymbiosis of cnidarians and algae. In: Muscatine, L., Lenhoff, H. M. (eds.) Coelenterate biology: reviews and perspectives. Academic Press, New York, p. 359–395Google Scholar
  40. Muscatine, L. (1980). Productivity of zooxanthellae. In: Falkowski, P. G. (ed.) Primary productivity in the sea. Plenum Press, New York, p. 381–402Google Scholar
  41. Muscatine, L., Cernichiari, E. (1969). Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. mar. biol. Lab., Woods Hole 137: 506–526Google Scholar
  42. Muscatine, L., Falkowski, P., Dubinsky, Z. (1983). Carbon budgets in symbiotic associations. In: Schenk, E. A., Schwemmler, W. (eds.) Endocytobiology. II. Intracellular space as oligogenetic ecosystem. Walter de Gruyter, Berlin, p. 649–659Google Scholar
  43. Muscatine, L., Pool, R. R., Cernichiari, E. (1972). Some factors influencing selective release of soluble organic material by zooxanthellae from reef corals. Mar. Biol. 13: 298–308Google Scholar
  44. Patton, J. S., Abraham, S., Benson, A. A. (1977). Lipogenesis in the intact coralPocillopora capitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle between symbiont and host. Mar. Biol. 44: 235–247Google Scholar
  45. Patton, J. S., Burris, J. E. (1983). Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar. Biol. 75: 131–136Google Scholar
  46. Rees, T. A. V. (1986). The green hydra symbiosis and ammonium. I. The role of the host in ammonium assimilation and its possible regulatory significance. Proc. R. Soc. (Ser. B) 229: 425–314Google Scholar
  47. Reinhold, L., Kaplan, A. (1984). Membrane transport of sugars and amino acids. A. Rev. Pl. Physiol. 35: 45–83Google Scholar
  48. Schlichter, D., Kremer, B. P., Svoboda, A: (1984). Zooxanthellae providing assimilatory power for the incorporation of exogenous acetate inHeteroxenia fuscescens (Cnidaria: Alcyonaria). Mar. Biol. 83: 277–286Google Scholar
  49. Schlichter, D., Svoboda, A., Kremer, B. P. (1983). Functional autotrophy ofHeteroxenia fuscescens (Anthozoa: Alcyonaria): carbon assimilation and translocation of photosynthates from symbionts to host. Mar. Biol. 78: 29–38Google Scholar
  50. Schmitz, K., Kremer, B. P. (1977). Carbon fixation and analysis of assimilates in a coral-dinoflagellate symbiosis. Mar. Biol. 42: 305–313Google Scholar
  51. Steele, R. D. (1976). Light intensity as a factor in the regulation of the density of symbiotic zooxanthellae inAiptasia tagetes. J. Zool., Lond. 179: 387–405Google Scholar
  52. Steen, R. G., (1986a). Evidence for heterotrophy by zooxanthellae in symbiosis withAiptasia pulchella. Biol. Bull. mar. biol. Lab., Woods Hole 170: 267–286Google Scholar
  53. Steen, R. G. (1986b). Impact of symbiotic algae on sea anemone metabolism: analysis by in vivo31P nuclear magnetic resonance spectroscopy. J. Exp. Zool. 240: 315–325Google Scholar
  54. Steen, R. G. (1987). Evidence for facultative heterotrophy in cultured zooxanthellae. Mar. Biol. 95: 15–23Google Scholar
  55. Steen, R. G., Muscatine, L. (1984). Daily budgets of photosynthetically fixed carbon in symbiotic zoanthids. Biol. Bull. mar. biol. Lab., Woods Hole 167: 477–487Google Scholar
  56. Steen, R. G., Muscatine, L. (1987). Low temperature evokes rapid exocytosis of symbiotic algae by a sea anemone. Biol. Bull. mar. biol. Lab., Woods Hole 172: 246–263Google Scholar
  57. Sukalski, K. A., Nordlie, R. C. (1989). Glucose-6-phosphatase: two concepts of membrane-function relationship. In: Meister, A. (ed.) Advances in enzymology, Vol. 62. J. Wiley and Sons, New York, p. 93–117Google Scholar
  58. Sullivan, C. W., Volcani, B. E. (1974). Synergistically stimulated (Na+,K+)-adenosine triphosphatase from plasma membrane of a marine diatom. Proc. Natn. Acad. Sci. U.S.A. 71: 4376–4380Google Scholar
  59. Sutton, D. C., Hoegh-Guldberg, O. (1990). Host-zooxanthella interactions in four temperature marine invertebrate symbioses. Assessment of effect of host extracts on symbionts. Biol. Bull. mar. biol. Lab., Woods Hole 178: 179–186Google Scholar
  60. Thorington, G., Margulis, L. (1981).Hydra viridis: Transfer of metabolites betweenHydra and symbiotic algae. Biol. Bull. mar. biol. Lab., Woods Hole 160: 175–188Google Scholar
  61. Trench, R. K. (1971a). The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. I. Assimilation of photosynthetic products of zooxanthellae by two marine coelenterates. Proc. R. Soc. (Ser. B) 177: 225–235Google Scholar
  62. Trench, R. K. (1971b). The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. Liberation of fixed14C by zooxanthellae in vitro. Proc. R. Soc. (Ser. B) 177: 237–250Google Scholar
  63. Trench, R. K. (1971c). The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. III. The effects of homogenates of host tissues on the excretion of photosynthesis products in vitro by zooxanthellae from two marine coelenterates. Proc. R. Soc. (Ser. B) 177: 251–264Google Scholar
  64. Trench, R. K. (1979). The cell biology of plant-animal symbiosis. A. Rev. Pl. Physiol. 30: 485–531Google Scholar
  65. Tycko B., Maxfield, F. R. (1982). Rapid acidification of endocytic vesicles containing alpha-macroglobulin. Cell (MIT Press, Cambridge, Mass.) 28: 643–651Google Scholar
  66. Wright, E. M., Diamond, J. M. (1969). Patterns of non-electrolyte permeability. Proc. R. Soc. (Ser. B) 172: 227–271Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • A. Macon McDermott
    • 1
  • R. S. Blanquet
    • 1
  1. 1.Department of BiologyGeorgetown UniversityWashington, D.C.USA

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