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Marine Biology

, Volume 75, Issue 2–3, pp 157–167 | Cite as

Nutrient uptake kinetics of freshly isolated zooxanthellae

  • C. F. D'Elia
  • S. L. Domotor
  • K. L. Webb
Article

Abstract

Zooxanthellae of the species Gymnodinium (=Symbiodinium) microadriaticum freshly isolated from a variety of hosts (Zoanthus spp., Tridacna crocea, Seriatopora hystrix, Montastrea annularis, Porites furcata, and Stylophora pistillata) in the tropical Pacific Ocean and the Caribbean Sea exhibited saturation uptake kinetics when incubated in seawater enriched with nitrate, nitrite or ammonium. Half-saturation constants (Ks) for nitrate ranged from 0.23 to 3.14 μM, for nitrite from 0.23 to 7.15 μM, and for ammonium from 5.03 to 21.99 μM. Maximum specific uptake rates (Vmax) for ammonium (1.05 to 2.79 d-1) exceeded those for both nitrate (not detectable to 0.54 d-1) and nitrite (not detectable to 0.67 d-1). Light did not affect the uptake rate of any substrate tested, nor did the addition of ammonium in concentrations up to 20 μM reduce the rate of nitrate uptake at Vmax, but nitrite uptake was inhibited by the addition of nitrate to the medium. The inhibition of nitrite uptake by nitrate could not be described either as competitive or non-competitive. Although maximum specific uptake rates obtained for ammonium appear to exceed maximum potential specific growth rate in terms of nitrogen of the algae, the actual growth potential of the algae must be limited not only by nutrient concentrations to which they are exposed, but also by the percentage of assimilated nitrogen that they translocate to their host. Uptake rates obtained for isolated zooxanthellae in this study are similar to those obtained previously for intact coral-zooxanthellae symbioses. This evidence is consistent with the hypothesis that nutrient uptake by intact zooxanthellae-host symbioses occurs by diffusion down a concentration gradient created by localized substrate depletion by the zooxanthellae in host tissue.

Keywords

Nitrate Nutrient Uptake Nitrite Uptake Rate Pacific Ocean 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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Literature cited

  1. Burris, R. H.: Uptake and assimilation of 15NH4+ by a variety of corals. Mar. Biol. 75, 151–155 (1983)Google Scholar
  2. Caperon, J. and J. Meyer: Nitrogen-limited growth of marine phytoplankton II. Uptake kinetics and their role in nutrient limited growth of phytoplankton. Deep-Sea Res. 19, 619–632 (1972)Google Scholar
  3. Carpenter, E. J. and R. R. L. Guillard: Intraspecific differences in nitrate half-saturation constants for three species of marine phytoplankton. Ecology 52, 183–185 (1971)Google Scholar
  4. Crossland, C. J. and D. J. Barnes: Nitrate assimilation enzymes from two hard corals, Acropora acuminata and Goniastrea australensis. Comp. Biochem. Physiol. 57B, 151–157 (1977)Google Scholar
  5. D'Elia, C. F.: The uptake and release of dissolved phosphorus by reef corals. Limnol. Oceanogr. 22, 301–315 (1977)Google Scholar
  6. D'Elia, C. F. and K. L. Webb: The dissolved nitrogen flux of reef corals. Third Int. Coral Reef Symp. 1, 325–330 (1977)Google Scholar
  7. D'Elia, C. F., K. L. Webb and J. W. Porter: Nitrate-rich ground-water inputs to Discovery Bay, Jamaica: a significant source of N to local coral reefs? Bull. mar. Sci. 31, 903–910 (1981)Google Scholar
  8. Domotor, S. and C. F. D'Elia: Nutrient uptake kinetics and growth of zooxanthellae in laboratory culture. (In preparation)Google Scholar
  9. Dugdale, R. C. and J. J. Goering: Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol. Oceanogr. 12, 196–206 (1967)Google Scholar
  10. Eppley, R. W.: Relations between nutrient assimilation and growth in phytoplankton with a brief review of estimates of growth rate in the ocean. In: Physiological bases of phytoplankton ecology, pp 234–250. Ed. by T. Platt, Bull. 210, Department of Fisheries and Oceans, Ottawa, Canada 1981Google Scholar
  11. Eppley, R. W. and J. L. Coastsworth: Uptake of nitrate and nitrite by Ditylum brightwellii — kinetics and mechanisms. J. Phycol. 4, 151–156 (1968)Google Scholar
  12. Eppley, R. W., J. N. Rogers and J. J. McCarthy: Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr. 14, 912–920 (1969)Google Scholar
  13. Franzisket, L.: Uptake and accumulation of nitrate and nitrite by reef corals. Naturwiss. 12, 552 (1973)Google Scholar
  14. Franzisket, L.: Nitrate uptake by reef corals. Int. Rev. ges. Hydrobiol. 59, 1–7 (1974)Google Scholar
  15. Froelich, P. N. and M. E. Q. Pilson: Systematic absorbance errors with Technicon AutoAnalyzer II colorimeters. Water Res. 12, 599–603 (1978)Google Scholar
  16. Gavis, J.: Munk and Riley revisited: nutrient diffusion transport and rates of phytoplankton growth. J. mar. Res. 34, 161–179 (1976)Google Scholar
  17. Glibert, P. M. and J. C. Goldman: Rapid ammonium uptake by marine phytoplankton. Mar. Biol. Lett. 2, 25–31 (1981)Google Scholar
  18. Hallock, P.: Algal symbiosis: a mathematical analysis. Mar. Biol. 62, 249–255 (1981)Google Scholar
  19. Harrison, P. J. and C. O. Davis: Use of the perturbation technique to measure nutrient uptake rates of natural phytoplankton populations. Deep-Sea Res. 24, 247–255 (1977)Google Scholar
  20. Helder, W. and R. T. P. DeVries: An automatic phenol-hypochlorite method for the determination of ammonia in sea-and brackish waters. Neth. J. Sea Res. 13, 154–160 (1979)Google Scholar
  21. Jackson, G. A.: Phytoplankton growth and zooplankton grazing oligotrophic oceans. Nature, Lond. 284, 439–441 (1980)Google Scholar
  22. Jeffrey, S. W. and G. F. Humphrey: New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae, and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191–194 (1975)Google Scholar
  23. Johannes, R. E. and W. J. Wiebe: A method for determination of coral tissue biomass and composition. Limnol. Oceanogr. 15, 822–824 (1970)Google Scholar
  24. Kawaguti, S.: Ammonium metabolism of the reef corals. Biol. J. Okayama Univ. 1, 171–176 (1953)Google Scholar
  25. Lewis, D. H. and D. C. Smith: The autotrophic nutrition of symbiotic marine coelenterates with special reference to hermatypic corals. I. Movement of photosynthetic products between the symbionts. Proc. R. Soc. Lond. B. 178, 111–129 (1971)Google Scholar
  26. MacIsaac, J. J. and R. C. Dugdale: The kinetics of nitrate and ammonium uptake by natural populations of marine phytoplankton. Deep-Sea Res. 16, 45–57 (1969)Google Scholar
  27. McCarthy, J. J.: The kinetics of nutrient utilization. In: Physiological bases of phytoplankton ecology, pp 234–250. Ed. by T. Platt, Bull. 210, Department of Fisheries and Oceans, Ottawa, Canada 1981Google Scholar
  28. McCarthy, J. J. and J. C. Goldman: Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters. Science, N.Y. 23, 670–672 (1979)Google Scholar
  29. Mosteller, F. and J. W. Tukey: Data analysis and regression, 558 pp. Reading, Mass: Addision-Wesley Publishing Co. 1977Google Scholar
  30. Muscatine, L.: Productivity of zooxanthellae. In: Primary productivity in the sea, pp 381–402. Ed. by P. G. Falkowski. New York: Plenum Publishing Corp. 1980aGoogle Scholar
  31. Muscatine, L.: Uptake, retention, and release of dissolved inorganic nutrients by marine alga-invertebrate associations. In: Cellular interactions in symbiosis and parasitism, pp 229–244. Ed. by C. B. Cook. Columbus: Ohio State University Press 1980bGoogle Scholar
  32. Muscatine, L. and E. Cernichiari: Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. mar. biol. Lab., Woods Hole 137, 506–523 (1969)Google Scholar
  33. Muscatine, L. and C. F. D'Elia: The uptake, retention and release of ammonium by reef corals. Limnol. Oceanogr. 23, 725–734 (1978)Google Scholar
  34. Muscatine, L. and R. E. Marian: Dissolved inogranic nitrogen flux in symbiotic and non-symbiotic medusae. Limnol. Oceanogr. 27, 910–917 (1982)Google Scholar
  35. Muscatine, L., T. H. Masuda and R. Burnap: Ammonium uptake by symbiotic and aposymbiotic reef corals. Bull. mar. Sci. 29, 572–575 (1979)Google Scholar
  36. Muscatine, L. and J. W. Porter: Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27, 454–459 (1977)Google Scholar
  37. Neame, K. D. and T. G. Richards: Elementary kinetics of membrane carrier transport, 120 pp. New York: John Wiley and Sons 1972Google Scholar
  38. Parsons, T. R. and J. D. H. Strickland: Discussion of spectrophotometric determination of marine-plant pigments, with revised equations for ascertaining chlorophylls and carotenoids. J. mar. Res. 21, 155–163 (1963)Google Scholar
  39. Pasciak, W. J. and J. Gavis: Transport limitation of nutrient uptake in phytoplankton. Limnol. Oceanogr. 18, 511–515 (1973)Google Scholar
  40. Pomeroy, L. R. and E. J. Kuenzler: Phosphorus turnover by coral reef animals. Proc. Conf. Radioecol. (2nd), pp 474–482, AEC Conf.-67053 (1969)Google Scholar
  41. Propp, M. V.: Release and uptake of ammonium, nitrate, and orthophosphate by some corals. Sov. J. mar. Biol. 7, 198–204 (1981)Google Scholar
  42. Raven, J. A.: Nutrient transport in microalgae. In: Advances in microbial physiology, vol. 21, pp 47–226. Ed. by A. H. Rose and J. G. Morris. New York: Academic Press 1980Google Scholar
  43. Schoenberg, D. A. and R. K. Trench: Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and spevificity in its symbiosis with invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proc. R. Soc. Lond. B 207, 405–427 (1980)Google Scholar
  44. Syrett, P. J.: Nitrogen metabolism of microalgae. In: Physiological bases of phytoplankton ecology, pp 182–210. Ed. by T. Platt, Bull. 210, Department of Fisheries and Oceans, Ottawa, Canada 1981Google Scholar
  45. Szmant-Froelich, A. and M. E. Q. Pilson: Nitrogen excretion by colonies of the temperate coral Astrangia danae with and without zooxanthellae. Proc. 3d Int. Coral Reef Symp. 1, 417–423 (1977)Google Scholar
  46. Taylor, D. L.: The cellular interactions of algal-invertebrate symbiosis. Adv. mar. Biol. 11, 1–56 (1973)Google Scholar
  47. Taylor, D. L.: Symbiotic marine algae: taxonomy and biological fitness. In: Symbiosis in the sea, pp 245–262. Ed. by W. Vernberg. Columbia: University of South Carolina Press 1974Google Scholar
  48. Taylor, D. L.: Nutrition of algal-invertebrate symbiosis. II. Effects of exogenous nitrogen sources on growth, photosynthesis and the rate of excretion by algal symbionts in vivo and in vitro. Proc. R. Soc. Lond. B. 201, 401–412 (1978a)Google Scholar
  49. Taylor, D. L.: Artificially induced symbiosis between marine flagellates and vertebrate tissues in culture. J. Protozool. 25, 77–81 (1978b)Google Scholar
  50. Tomas, C. R.: Olisthodiscus luteus (Chrysophyceac). III. Uptake and utilization of nitrogen and phosphorus. J. Phycol. 15, 5–12 (1979)Google Scholar
  51. Trench, R. K.: Cellular and molecular interactions in symbioses between dinoflagellates and marine invertebrates. Pure Appl. Chem. 53, 819–835 (1981)Google Scholar
  52. US Environmental Protection Agency: Method for chemical analysis of water and wastes. EPA-600/4-79-020. Off. Res. Devel. Cincinnati, Ohio (1979)Google Scholar
  53. Webb, K. L. and W. J. Wiebe: The kinetics and possible significance of nitrate uptake by several algal-invertebrate symbioses. Mar. Biol. 47, 21–27 (1978)Google Scholar
  54. Webb, K. L., W. D. DuPaul, W. Wiebe, W. Sottile and R. E. Johannes: Eniwetok (Eniwetok) Atoll: aspects of the nitrogen cycle on the coral reef. Limnol. Oceanogr 20, 198–210 (1975)Google Scholar
  55. Yamazato, K.: Calcification in a solitary coral, Fungia scutaria L. in relation to environtnental factors. Bull. Sci. Eng. Div., Univ. Ryukyus, Math. Nat. Sci. 13, 57–122 (1970)Google Scholar
  56. Yonge, C. M. and A. G. Nicholls: Studies on the physiology of corals. 4. The structure, distribution and physiology of zooxanthellae. Sci. Rep. Great Barrier Reef Exped. 1, 135–176 (1931)Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • C. F. D'Elia
    • 1
  • S. L. Domotor
    • 1
  • K. L. Webb
    • 2
  1. 1.Center for Environmental and Estuarine StudiesChesapeake Biological Laboratory, University of MarylandSolomonsUSA
  2. 2.Virginia Institute of Marine ScienceCollege of William and MaryGloucester PointUSA

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