Abstract
The phosphorus metabolism of Pyrocystis noctiluca Murray (Schuett) 1886 has characteristics which may enhance its potential for success in orthophosphate impoverished waters. The steady-state phosphate uptake rates were equal in the light and dark, and were directly proportional to both the phosphorus cell quota and the cell division rate. In contrast, nutrient-saturated uptake rates were multiphasic, faster in the light than the dark, 2 to 4 orders of magnitude greater than steady-state rates, and were inversely proportional to both the phosphorus cell quota and the cell division rate. These uptake characteristics suggest that P. noctiluca may take up phosphate coincidently at their typically low ambient concentrations as well as to exploit episodic nutrient events in nature. Cell division rates were a hyperbolic function of the ambient orthophosphate concentration. The shortest doubling time was 8.7 d, the phosphate concentration at half the maximum division rate was 0.15 μM and the threshold, concentration for cell division was ca 0.05 μM PO 3-4 . Division rates of P. noctiluca in the ocean are much faster than predicted from the measured ambient orthophosphate concentrations. Since this dinoflagellate has high naturally occurring alkaline phosphatase activities, and can utilize organic-P compounds, we suggest that organic-P can be as important as orthophosphate in supporting the observed division rates of P. noctiluca in the sea.
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Literature cited
Beers, J. R., D. M. Stevens and J. B. Lewis: Primary productivity in the Caribbean Sea off Jamaica and the tropical North Atlantic off Barbados. Bull mar. Sci. 18, 86–104 (1968)
Bendschneider, K. and R. J. Robinson: A new spectrophotometric determination of nitrate in sea water. J. mar. Res. 11, 87–96 (1952)
Bhovichitra, M. and E. Swift: Light and dark uptake of nitrate and ammonia by large oceanic dinoflagellates: Pyrocystis noctiluca, Pyrocystis fusiformis, and Dissodinium lunula. Limnol. Oceanogr. 22, 73–83 (1977)
Butler, E. I., S. Knox and M. I. Liddicoat: The relationship between inorganic and organic nutrients on sea water. J. mar. Biol. Ass. U.K. 59, 349–350 (1979)
Caperon, J. and J. Meyers: 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)
Davis, C. O., Harrison, P. J. and R. Dugdale: Continuous cultures of marine diatoms under silicate limitation. I. Synchronized life cycle of Skeletonema costatum. J. Phycol. 9, 275–282 (1973)
Dowd, J. E. and D. S. Riggs: A comparison of Michaelis-Menten constants from various linear transformations. J. Biol. Chem. 240, 863–869 (1965)
Elgavish, A., G. A. Elgavish, T. Berman and M. Holmann: Phosphorus utilization and storage in batch cultures of the dinoflagellate peridinium cinctum f. westii. J. Phycol. 16, 626–633 (1980)
Elgavish, A. and G. A. Elgavish: 31P-NMR differentiation between intracellular phosphate pools in Cosmarium (Chlorophyta). J. Phycol. 16, 368–374 (1980)
Elgavish, A., M. Holmann and T. Berman: A comparative study of phosphorus utilization and storage on batch cultures of Peridinium cinctum, Pediastrum duplex and Cosmarium sp. from Lake Kinneret (Israel). J. Phycol. 21, 47–54 (1982)
Eppley, R. W., E. H. Renger, E. L. Venrick and M. M. Mullin: A study of plankton dynamics and nutrient cycling in the central gyre of the North Pacific Ocean. Limnol. Oceanogr. 18, 534–551 (1973)
Fitzgerald, G. P. and T. C. Nelson: Extractive and enzymatic analysis for limiting and surplus phosphorus in algae. J. Phycol. 2, 32–37 (1966)
Fuhs, G. W.: Phosphorus content and the rate of growth in the diatom Cyclotella nana and Thalassiosira fluviatilis. J. Phycol. 5, 305–321 (1969)
Fuhs, G. W., S. D. Demmerle, E. Canelli and M. Chen: Characterization of phosphorus-limited algae. In: Nutrients and Eutrophication, pp 113–132. Ed. by G. E. Likens. Am. Soc. Limnol Oceanogr. Spec. Symp., Vol. 1, Lawrence, Kansas: Allen Press 1972
Goldman, J. C., J. J. McCarthy and D.G. Peavey: Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature, Lond. 279, 210–215 (1979)
Goldman, J. C. and P. M. Glibert: Comparative rapid ammonium uptake by four species of marine phytoplankton. Limnol. Oceanogr. 273, 814–827 (1982)
Gotham, I. J. and G. Y. Rhee: Comparative kinetic studies of phosphate limited growth and phosphate uptake in phytoplankton in continuous culture. J. Phycol. 171, 157–165 (1981)
Guillard, R. R. L. and J. H. Ryther: Studies of marine plankton diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229–239 (1962)
Harold, F. M.: Inorganic polyphosphates in biology: structure, metabolism and function. Bacterial Rev. 30, 772–795 (1966)
Haug, A., S. Myklestad and E. Sakshaug: Studies on the phytoplankton ecology of the Trondheimsfjord. The chemical composition of phytoplankton populations. J. exp. mar. Biol. Ecol. 11, 15–26 (1973)
Jackson, G. A.: Phytoplankton growth and zooplankton grazing in oligotrophic oceans. Nature, Lond. 284, 439–440 (1980)
Kanai, R., S. A. Aoki and S. Miyachi: Quantitative separation of polyphosphates in Chlorella cells. Plant Cell Physiol. 6, 467–473 (1965)
Ketchum, B. H., N. Corwin and D. J. Keen: The significance of organic phosphorus determinations in ocean water. Deep-Sea Res. 2, 172–181 (1955)
Kuenzler, E. J., R. R. L. Guillard and N. Corwin: Phosphate-free sea water for reagent blanks in chemical analysis. Deep-Sea Res. 10, 749–755 (1963)
Kuenzler, E. J. and J. P. Perras: Phosphatases of marine algae. Biol. Bull. mar. biol. Lab., Woods Hole 128, 271–284 (1965)
Lehman, J. T. and D. Scavia: Microscale patchiness of nutrients in plankton communities. Science, N.Y. 216, 729–730 (1982)
Lowry, O. H., N. J. Rosenbrough, A. L. Farr and R. J. Randall: Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951)
McCarthy, J. J. and J. C. Goldman: Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters. Science, N.Y. 203, 670–672 (1979)
McDuff, R. E. and S. W. Chisholm: The calculation of in situ growth rates of phytoplankton populations from the fraction of cells undergoing mitoses. A clarification. Limnol. Oceanogr. 27, 783–788 (1982)
Menzel, D. W. and J. H. Ryther: The annual cycle of primary production in the Sargasso Sea off Bermuda. Deep-Sea Res. 66, 351–365 (1960)
Menzel, D. W. and N. Corwin: The measurement of total phosphorus in sea water based on the liberation of organically bound phosphate by persulfate oxidation. Limnol. Oceanogr. 10, 280–283 (1965)
Murphy, J. and J. P. Riley: A modified single solution method for the determination of phosphate in natural water. Anal. Chem. Acta. 27, 31–36 (1962)
Myklestad, S.: Production of carbohydrates by marine planktonic diatoms. II. Influence of the N:P ratio in the growth medium on the assimilation ratio, growth rate, and production of carbohydrates by Chaetoceros affinis var willei (Gran) Hustedt and Skeletonema costatum (Grev). Cleve. J. exp. mar. Biol. Ecol. 29, 161–179 (1977)
Paasche, E.: Silicon and the ecology of marine plankton diatoms. II. Silicate-uptake kinetics in five diatom species. Mar. Biol. 19, 262–266 (1973)
Parsons, T. R. and M. Takahashi: Biological oceanographic processes. 186 pp. New York: Pergamon Press 1973
Packard, T. T., T. M. Moore and T. Harmon: Biochemical assays. In: Chemostat methodology and chemical analysis, pp 119–130. Ed. by S. P. Pavlou. Spec. Rep. 52, Dept. Oceanogr., Univ. Washington, Seattle, Washington 1972
Perry, M. J.: Alkaline phosphatase activity in subtropical central North Pacific waters using a sensitive flurometric method. Mar. Biol. 15, 113–119 (1972)
Perry, M. J.: Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in oligotrophic waters of the central North Pacific. Limnol. Oceanogr. 21, 88–107 (1976)
Qasim, S. A., P. M. A. Bhattathirio and V. P. Devassy: Growth kinetics and nutrient requirements of two tropical marine phytoplankton. Mar. Biol. 21, 299–304 (1973)
Rhee, G. Y.: Competition between an alga and an aquatic bacterium for phosphate. Limnol. Oceanogr. 17, 505–514 (1972)
Rhee, G. Y.: A continuous culture study of phosphate uptake, growth rate and polyphosphate in Scenedesmus sp. J. Phycol. 9, 495–506 (1973)
Rhee, G. Y.: Phosphate uptake under nitrate limitation by Scenedesmus sp. and its ecological implications. J. Phycol. 10, 470–475 (1974)
Rhee, G. Y.: Effects of N:P atomic ratios and nitrate limitation on algal growth, cell composition and nitrate uptake. Limnol. Oceanogr 23, 10–25 (1978)
Rivkin, R. B.: Phosphorus metabolism in the oceanic dinoflagellate Pyrocystis noctiluca, 172 pp. Ph.D. thesis, University of Rhode Island 1979
Rivkin, R. B. and E. Swift: Diel and vertical patterns of alkaline phosphatase activity in the oceanic dinoflagellate Pyrocystis noctiluca. Limnol. Oceanogr. 24, 107–116 (1972)
Rivkin, R. B. and E. Swift: Characterization of alkaline phosphatase and organic phosphorus utilization in the oceanic dinoflagellate Pyrocystis noctiluca. Mar. Biol. 61, 1–8 (1980)
Rivkin, R. B. and E. Swift: Phosphate uptake by the oceanic dinoflagellate Pyrocystis noctiluca. J. Phycol. 18, 113–180 (1982)
Rivkin, R. B., H. H. Seliger, E. Swift and W. H. Biggley: Light-shade adaptation by the oceanic dinoflagellates Pyrocystis noctiluca and P. fusiformis. Mar. Biol. 68, 181–191 (1982)
Rivkin, R. B., E. Swift, W. H. Biggley and M. A. Voytek: Growth and carbon uptake by natural populations of the oceanic dinoflagellates Pyrocystis noctiluca and Pyrocystis fusiformis. Deep-Sea Res 31, 353–367 (1984)
Rowan, K. S.: Phosphorus metabolism in plants. Int. Rev. Cytol. 19, 301–390 (1966)
Ryther, J. H., D. W. Menzel and R. F. Vaccaro: Diurnal variations in some chemical and biological properties of the Sargasso Sea. Limnol. Oceanogr. 6, 149–153 (1961)
Ryther, J. H. and W. H. Dunstan: Nitrogen, phosphorus and eutrophication in coastal marine environment. Science, N.Y. 171, 1198–1203 (1971)
Sakshaug, E. and S. Myklestad: Studies on the phytoplankton ecology of the Trondheimsfjord. III. Dynamics of phytoplankton blooms in relation to environmental factors, bioassay experiments and parameters for the physiological state of the population. J. exp. mar. Biol. Ecol. 11, 157–188 (1973)
Sakshaug, E. and O. Holm-Hansen: Chemical composition of Skeletonema costatum (Grev.) Cleve and Pavlova (Monochrysis) lutheri (Droop) Green as a function of nitrate, phosphate, and iron-limited growth. J. exp. mar. Biol. Ecol. 29, 1–34 (1977)
Sakshaug, E. and A. Jensen: The use of cage cultures in studies of the biochemistry and ecology of marine phytoplankton. Oceanogr. mar. Biol. Ann. Rev. 16, 81–106 (1978)
Sander, F. and E. Moore: Significance of ammonia in determining the N:P ratio of the sea water off Barbados, West Indies. Mar. Biol. 55, 17–21 (1979)
Semina, H. J. and I. A. Tarkhova: Ecology of plankton in the Northern Pacific Ocean. In: Biological oceanography of the Northern North Pacific Ocean, pp 117–124. Ed. by A. Y. Takenouti. Tokyo: Identsu Shoten 1972
Sharp, J. H., M. J. Perry, E. H. Renger and R. W. Eppley: Phytoplankton rate processes in the oligotrophic waters of the central North Pacific Ocean. J. Plankt. Res. 2, 335–353 (1980)
Skipnes, O., I. Eide and A. Jensen: Cage culture turbidostat: a device for rapid determination of algal growth rate. Appl. environ. Microbiol. 40, 318–325 (1980)
Sokal, R. R. and F. J. Rohlf: Biometry, 776 pp. San Francisco: Freeman Press 1969
Solórzano, L.: The determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr. 13, 799–891 (1969)
Steemann Nielsen, E.: Growth of plankton algae as a function of N-concentration, measured by means of a batch technique. Mar. Biol. 46, 185–189 (1978a)
Steeman Nielsen, E.: Growth of the unicellular algae Selenastrum capricornutum as a function of P with some information also on N. Verh. int. Ver. theor. angew. Limnol. 20, 38–42 (1978b)
Sukhanova, I. N.: Vertical distribution of some peridinians in the equatorial Pacific. In: Life activity of pelagic communities in the ocean tropics, pp 210–217. Ed. by M. E. Vinogradov. Jerusalem: Israel Program Sci. Transl. 1973
Swift, E. and E. G. Durbin: The phased division and cytological characteristics of Pyrocystis spp. can be used to estimate doubling times of their populations in the sea. Deep-Sea Res. 19, 189–198 (1972)
Swift, E., M. Stuart and V. Meunier: The in situ growth rates of some deep living oceanic dinoflagellates: Pyrocystis fusiformis and Pyrocystis noctiluca. Limnol. Oceanogr. 21, 418–426 (1976)
Swift, E. and V. Meunier: The effect of light intensity on division rates, stimulable bioluminescence, and cell size of the oceanic dinoflagellates Dissodinium lunula, Pyrocystis fusiformis and P. noctiluca. J. Phycol. 12, 14–22 (1976)
Swift, E., V. Meunier, W. H. Biggley, J. Hoarau and J. Barras: Factors affecting bioluminescent capacity in oceanic dinoflagellates. In: Bioluminescence current perspectives, pp 95–106. Ed. by K. H. Nealson. Minneapolis, MN: Burgess Pub. 1981
Swift, E., M. Voytek, R. Rivkin and W. Biggley: Ceratium division rates in the Gulf Stream and Sargasso Sea. AGU/ASLO, San Antonio, TX. Feb. 1982
Taylor, F. J. R.: General features of dinoflagellate material collected by the Anton Brunn during the International Indian Ocean Expedition. In: The biology of the Indian Ocean, pp 155–169. Ed. by B. Zeitzschel. Ecol. Stud., Vol. 3. New York: Springer 1973
Thomas, W. H.: On nitrogen deficiency in tropical Pacific oceanic phytoplankton. Photosynthetic parameters of rich and poor water. Limnol. Oceanogr. 15, 380–385 (1970a)
Thomas, W. H.: Effects of ammonia and nitrate concentrations on chlorophyll increases in natural Pacific phytoplankton populations. Limnol. Oceanogr. 15, 386–392 (1970b)
Thomas, W. H. and A. N. Dodson: Effects of phosphate concentration on cell division rates and yield of a tropical oceanic diatom. Biol. Bull. mar. biol. Lab., Woods Hole 134, 199–208 (1968)
Voytek, M. A.: Species-specific cell division and carbon production dynamics for natural populations of Ceratium spp. and Cerataccorys horrida, 104 pp. Masters thesis, University of Rhode Island 1984
Weiler, C. S.: Population structure and in situ division rates of Ceratium in oligotrophic waters of the North Pacific central gyre. Limnol. Oceanogr. 25, 610–619 (1980)
Wood, E. P., F. A. J. Armstrong and R. A. Richards: Determination of nitrate in sea water by cadmium-copper reduction to nitrite. J. mar. Biol. Ass. U.K. 47, 23–31 (1967)
Wynne, D. and T. Berman: Hot water extractable phosphorus — an indicator of the nutritional status of Peridinium cinctum (Dinophyeae). J. Phycol. 16, 40–46 (1980)
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Rivkin, R.B., Swift, E. Phosphorus metabolism of oceanic dinoflagellates: phosphate uptake, chemical composition and growth of Pyrocystis noctiluca . Mar. Biol. 88, 189–198 (1985). https://doi.org/10.1007/BF00397166
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DOI: https://doi.org/10.1007/BF00397166