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Species differences in accumulation of nitrogen pools in phytoplankton

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Abstract

The changes in the intracellular concentrations of nitrate, ammonium, free amino acids, protein, DNA, RNA and total nitrogen were measured in batch cultures of seven species of marine phytoplankton as they progressed from being nitrogen sufficient to being nitrogen starved. After several days of nitrogen starvation, either nitrate or ammonium was added to the cultures, and the measurements were continued for 10 to 36 h. By this means it was possible to assess the long-term and short-term changes in cellular nitrogen compounds and how they relate to phytoplankton nitrogen uptake and growth. Considerable species differences were observed in the amounts and kinds of nitrogen compounds which were stored and the degree to which the utilization of these compounds could support growth if the external nitrogen supply is low or variable. Despite the species variation, the results suggest that the concentrations or ratios of a number of intracellular nitrogen compounds can be used to assess the nitrogen deficiency and/or growth rate of natural phytoplankton populations.

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Literature cited

  • Armitage, M. E. and R. J. Morris: The effect of changing environmental salinity on the free amino-acid composition of an estuarine population of Neomysis integer. Est mar. coast. Shelf Sci. 14, 301–311 (1982)

    Google Scholar 

  • Aspinall, D. and L. G. Paleg: Proline accumulation: physiological aspects. In: Physiology and biochemistry of drought resistance in plants, pp 205–241. Ed. by L. G. Paleg and D. Aspinall. Sydney, Australia: Academic Press 1981

    Google Scholar 

  • Brown, L. M. and J. A. Hellebust: Sorbital and proline as intracellular osmotic solutes in the green alga Stichococcus bacillaris. Can. J. Bot. 56, 676–679 (1978)

    Google Scholar 

  • Bryant, D. A., G. Guglielmi, N. Tandeau de Marsac, A. N. Castets and G. Cohen-Bazire: The structure of cyanobacterial phycobilisomes: a model. Arch. Microbiol. 123, 113–127 (1979)

    Google Scholar 

  • Caperon, J. and J. Meyer: Nitrogen-limited growth of phytoplankton I. Changes in population characteristics with steady-state growth rate. Deep-Sea Res. 19, 601–618 (1972)

    Google Scholar 

  • Chan, A. T.: Comparative physiological study of marine diatoms and dinoflagellates in relation to irradiance and cell size. J. Phycol. 14, 396–402 (1978)

    Google Scholar 

  • Clarke, M. R., E. J. Denton and J. B. Gelpen-Brown: On the use of ammonium for buoyancy in squid. J. mar. biol. Ass. U.K. 59, 259–276 (1979)

    Google Scholar 

  • Collos, Y.: Transient situations in nitrate assimilation by marine diatoms. I. Changes in uptake parameters during nitrogen starvation. Limnol. Oceanogr. 25, 1075–1081 (1980)

    Google Scholar 

  • Collos, Y.: Transient situations in nitrate assimilation by marine diatoms. III. Short-term uncoupling of nitrate uptake and reduction. J. exp. mar. Biol. Ecol. 62, 285–296 (1982)

    Google Scholar 

  • Cook, R. J. and C. Anthony: Regulation by glutamine of ammonia transport in Aspergillus nidulans. Microbiol. 109, 275–286 (1978)

    Google Scholar 

  • Conover, S. A. M.: Partitioning of nitrogen and carbon in cultures of the marine diatom Thalassiosira fluviatilis supplied with nitrate, ammonium, or urea. Mar. Biol. 32, 231–246 (1975)

    Google Scholar 

  • Conway, H. L. and P. J. Harrison: Marine diatoms grown in chemostats under silicate or ammonium limitation IV. Transient response of Chaetoceros gracilis, Skeletonema costatum and Thalassiosira gravida to a single addition of the limiting nutrient. Mar. Biol. 43, 33–43 (1977)

    Google Scholar 

  • Conway, H. L., P. J. Harrison and C. O. Davis: Marine diatoms grown in chemostats under silicate or ammonium limitation II. Transient response of Skeletonema costatum to a single addition of the limiting nutrient. Mar. Biol. 35, 187–199 (1976)

    Google Scholar 

  • Cowey, C. B. and E. D. S. Corner: Amino acids and some other nitrogenous compounds in Calanus finmarchicus. J. mar. biol. Ass. U.K. 43, 485–493 (1963)

    Google Scholar 

  • Crissman, H. A. and J. A. Steinkamp: Rapid, one step staining procedures for analysis of cellular DNA and protein by single and dual laser flow cytometry. Cytometry 3, 84–90 (1982)

    Google Scholar 

  • Davis, C. O.: Lighting systems. In: Phytoplanktor, growth dynamics. Vol. 1, pp 19–23. Ed. by S. P. Pavlou. Seattle, WA: University of Washington Special Report 52, 1972

  • Demanche, J. M., H. C. Curl, Jr., D. W. Lundy and P. L. Donaghay: The rapid response of the marine diatom Skeletonema costatum to changes in external and internal nutrient concentration. Mar. Biol. 53, 323–333 (1979)

    Google Scholar 

  • Dortch, Q.: Nitrate and ammonium uptake and assimilation by three marine diatoms, 299 pp. Ph. D. Thesis, University of Washington 1980

  • Dortch, Q.: Effect of growth conditions on accumulation of internal nitrate, ammonium, amino acids, and protein in three marine diatoms. J. exp. mar. Biol. Ecol. 61, 242–264 (1982)

    Google Scholar 

  • Dortch, Q., S. I. Ahmed and T. T. Packard: Nitrate reductase and glutamate dehydrogenase activities in Skeletonema costatum as measures of nitrogen assimilation rates. J. Plank. Res. 1, 169–186 (1979)

    Google Scholar 

  • Dortch, Q., J. R. Clayton, Jr., S. S. Thoresen, S. L. Bressler and S. I. Ahmed: Response of marine phytoplankton to nitrogen deficiency: decreased nitrate uptake vs enhanced ammonium uptake. Mar. Biol. 70, 13–19 (1982)

    Google Scholar 

  • Dortch, Q., T. L. Roberts, J. R. Clayton, Jr. and S. I. Ahmed: RNA/DNA ratios and DNA concentrations as indicators of growth rate and biomass in planktonic marine organisms. Mar. Ecol. Prog. Ser. 13, 61–71 (1983)

    Google Scholar 

  • Friedrich, G. E. and T. E. Whitledge: Autoanalyzer procedures for nutrients. In: Phytoplankton growth dynamics Vol. I, pp 38–55. Ed. by S. P. Pavlou, Seattle, WA: University of Washington Special Report 52, 1972

  • Gardner, W. S. and W. H. Miller, III.: Intracellular composition and net release rates of free amino acids in Daphnia magna. Can. J. Fish aquat. Sci. 38, 157–162 (1981)

    Google Scholar 

  • Gardner, W. S. and D. Scavia: Kinetic examination of nitrogen release by zooplankters. Limnol. Oceanogr. 26, 801–810 (1981)

    Google Scholar 

  • Glibert, P. M. and J. C. Goldman: Rapid ammonium uptake by marine phytoplankton. Mar. Biol. Lett. 2, 25–31 (1981)

    Google Scholar 

  • Goldman, J. C. and P. M. Glibert: Comparative rapid ammonium uptake by four species of marine phytoplankton. Limnol. Oceanogr. 27, 814–827 (1982)

    Google Scholar 

  • Guillard, R. R. L. and J. H. Ryther: Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229–239 (1962)

    Google Scholar 

  • Harrison, P. J., H. L. Conway, R. W. Holmes and C. O. Davis: Marine diatoms grown in chemostats under silicate or ammonium limitation III. Cellular chemical composition and morphology of Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida. Mar. Biol. 43, 19–31 (1977)

    Google Scholar 

  • Hitchcock, G. L.: A comparative study of the size-dependent organic composition of marine diatoms and dinoflagellates. J. Plank. Res. 4, 363–377 (1982)

    Google Scholar 

  • Horrigan, S. G. and J. J. McCarthy: Phytoplankton uptake of ammonium and urea during growth on oxidized forms of nitrogen. J. Plank. Res. 4, 379–389 (1982)

    Google Scholar 

  • Huffaker, R. C. and L. W. Peterson: Protein turnover in plants and possible means of its regulation. Annu. Rev. Plant Physiol. 25, 363–392 (1974)

    Google Scholar 

  • Jeffries, H. P.: Seasonal composition of temperate plankton communities: free amino acids. Limnol. Oceanogr. 14, 41–52 (1969)

    Google Scholar 

  • Kessler, H.: Beitrag zur Kenntnis der chemischen und physikalischen Eigenschaften des Zellsaftes von Noctiluca miliaris. Veröff Inst. Meeresforsch. Bremerhaven 2, 357–368 (1966)

    Google Scholar 

  • Kester, D. R., I. W. Duedall, D. N. Connors and R. M. Pytkowicz: Preparation of artificial seawater. Limnol. Oceanogr. 12, 176–179 (1967)

    Google Scholar 

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

    Google Scholar 

  • McCarthy, J. J. and J. C. Goldman: Nitrogenous nutrition of marine phytoplankton in nutrient depleted waters. Science, N.Y. 203, 670–672 (1979)

    Google Scholar 

  • Packard, T. T. and Q. Dortch: Particulate protein-nitrogen in north Atlantic surface waters. Mar. Biol. 33, 347–354 (1975)

    Google Scholar 

  • Packard, T. T., T. M. Moore and D. A. Harmon: Biochemical assays. In: Phytoplankton growth dynamics. Vol. I, pp 119–130. Ed. by S. P. Pavlou, Seattle, WA: University of Washington Special Report 52, 1972

  • Perry, M. J., M. C. Talbot and R. S. Alberte: Photoadaption in marine phytoplankton: response of the phytosynthetic unit. Mar. Biol. 62, 91–101 (1981)

    Google Scholar 

  • Perry, M. J., M. C. Talbot, J. C. Smith, and N. A. Welschmeyer: Nitrogen limitation in marine phytoplankton: response of the photosynthetic apparatus. (In preparation)

  • Prasad, A. S., E. DuMochelle, D. Konvich and D. Oberleas: A simple fluorometric method for the determination of RNA and DNA in tissues. J. lab. clin. Med. 80, 598–602 (1972)

    Google Scholar 

  • Rhee, G.-Y.: Dual nutrient limitation. Limnol. Oceanogr. 23, 10–25 (1978)

    Google Scholar 

  • Sim, A. P., B. F. Folkes and A. H. Bussey: Mechanisms involved in the regulation of nitrogen assimilation in microorganisms and plants. In: Recent aspects of nitrogen metabolism in plants. pp 92–114. Ed. by E. J. Hewitt and C. V. Cutting. New York: Academic Press (1968)

    Google Scholar 

  • Solórzano, L. and J. H. Sharp: Determination of total dissolved nitrogen in natural waters. Limnol. Oceanogr. 25, 751–754 (1980)

    Google Scholar 

  • Stanier, R. Y. and G. Cohen-Bazire: Phototrophic prokaryotes: the cyanobacteria. Annu. Rev. Microbiol. 31, 225–274 (1977)

    Google Scholar 

  • Stanley, S. O., and C. M. Brown: Inorganic nitrogen metabolism in marine bacteria: the intracellular free amino acid pools of a marine pseudomonad. Mar. Biol. 38, 101–109 (1976)

    Google Scholar 

  • Syrett, P. J.: Nitrogen metabolism of microalgae. Can. Bull. Fish Aquat. Sci. 210, 182–210 (1981)

    Google Scholar 

  • Thoresen, S. S., Q. Dortch and S. I. Ahmed: Comparison of methods for extracting intracellular pools of inorganic nitrogen from marine phytoplankton. J. Plank. Res. 4, 695–704 (1982)

    Google Scholar 

  • Thoresen, S. S., J. R. Clayton, Jr., Q. Dortch and S. I. Ahmed: A rapid technique for the determination of RNA and DNA in marine phytoplankton. J. Plank. Res. 5, 253–261 (1983)

    Google Scholar 

  • Turpin, D. H. and P. J. Harrison: Fluctuations in free amino acid pools of Gymnodinium splendens (Dinophyceae) in response to an ammonia perturbation: evidence for GS pathway. J. Phycol. 14, 461–464 (1978)

    Google Scholar 

  • Undenfriend, S., S. Stein, P. Böhlen, W. Dairman, W. Leimgruber and M. Weigle: Fluorescamine: a reagent for assay of amino acids peptides, proteins, and primary amines in the picomole range. Science N.Y. 178, 871–873 (1972)

    Google Scholar 

  • Wheeler, P. A.: Use of methylammonium as an ammonium analogue in nitrogen transport and assimilation studies with Cyclotella cryptica (Bacillariophyceae). J. Phycol. 16, 328–334 (1980)

    Google Scholar 

  • Wheeler, P. A., P. N. Glibert and J. J. McCarthy: Ammonium uptake and incorporation by Chesapeake Bay phytoplankton: short term uptake kinetics. Limnol. Oceanogr. 27, 1113–1128 (1982)

    Google Scholar 

  • Wynn-Jones, R. G. and R. Storey: Betaines. In: Physiology and biochemistry of drought resistance in plants, pp 171–204. Ed. by L. G. Paleg and D. Aspinall Sydney: Academic Press 1981

    Google Scholar 

  • Yentsch, C. M., P. K. Horan, K. Muirhead, Q. Dortch, E. Haugen, L. Legendre, L. S. Murphy, M. J. Perry, D. Phinney, S. A. Pomponi, R. W. Spinrad, M. Wood, C. S. Yentsch and B. J. Zahuranec. Flow cytometry and cell sorting: a powerful technique with potential applications in aquatic sciences. Limnol. Oceanogr. 28, 1275–1280 (1983)

    Google Scholar 

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Author notes

  1. Q. Dortch

    Present address: Bigelow Laboratory for Ocean Sciences, McKown Point, 04575, West Boothbay Harbor, Maine, USA

Authors and Affiliations

  1. School of Oceanography, University of Washington, 98195, Seattle, Washington, USA

    Q. Dortch, S. S. Thoresen & S. I. Ahmed

  2. School of Fisheries, University of Washington, 98195, Seattle, Washington, USA

    J. R. Clayton Jr.

Authors
  1. Q. Dortch
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  2. J. R. Clayton Jr.
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  3. S. S. Thoresen
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  4. S. I. Ahmed
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Additional information

Communicated by R. W. Doyle, Halifax

Contribution No. 1373 from the School of Oceanography, University of Washington and Contribution No. 83006 from the Bigelow Laboratory for Ocean Sciences

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Dortch, Q., Clayton, J.R., Thoresen, S.S. et al. Species differences in accumulation of nitrogen pools in phytoplankton. Marine Biology 81, 237–250 (1984). https://doi.org/10.1007/BF00393218

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