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Effect of diel photoperiod on nitrogen metabolism of cultured and symbiotic zooxanthellae

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Abstract

Ammonium uptake and assimilation by zooxanthellae (Symbiodinium sp.) cultured with an excess of nitrate was enhanced in light. Uptake was decreased by the same amount when zooxanthellae were incubated in darkness either after 6 h pretreatment in light, or at the end of the dark period of a 12 h light: 12 h dark cycle. This suggested that short-term incubations of zooxanthellae were valid tests for light enhancement of dissolved inorganic nitrogen (DIN) uptake. Assimilation of ammonium into glutamine (Gln) and glutamate (Glu) was also decreased in darkness. During a 12 h light: 12 h dark cycle, free pools of both Gln and Glu fell quickly at the start of the light period, followed by steady increases until the beginning of the next dark period. Of the four other major components of free amino acid pools tested, only the nonprotein amino acid taurine showed diel fluctuations. Gln and Glu pools in zooxanthellae freshly isolated from reef-forming corals also showed differences between day and night, suggesting changes in patterns of DIN assimilation over the diurnal cycle.

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References

  • Anderson SL, Burris JE (1987) Role of glutamine synthetase in ammonia assimilation by symbiotic marine dinoflagellates (zooxanthellae). Mar Biol 94: 451–458

    Google Scholar 

  • Burris RH (1983) Uptake and assimilation of 15NH +4 by a variety of corals. Mar Biol 75: 151–155

    Google Scholar 

  • Cates N, McLaughlin JJA (1976) Differences of ammonia metabolism in symbiotic and aposymbiotic Condylactus and Cassiopea spp. J exp mar Biol Ecol 37: 31–41

    Google Scholar 

  • Cochlan WP, Harrison PJ, Denman KL (1991) Diel periodicity of nitrogen uptake by marine phytoplankton in nitrate-rich environments. Limnol Oceanogr 36: 1689–1700

    Google Scholar 

  • Cook CB, D'Elia CF (1987) Are natural populations of zooxanthellae ever nutrient-limited? Symbiosis 4: 199–212

    Google Scholar 

  • Cook CB, D'Elia CF, Muller-Parker G (1988) Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida. Mar Biol. 98: 253–262

    Google Scholar 

  • Cook CB, Fitt WK (1990) Some effects of dissolved inorganic nutrients on the growth of zooxanthellae in the hydroid Myrionema amboinese. In: Nardon P, Gianinazzi-Pearson V, Grenier AM, Margulis L, Smith DC (eds) Endocytobiology. IV. INRA, Paris, pp 285–288

    Google Scholar 

  • Cook CB, Muller-Parker G, D'Elia CF (1992) Ammonium enhancement of dark carbon fixation and nitrogen limitation in symbiotic zooxanthellae: effects of feeding and starvation of the sea anemone Aiptasia pallida. Limnol Oceanogr 37: 131–139

    Google Scholar 

  • Cook CB, Muller-Parker G, Orlandini CD (1994) Ammonium enhancement of dark carbon fixation and nitrogen limitation in zooxanthellae symbiotic with the reef corals Madracis mirabilis and Montastrea annularis. Mar Biol 118: 157–165

    Google Scholar 

  • Craggs RJ, McAuley PJ, Smith VJ (1994) Batch culture screening of marine microalgal nutrient removal from primary sewage effluent. Hydrobiologca 288: 157–166

    Google Scholar 

  • D'Elia CF, Cook CB (1988) Methylamine uptake by zooxanthellae —invertebrate symbioses: insights into host ammonium environment and nutrition. Limnol Oceanogr 33: 1153–1165

    Google Scholar 

  • D'Elia CF, Domotor SL, Webb KL (1983) Nutrient uptake kinetics of freshly isolated zooxanthellae. Mar Biol 75: 157–167

    Google Scholar 

  • D'Elia CF, Webb KL (1977) The dissolved nitrogen flux of reef corals. Proc 3rd int coral Reef Symp 1: 325–330 [Taylor DL (ed) Rosenstiel School of Marine and Atmospheric Science, University of Miami]

    Google Scholar 

  • D'Elia CF, Wiebe WJ (1990) Biogeochemical cycles in coral-reef ecosystems. In: Dubinsky Z (ed) Ecosystems of the World. 25. Coral Reefs. Elsevier Science Publishers, Amsterdam, pp 39–74

    Google Scholar 

  • Domotor SL, D'Elia CF (1984) Nutrient uptake kinetics and growth of zooxanthellae maintained in laboratory culture. Mar Biol 80: 93–101

    Google Scholar 

  • Dubinsky Z, Stambler N, Ben-Zion M, McCloskey LR, Muscatine L, Falkowski PG (1990) The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc R Soc (Ser B) 239: 231–246

    Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. BioSci. 43: 606–611

    Google Scholar 

  • Fitt WK, Chang SS, Trench RK (1981) Motility patterns of different strains of the symbiotic dinoflagellate Symbiodinium microadriaticum (=Gymnodinium microadriaticum) (Freudenthal) in culture. Bull mar Sci 31: 436–443

    Google Scholar 

  • Fitt WK, Cook CB (1990) Some effects of host feeding on growth of zooxanthellae in the marine hydroid Myrionema amboinese in the laboratory and in nature. In: Nardon P, Gianinazzi-Pearson V, Grenier AM, Margulis L, Smith DC (eds) Endocytobiology. IV INRA, Paris, pp 281–284

    Google Scholar 

  • Flynn KJ (1990) The determination of nitrogen status in microalgae. Mar Ecol Prog Ser 61: 297–307

    Google Scholar 

  • Flynn KJ, Dickson DMJ, Al-Amoudi OA (1989) The ratio of glutamine: glutamate in microalgae: a biomarker for N-status suitable for use at natural cell densities. J Plankton Res 11: 165–170

    Google Scholar 

  • Flynn K, Flynn KJ, Jones KJ (1993) Changes in dinoflagellate intracellular amino acids in response to diurnal changes in light and N supply. Mar Ecol Prog Ser 100: 245–252

    Google Scholar 

  • Flynn KJ, Hipkin CR (1990) Changes in intracellular amino acids and glutamine: glutamate during N-deprivation and refeeding in Candida nitratophila. New Phytol 114: 435–440

    Google Scholar 

  • Franzisket L (1973) Uptake and accumulation of nitrate and nitrite by reef corals. Naturwissenschaften 12: p. 552

    Google Scholar 

  • Franzisket L (1974) Nitrate uptake by reef corals. Int Revue ges Hydrobiol 59: 1–7

    Google Scholar 

  • Gladfelter EH (1983) Spatial and temporal patterns of mitosis in the cells of the axial polyp of the reef coral Acropora cervicornis. Biol Bull mar biol Lab, Woods Hole 165: 811–815

    Google Scholar 

  • Hoegh-Guldberg O (1994) Population dynamics of symbiotic zooxanthellae in the coral Pocillopora damicornis exposed to elevated ammonium [(NH4)2SO4] concentrations. Pacif Sci 48: 263–272

    Google Scholar 

  • Hoegh-Guldberg O, Smith GJ (1989) Influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Mar Ecol Prog Ser 57: 173–186

    Google Scholar 

  • Kanda J, Ziemann DA, Conquest LD, Biefang PK (1989) Light-dependency of nitrate uptake by phytoplankton over the spring bloom in Auke Bay, Alaska. Mar Biol 103: 563–569

    Google Scholar 

  • Kawaguti S (1953) Ammonium metabolism of the reef corals. Biol J Okayama Univ 1: 171–176

    Google Scholar 

  • Lerch KA, Cook CB (1984) Some effects of photoperiod on the motility rhythm of cultured zooxanthellae. Bull mar Sci 34: 477–483

    Google Scholar 

  • Levasseur M, Thompson PA, Harrison PJ (1993) Physiological acclimation of marine phytoplankton to different nitrogen sources. J Phycol 29: 587–595

    Google Scholar 

  • McAuley PJ (1992) The effect of maltose release on growth and nitrogen metabolism of symbiotic Chlorella. Br Phycol J 27: 417–422

    Google Scholar 

  • McAuley PJ (1994) Amino acid content of zooxanthellae freshly isolated from Pocillopora damicornis. Pacif Sci 48: 247–253

    Google Scholar 

  • McAuley PJ, Cook CB (1994) Effects of host feeding and dissolved ammonium on cell division and nitrogen status of zooxanthellae in the hydroid Myrionema amboinense. Mar Biol 121: 343–348

    Google Scholar 

  • McIsaac JJ, Dugdale RC (1972) Interaction of light and inorganic nitrogen in controlling nitrogen uptake in the sea. Deep-Sea Res 19: 209–232

    Google Scholar 

  • Miflin BJ, Lea PJ (1976) Review: the pathway of nitrogen assimilation in plants. Phytochem 15: 873–885

    Google Scholar 

  • Muller-Parker G, McCloskey LR, Hoegh-Guldberg O, McAuley PJ (1994) Response of animal-algal biomass of the coral Pocillopora damicornis to seawater ammonium enrichment. Pacif Sci 48: 273–283

    Google Scholar 

  • Muscatine L (1980) Uptake, retention, and release of dissolved inorganic nutrients by marine alga — invertebrate associations. In: Cook CB, Pappas PW, Rudolf ED (eds) Cellular interactions in symbiosis and parasitism. Ohio State University Press, Columbus, Ohio, pp 229–244

    Google Scholar 

  • Muscatine L, D'Elia CF (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23: 725–734

    Google Scholar 

  • Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Soc (Ser B) 236: 311–324

    Google Scholar 

  • Muscatine L, Marian RE (1982) Dissolved inorganic flux in symbiotic and nonsymbiotic medusae. Limnol Oceanogr 27: 910–918

    Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioSci 27: 454–459

    Google Scholar 

  • Provasali L (1966) Media and prospects for the cultivation of marine algae. In: Watanbe A, Hattori R (eds) Cultures and collections of algae. University Press, Tokyo, pp 63–75

    Google Scholar 

  • Rahav O, Falkowski P, Dubinsky Z, Achituv Y (1989) Ammonium metabolism in the zooxanthellate coral Stylophora pistillata. Proc R Soc (Ser B) 236: 325–337

    Google Scholar 

  • Rees TAV (1989) The green hydra symbiosis and ammonium. II. Ammonium assimilation and release by freshly isolated symbionts and cultured algae. Proc R Soc (Ser B) 235: 365–382

    Google Scholar 

  • Spencer-Davies P (1992) Endosymbiosis in marine cnidarians. In: John DM, Hawkins SJ, Price JH (eds) Systematics Association Special Volume. No. 46, Plant — animal interactions in the marine benthos. Clarendon Press, Oxford pp 511–540

    Google Scholar 

  • Stambler N, Popper N, Dubinsky Z, Stimson J (1991) Effects of nutrient enrichment and water motion on the coral Pocillopora damicornis. Pacif Sci 45: 299–307

    Google Scholar 

  • Summons RE, Boag TS, Osmond CB (1986) The effect of ammonium on photosynthesis and the pathway of ammonium assimilation in Gymnodinium microadriatieum in vitro and in symbiosis with tridacnid clams and corals. Proc R Soc (Ser B) 227: 147–159

    Google Scholar 

  • Turpin D (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27: 14–20

    Google Scholar 

  • Wilkerson FP, Muller-Parker G, Muscatine L (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28: 1009–1014

    Google Scholar 

  • Wilkerson FP, Muscatine L (1984) Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic sea anemone. Proc R Soc (Ser B) 221: 71–86

    Google Scholar 

  • Wilkerson FP, Trench RK (1986) Uptake of dissolved morganic nitrogen by the symbiotic clam Tridacna gigas and the coral Acropora sp. Mar Biol 93: 237–246

    Google Scholar 

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Authors and Affiliations

  1. School of Biological and Medical Sciences, University of St. Andrews, Sir Harold Mitchell Building, KY16 8LB, St. Andrews, Fife, Scotland

    P. J. McAuley

  2. School of Biological and Medical Sciences, Gatty Marine Laboratory, University of St. Andrews, KY16 8LB, St. Andrews, Fife, Scotland

    V. J. Smith

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  1. P. J. McAuley
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  2. V. J. Smith
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Communicated by J. Mauchline, Oban

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McAuley, P.J., Smith, V.J. Effect of diel photoperiod on nitrogen metabolism of cultured and symbiotic zooxanthellae. Marine Biology 123, 145–152 (1995). https://doi.org/10.1007/BF00350333

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  • DOI: https://doi.org/10.1007/BF00350333

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