Abstract
The effects of nitrate limitation and nitrate starvation on the photochemical efficiency of photosystem II (Fv/F m) were examined in batch cultures of two species of symbiotic dinoflagellates, Symbiodinium kawagutii and S. pilosum. F v/F m values were determined along growth curves and show that the F v/F m values are negatively correlated with external nitrogen concentrations in cultures of both species. Changes in growth irradiances in the batch cultures due to increments of the cell densities were estimated S. kawagutii cultures showed a negative correlation between F v/F m and growth irradiance. These results indicate that F v/F m is dependent on the light history of the cultures and on the individual sensitivity of each species, and independent of their nutrient status. Nitrate starvation was analyzed by measuring changes in the quantum yield of fluorescence (Fv/F m), electron transport rate (ETR) and non-photochemical quenching (NPQ) at five time points along the growth curves under three conditions: control (C), without nitrogen (N−), and with ammonia (N+) as a nitrogen source sufficient to meet daily nitrogen requirements. Cells collected during the exponential growth phase and exposed to N− and N+ showed significant reductions in their maximum ETR relative to controls (20% in S. pilosum and 40% in S. kawagutii). The loss of electron transport capacity is consistent with a sink limitation rather than the result of nitrogen starvation. Under nitrate-starvation, the induction of NPQ resulted in effective protection against photosystem II damage in S. pilosum. In contrast, S. kawagutii cells failed to induced NPQ resulting in a concomitant increase in the excitation pressure over photosystem II leading to damage. Collectively the data indicate that F v/F m is not a robust indicator of nitrogen limitation in symbiotic dinoflagellates and that protection against photosystem II damage under sink limitations, is largely dependent on the differential capacities of each species to induce NPQ.
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Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinean coral Galaxea fascicularis. Mar Biol 142:419–426
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185
Blank RJ (1987) Cell architecture of the dinoflagellate Symbiodinium sp. Inhabiting the Hawaiian coral Montipora verrucosa. Mar Biol 94:143–155
Brodribb T, Hill RS (1997) Light response characteristics of a morphologically diverse group of southern hemisphere conifers as measured by chlorophyll fluorescence. Oecologia 110:10–17
Brown BE, Dunne RP, Goodson MS, Douglas AE (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21:119–126
Chang SS, Prézelin BB, Trench RK (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol 76:219–229
Cullen J, Yang X, MacIntyre HL (1992) Nutrient limitation and marine photosynthesis. In: Falkowski PG, Woodhead AD (eds) Primary productivity and biogeochemical cycles in the sea. Plenum, New York pp 69–88
Enríquez S, Merino M, Iglesias-Prieto R (2002) Variations in the photosynthetic performance along the leaves of the tropical seagrass Thalassia testudinum. Mar Biol 140:891–900
Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174
Falkowski PG, Kolber Z (1993) Estimation of phytoplankton photosynthesis by active fluorescence. Mar Sci Symp 197:92–103
Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Ammonium ions and organic materials maintain the density of zooxanthellae. BioScience 43:606–611
Geider RJ, LaRoche J, Greene R, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum triconutum (Bacillariophyceae) to nitrate, phosphate or iron starvation. J Phycol 29:755–766
Gorbunov M, Kolber ZS, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46:75–85
Goreau TF, Goreau NI (1959) The physiology of skeletal formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239–250
Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86
Iglesias-Prieto R (1997) Temperature-dependent inactivation of photosystem II in symbiotic dinoflagellates. Proc 8 th Intl Coral Reef Symp 2:1313–1318
Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Response of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 133:163–175
Iglesias-Prieto R, Trench RK (1997a) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of the chlorophyll-protein complex to different photon-flux densities. Mar Biol 130:23–33
Iglesias-Prieto R, Trench RK (1997b) Photoadaptation, photoacclimation and niche diversification in invertebrate-dinoflagellate symbioses. Proc 8 th Intl Coral Reef Symp 2:1319–1324
Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) The photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305
Iglesias-Prieto R, Govind NS, Trench RK (1993) Isolation and characterization of three membrane-bound chlorophyll-protein complexes from four dinoflagellate species. Phil Trans R Soc London B 340:381–392
Jones RJ, Hoegh-Guldberg O (2001) Diurnal variations in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99
Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230
Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge
Kolber Z, Zehr J, Falkowski PG (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol 88:923–929
LaJeunesse TC (2001) Investigating the biodiversity, ecology and phylogeny of endosymbiotic dinoflagellates of the genus Symbiodinium using the internal transcribed spacer region: in search of a “species” level marker. J Phycol 37:866–880
LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
LaRoche J, Geider RJ, Graziano LM, Murray H, Lewis K (1993) Induction of specific proteins in eukaryotic algae grown under iron-, phosphorus-, or nitrogen-deficient conditions. J. Phycol 29:767–777
Lesser MP (1996) Exposures of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis. Limnol Oceanogr 41:271–283
Lesser MP, Gorbunov M (2001) Diurnal and bathymetric changes in chlorophyll fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer. Mar Ecol Prog Ser 212:69–77
Levasseur M, Thompson PA, Harrison PJ (1993) Physiological acclimation of marine phytoplankton to different nitrogen sources. J Phycol 29:587–595
MacIntyre JG, Cullen JJ, Cambella AD (1997) Vertical migration, nutrition and toxicity in the dinoflagellate Alexandrium tamarense. Mar Ecol Prog Ser 148:201–216
Maxwell DP, Falk S, Trick CG, Huner NP (1994) Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol 105:535–543
Muscatine L (1980) Productivity of zooxanthellae. In: Falkowski PG (ed) Primary productivity in the sea. Plenum press, New York, pp 381–402
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments BioScience 27:454–460
Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611
Muscatine L, Falkowski PG, Dubinsky Z, Cook DA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthelae in a reef coral. Proc R Soc London B 236:311–324
Olaizola M, Geider RJ, Harrison WG, Graziano LM, Ferrari GM, Schlittnhardt PM (1996) Synoptic study of variations in the fluorescence-based maximum quantum efficiency of photosynthesis across the North Atlantic Ocean. Limnol Oceanogr 41:755–765
Öquist G, Anderson JM, McCaffery S, Chow WS (1992) Mechanistic difference in photoinhibition of sun and shade plants. Planta 188:422–431
Parkhill JP, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529
Rhiel E, Krupinska K, Wehrmeyer W (1986) Effects of nitrogen starvation on the function and organization of the photosynthetic membranes in Cryptomonas maculata (Cryptophyceae). Planta 169:361–369
Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J. Phycol 34:407–417
Ruban AV, Horton P (1995) Regulation of non-photochemical quenching of chlorophyll fluorescence in plants. Aust J Plant Physiol 22:221–230
Shibata K (1959) Spectrophotometry of translucent biological materials-opal glass transmission method. Methods Biochem Anal 7:77–109
Stanley GD (2003) The evolution of modern corals and their early history. Earth-Sci Rev 60:195–225
Steglich C, Behrenfeld M, Koblizek M, Claustre H, Penno S, Prasil O, Partensky F, Hess WR (2001) Nitrogen deprivation strongly affects photosystem II but not phycoerythrin level in the divinyl-chlorophyll b -containing cyanobacterium Prochlorococcus marinus. Biochim Biophys Acta 1503:341–349
Strickland JDH, Parsons TR (1972) A manual of sea water analysis. Fisheries Research Board of Canada, Vancouver
Trench RK (1997) Diversity of symbiotic dinoflagellates and the evolution of microalgal-invertebrate symbioses Proc 8 th Intl Coral Reef Symp 2:1275–1286
Warner ME, Fitt WK, Schmidt GM (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from different species of reef corals: a novel approach. Plant Cell Environ 19:291–299
Warner ME, Fitt WK, Schmidt GM (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012
Winters G, Loya Y, Röttgers R, Beer S (2003) Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ. Limnol Oceanogr 48:1388–1393
Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinherdtii. Plant Physiol 117:129–139
Acknowledgements
We thank Sergio Castillo for his help during the nutrient analyses, Martín Merino and Susana Enríquez for their helpful comments, and Ania Banaszak and Paul Blanchon for their editorial assistance. A.R.-R. was supported by a graduate scholarship (95358) from the National Council for Science and Technology (CONACYT). This work was funded by CONACYT (32517-T) and DGAPA (IN215197) grants to R.I.-P.
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Communicated by P.W. Sammarco, Chauvin
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Rodríguez-Román, A., Iglesias-Prieto, R. Regulation of photochemical activity in cultured symbiotic dinoflagellates under nitrate limitation and deprivation. Marine Biology 146, 1063–1073 (2005). https://doi.org/10.1007/s00227-004-1529-x
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DOI: https://doi.org/10.1007/s00227-004-1529-x