Abstract
The effect of ammonium concentration on photosynthetic activity estimated as in vivo chlorophyll fluorescence, i.e. maximal quantum yield (Fv/Fm) and electron transport rate (ETR) and on the accumulation of mycosporine-like amino acids (MAAs), chlorophyll a (chl a), biliproteins (BP) and soluble proteins (SP) in the red algae Porphyra leucosticta Thuret in Le Jolis collected from Lagos (Málaga, Spain) and Porphyra umbilicalis (Linnaeus) J. Agardh from Helgoland (Germany) was evaluated. Discs of both species were incubated with three ammonium concentrations (0, 100 and 300 µM) under artificial PAR and UV radiation for 7 days. Photosynthetic activity decreased under the culture conditions due to UV radiation and ammonium availability. The decrease of both Fv/Fm and maximal ETR was related to ammonium supply, i.e. the lowest decrease occurred in algae growing with the highest concentration of ammonium. In both species, after 7 days of culture, the content of chl a, BP and SP was higher under 300 µM than that under 0 and 100 µM ammonium. In both species, the content of MAAs was increased under 300 µM ammonium compared to the initial value, whereas a decrease under 0 and 100 µM ammonium was observed only in P. leucosticta. The content of MAAs in P. umbilicalis did not present significant differences compared to the initial value, probably because of the high initial content of MAAs. In both Porphyra species, four MAAs were identified: shinorine, porphyra-334, palythine and asterina-330. However, P. leucosticta modified its MAA pattern during the incubation time, reaching the same percentages found for P. umbilicalis, which did not show any change during the experimental period. P. leucosticta exhibited a decrease in BP/SP and BP/chl a ratios through the incubation time and an increase in MAAs/BP. The ratio MAAs/chl a did not show any variation with time or treatment, as was also true for all ratios in P. umbilicalis. In summary, ammonium supply diminished the decrease of Fv/Fm, increased the content of photosynthetic pigments (chlorophyll and biliprotein) and soluble protein, and stimulated of the accumulation of MAAs in the red algae P. leucosticta and P. umbilicalis.
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References
Aguilera J, de Gálvez Aranda MV, Conde R, Pérez Rodríguez E, Viñegla B, Abdala R, Segovia M, Herrera E, Figueroa FL (2004) Series temporales de medida de radiación solar ultravioleta y fotosintética en Málaga. Acta Dermosif 95:25–31
Algarra P, Niell FX (1990) Short-term pigment response of Corallina elongata Ellis et Soland to light intensity. Aquat Bot 36:127–138
Altamirano M, Flores-Moya A, Figueroa FL (2000) Long-term effect of natural sunlight under various ultraviolet conditions on growth and photosynthesis of intertidal Ulva rigida (Chlorophyceae) cultured in situ. Bot Mar 43:119–126
Beardall J, Roberts S, Millhouse J (1991) Effects of nitrogen limitation on uptake of inorganic carbon and specific activity of ribulose-1,5 biphosphate carboxilase/oxygenase in green microalgae. Can J Bot 69:1146–1150
Beer S, Eshel A (1985) Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Aust J Mar Freshw Res 36:785–792
Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystem I and II in microalgae. Plant Physiol 110:689–696
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem 72:248–254
Costanzo SD, O’Donohue MJ, Dennison WC (2000) Gracilaria edulis (Rhodophyta) as a biological indicator of pulsed nutrients in oligotrophic waters. J Phycol 36:680–685
Dring MJ, Wagner A, Franklin LA, Kuhlenkamp R, Lüning K (2001) Seasonal and diurnal variations in ultraviolet-B and ultraviolet-A irradiances at and below the sea surface at Helgoland (North Sea) over a 6-year period. Helgol Mar Res 55:3–11
Dunlap WC, Chalker BE, Oliver JK (1986) Bathymetric adaptations of reef-building corals at Davies Reef, Australia. III. UV-B absorbing compounds. J Exp Mar Biol Ecol 104:239–248
Favre-Bonvin J, Bernillon J, Salin N, Arpin N (1987) Biosynthesis of mycosporine: mycosporine-glutaminol in Trichothecium roseum. Phytochemistry 26:2509–2514
Figueroa FL, Aguilera J, Jiménez C, Vergara JJ, Robles MD, Niell FX (1995) Growth, pigment synthesis and nitrogen assimilation in the red alga Porphyra sp. (Bangiales, Rhodophyta) under blue and red light. Sci Mar 59:9–20
Figueroa FL, Salles S, Aguilera J, Jiménez C, Mercado J, Viñegla B, Flores-Moya A, Altamirano M (1997) Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta Thur. in Le Jol. Mar Ecol Prog Ser 151:81–90
Figueroa FL, Conde-Álvarez R, Gómez I (2003) Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions. Photosynth Res 75:259–275
Franklin LA, Kräbs G, Kuhlenkamp R (2001) Blue light and UV-A radiation control the synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae). J Phycol 37:257–270
Geider RJ, Greene RM, Kolber Z, MacIntyre HL, Falkowski PG (1993) Fluorescence assessment of the maximum quantum efficiency of photosynthesis in the western North Atlantic. Deep-Sea Res 40:1205–1224
Geider RJ, MacIntyre HL, Graziano LM, McKay RML (1998) Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur J Phycol 33:315–332
Gleason DF (1993) Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coral Porites astreoides. Limnol Oceanogr 38:1452–1463
Gotham IJ, Rhee G (1981) Comparative kinetic studies of phosphate-limited growth and phosphate uptake in phytoplankton in continuous culture. J Phycol 17:257–265
Gröniger A, Hallier C, Häder D (1999) Influence of UV radiation and visible light on Porphyra umbilicalis: photoinhibition and MAA concentration. J Appl Phycol 11:437–445
Grzymski J, Johnsen G, Sakshug E (1997) The significance of intracellular self-shading on the bio-optical properties of brown, red and green macroalgae. J Phycol 33:408–414
Häder DP, Gröniger A, Hallier C, Lebert M, Figueroa FL, Jiménez C (2000) Photoinhibition by visible and ultraviolet radiation in the red macroalga Porphyra umbilicalis. Plant Ecol 145:351–358
Hanelt D, Melchersmann B, Wiencke C, Nultsch W (1997) Effects of high light stress on photosynthesis of polar macroalgae in relation to depth distribution. Mar Ecol Prog Ser 149:255–266
Henley WJ, Levavasseur G, Franklin LA, Osmond CB, Ramus J (1991) Photoacclimation and photoinhibition in Ulva rotundata as influenced by nitrogen availability. Planta 184:235–243
Herzig R, Falkowski PG (1989) Nitrogen limitation in Isochrysis galbana (Haptophyceae). I. Photosynthetic energy conversion and growth efficiencies. J Phycol 25:462–471
Hoyer K, Karsten U, Wiencke C (2002) Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar Biol 141:619–627
Inskeep W, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485
Kain JM (1987) Seasonal growth and photoinhibition in Plocamium cartilagineum (Rhodophyta) of the Isle of Man. Phycologia 26:88–99
Karsten U, West JA (2000) Living in the intertidal zone—seasonal effects on heterosides and sun-screen compounds in the red alga Bangia atropurpurea (Bangiales). J Exp Mar Biol Ecol 254:221–234
Karsten U, Wiencke C (1999) Factors controlling the formation of UV-absorbing mycosporine-like amino acids in the marine red alga Palmaria palmata from Spitsbergen (Norway). J Plant Physiol 155:407–415
Karsten U, Franklin LA, Lüning K, Wiencke C (1998) Natural ultraviolet and photosynthetic active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta 205:257–262
Kolber Z, Zehr J, Falkowski P (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol 88:923–929
Korbee-Peinado N, Abdala-Díaz RT, Figueroa FL, Helbling EW (2004) Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from Patagonia, Argentina. J Phycol 40:248–259
La Roche J, Geider RJ, Graziano LM, Murray H, Lewis K (1993) Induction of specific proteins in eukaryotic algae grow under iron-, phosphorus-, or nitrogen-deficient conditions. J Phycol 29:767–777
Lebert M, Schuster M, Häder DP (2002) The European Light Dosimeter Network: four years of measurements. J Photochem Photobiol B 66:81–87
Litchman E, Neale PJ, Banaszak AT (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limnol Oceanogr 47:86–94
López-Figueroa F, Niell FX (1991) Photocontrol of chlorophyll and biliprotein synthesis in seaweeds: possible photoreceptors and ecological considerations. Sci Mar 55:519–527
Mercado J, Jiménez C, Niell FX, Figueroa FL (1996) Comparison methods for measuring light absorption by algae and their application to the estimation of the package effect. Sci Mar 60:39–45
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
Pérez-Rodríguez E (2000) Caracterización bióptica de aguas oceánicas y costeras. Fotosíntesis, fotoinhibición y fotoprotección bajo radiación ultravioleta y fotosintética en macrófitos marinos. PhD thesis, Málaga University, Málaga, Spain
Portwich A, García-Pichel F (1999) Ultraviolet and osmotic stresses induce and regulate the synthesis of mycosporines in the cyanobacterium Chlorogloeopsis PCC 6912. Arch Microbiol 172:187–192
Roy S (2000) Strategies for the minimisation of UV-induced damage. In: de Mora SJ, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, New York, pp 177–205
Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62
Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262
Shick JM, Romaine-Lioud SD, Ferrier-Pages C, Gattuso JP (1999) Ultraviolet-B radiation stimulates shikimate pathway–dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol Oceanogr 44:1667–1682
Sokal RR, Rohlf FJ (eds) (1995) Biometry, 3rd edn. Freeman, New York
Sosik HM, Mitchell BG (1991) Absorption, fluorescence, and quantum yield for growth in nitrogen-limited Dunaliella tertiolecta. Limnol Oceanogr 36:910–921
Takano S, Uemura D, Hirata Y (1978a) Isolation and structure of a new amino acid, palythine, from the zoanthid Palythoa tuberculosa. Tetrahedron Lett 26:2299–2300
Takano S, Uemura D, Hirata Y (1978b) Isolation and structure of two new amino acids, palythinol and palythene, from the zoanthid Palythoa tuberculosa. Tetrahedron Lett 26:4909–4912
Tandeau de Marsac N, Houmardd J (1993) Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rev 104:119–190
Tsujino I, Yabe K, Sekekawa I (1980) Isolation and structure of a new amino acid, shinorine, from the red alga Chondrus yendoi Yamada et Mikami. Bot Mar 23:65–68
Vergara JJ, Bird KT, Niell FX (1995) Nitrogen assimilation following NH4+ pulses in the red alga Gracilariopsis lemaneiformis: effect on C metabolism. Mar Ecol Prog Ser 122:253–263
Vincent WF, Neale PJ (2000) Mechanisms of UV damage to aquatic organisms. In: de Mora SJ, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, New York, pp 149–176
Wulff A, Wängberg SA, Sundbäck K, Underwood GJC, Nilsson C (2000) Effects of UV-B radiation on a marine microphytobenthic community growing on a sand-substratum under different nutrient conditions. Limnol Oceanogr 45:1144–1152
Acknowledgements
This study was supported by the Ministry of Science and Technology (Spain, CICYT research project AGL 2001-1888-C03-02) and by the Junta de Andalucía (research group RNM-295). N.K.P. appreciates the grant of the Ministry of Education and Science of Spain and P.H. appreciates the grant of the Academy of Finland (no. 100445).
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Korbee, N., Huovinen, P., Figueroa, F.L. et al. Availability of ammonium influences photosynthesis and the accumulation of mycosporine-like amino acids in two Porphyra species (Bangiales, Rhodophyta). Marine Biology 146, 645–654 (2005). https://doi.org/10.1007/s00227-004-1484-6
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DOI: https://doi.org/10.1007/s00227-004-1484-6