Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from Patagonia, Argentina

Journal of Phycology

Volumn 40, Issue 2, 2004, Pages 248-259

  Peinado, Nathalie Korbee ^a   Abdala Díaz, Roberto T ^a   Figueroa, Félix L ^a   Helbling, E Walter ^b  

^a Department of Clinical Pharmacology   (Spain)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Ammonium; Biliproteins; chl fluorescence; Mycosporine like amino acids; Photosynthetic activity; Porphyra; Quantum yield; UV radiation

Indexed keywords

AMINO ACID; AMMONIUM; ULTRAVIOLET RADIATION;

PATAGONIA; SOUTH AMERICA;

ALGAE; COLUMBINA; PORPHYRA; RHODOPHYTA; RICKETTSIA SP. PAR;

EID: 1842475053     PISSN: 00223646     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1529-8817.2004.03013.x     Document Type: Article

References (81)

1. Aguilera, J., Jiménez, C., Figueroa, F. L., Lebert, M. & Häder, D.-P. 1999a. Effect of ultraviolet radiation on thallus absorption and photosynthetic pigments in the red alga Pophyra umbilicalis. J. Photochem. Photobiol. 48:75-82.
2. Aguilera, J., Karsten, U., Lippert, H., Vögele, B., Philipp, E., Hanelt, D. & Wiencke, C. 1999b. Effects of solar radiation on growth, photosynthesis and respiration of marine macroalgae from the Arctic. Mar. Ecol. Prog. Ser. 191:109-19.
3. Algarra, P. & Niell, F. X. 1990. Short-term pigment response of Corallina elongata Ellis et Soland to light intensity. Aquat. Bot. 36:127-38.
4. Algarra, P. & Rüdiger, W. 1993. Acclimation processes in the light harvesting complex red alga Porphyridium purpureum (Bory) Drew et Ross according to irradiance and nutrient availability. Plant Cell Environ. 16:149-59.
5. Aráoz, R. & Häder, D.-P. 1997. Ultraviolet radiation induces both degradation and synthesis of phycobilisomes in Nostoc sp.: a spectroscopic and biochemical approach. FEMS Microbiol. Ecol. 23:301-13.
6. Babin, M., Morel, A., Claustre, H., Bricaud, A., Kolber, Z. & Falkowski, P. G. 1996. Nitrogen- and irradiance-dependent variations of the maximum quantum yield of carbon fixation in eutrophic, mesotrophic and oligotrophic marine systems. Deep-Sea Res. 43:1241-72.
7. Banaszak, A. T. & Neale, P. J. 2001. Ultraviolet radiation sensitivity of photosynthesis in phytoplankton from an estuarine environment. Limnol. Oceanogr. 46:592-603.
8. Bandaranayake, W. M. 1998. Mycosporines: are they nature's sunscreens? Nat. Prod. Rep. 15:159-72.
9. Barbieri, E. S., Villafan̄e, V. E. & Helbling, E. W. 2002. Experimental assessment of UV effects upon temperate marine phytoplankton when exposed to variable radiation regimes. Limnol. Oceanogr. 47:1648-55.
10. Beach, K. S. & Smith, C. M. 1996. Ecophysiology of tropical rhodophytes. 1. Microscale acclimation in pigmentation. J. Phycol. 32:701-10.
11. Beardall, J., Roberts, S. & Millhouse, J. 1991. Effects of nitrogen limitation on uptake of inorganic carbon and specific activity of ribulose-1, 5 biphosphate carboxylase/oxygenase in green microalgae. Can J. Bot. 69:1146-50.
12. Beer, S. & Eshel, A. 1985. Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Aust. J. Mar. Freshw. Res. 36:785-92.
13. Beer, S., Larsson, C., Poryan, O. & Axelsson, L. 2000. Photosynthetic rates of Ulva (Chlorophyta) measured by pulse amplitude modulated (PAM) fluorometry. Eur. J. Phycol. 35:69-74.
14. Bentley, R. 1990. The shikimate pathway-a metabolic tree with many branches. Crit. Rev. Biochem. Mol. Biol. 25:307-84.
15. Bischof, K., Kräbs, G., Hanelt, D. & Wiencke, C. 2000. Photosynthetic characteristics and mycosporine-like amino acids under UV radiation: a competitive advantage of Mastocarpus stellatus over Chondrus crispus at the Helgoland shoreline? Helgol. Mar. Res. 54:47-52.
16. Boussiba, S. & Richmond, A. E. 1980. C-phycocyanin as a storage protein in the blue-green alga Spirulina platensis. Arch. Microbiol. 125:143-7.
17. Buma, A. G. J., Van Hannen, E. J., Roza, L., Veldhuis, M. J. W. & Gieskes, W. W. C. 1995. Monitoring ultraviolet B-induced DNA damage in individual diatom cells by immunofluorescence thymine dimer detection. J. Phycol. 31:314-21.
18. Buma, A. G. J., Engelen, A. H. & Gieskes, W. W. C. 1997. Wavelength-dependent induction of thymine dimers and growth rate reduction in the marine diatom Cyclotella sp. exposed to ultraviolet radiation. Mar. Ecol. Prog. Ser. 153:91-7.
19. Carreto, J. I., Lutz, V. A., De Marco, S. G. & Carignan, M. O. 1990. Fluence and wavelength dependence of mycosporine-like amino acid synthesis in the dinoflagellate Alexandrium excavatum. In Graneli, E., Edler, L., Sundstrom, B. & Anderson, D. M. [Eds.] Toxic Marine Phytoplankton. Elsevier, Amsterdam, pp. 275-9.
20. Cockell, C. S. & Knowland, J. 1999. Ultraviolet radiation screening compounds. Biol. Rev. 74:311-45.
21. Dunlap, W. C., Chalker, B. E. &Oliver, J. K. 1986. Bathymetric adaptations of reef-building corals at Davies Reef, Australia. III. UV-B absorbing compounds. J. Exp. Mar. Biol. Ecol. 104:239-48.
22. Dunlap, W. C. & Yamamoto, Y. 1995. Small-molecule antioxidants in marine organisms-antioxidant activity of mycosporineglycine. Comp. Biochem. Physiol. B 112:105-14.
23. Dunlap, W. C. &Shick, J. M. 1998. UV radiation absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J. Phycol. 34:418-30.
24. Favre-Bonvin, J., Bernillon, J., Salin, N. & Arpin, N. 1987. Biosynthesis of mycosporine: mycosporine-glutaminol in Trichothecium roseum. Phytochemistry 26:2509-14.
25. Figueroa, F. L., Aguilera, J. & Niell, F. X. 1995. Red and blue light regulation of growth and photosynthetic metabolism in Porphyra umbilicalis (Bangiales, Rhodophyta). Eur. J. Phycol. 30:11-8.
26. Figueroa, F. L., Salles, S., Aguilera, J., Jiménez, C., Mercado, J., Vinegla, B., Flores-Moya, A. & Altamirano, M. 1997. Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar. Ecol. Prog. Ser. 151:81-90.
27. Figueroa, F. L., 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. 75:259-75.
28. Franklin, L. A. & Forster, R. M. 1997. The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur. J. Phycol. 32:207-32.
29. Franklin, L. A., Yakovleva, I., Karsten, U. & Lüning, K. 1999. Synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae) and the consequences for sensitivity to ultraviolet B radiation. J. Phycol. 35:682-93.
30. Franklin, L. A. & Badger, M. R. 2001. A comparison of photosynthetic electron transport rates in macroalgae measured by pulse amplitude modulated chlorophyll fluorometry and mass spectrometry. J. Phycol. 37:756-67.
31. Franklin, L. A., Kräbs, G. & Kuhlenkamp, R. 2001. Blue light and UVA radiation control the synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae). J. Phycol. 37:257-70.
32. García-Pichel, F., Wingard, C. E. & Castenholz, R. W. 1993. Evidence regarding the UV sunscreen role of a mycosporine-like compound in the cyanobacterium Gloecapsa sp. Appl. Environ. Microbiol. 59:170-6.
33. Gleason, D. F. 1993. Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coral Porites astreoides. Limnol. Oceanogr. 38:1452-63.
34. Goericke, R. & Montoya, J. P. 1998. Estimating the contribution of microalgal taxa to chlorophyll a in the field-variations of pigment ratios under nutrient- and light-limited growths. Mar. Ecol. Prog. Ser. 169:97-112.
35. Gröniger, A., Hallier, C. & Häder, D.-P. 1999. Influence of UV radiation and visible light on Porphyra umbilicalis: photoinhibition and MAA concentration. J. Appl. Phycol. 11:437-45.
36. Häder, D.-P. & Figueroa, F. L. 1997. Photoecophysiology of marine macroalgae. Photochem. Photobiol. 66:1-14.
37. Hader, D.-P., Lebert, M., Sinha, R. O., Barbieri, E. & Helbling, E. W. 2002. Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae. Photochem. Photobiol. Sci. 1:809-14.
38. Helbling, E. W. 1989. Estuarine Circulation and Nutrient Variability in the Chubut River Estuary (Argentina) During 1986-1987. M.Sci. thesis. Scripps Institution of Oceanography, University of California San Diego, 138 pp.
39. Helbling, E. W., Chalker, B. E., Dunlap, W. C., Holm-Hansen, O. & Villafañe, V. E. 1996. Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation. J. Exp. Mar. Biol. Ecol. 204:85-101.
40. Helbling, W. E., Villafañe, V. E., Buma, A. G., Andrade, M. & Zaratti, F. 2001. DNA damage and photosynthetic inhibition induced by solar UVR in tropical phytoplankton (Lake Titicaca, Bolivia). Eur. J. Phycol. 36:157-66.
41. Henley, W. J., Levavasseur, G., Franklin, L. A., Lindley, S. T., Ramus, J. & Osmond, C. B. 1991a. Diurnal responses of photosynthesis and fluorescence in Ulva rotundata acclimated to sun and shade in outdoor culture. Mar. Ecol. Prog. Ser. 75:19-28.
42. Henley, W. J., Levavasseur, G., Franklin, L. A., Osmond, C. B. & Ramus, J. 1991b. Photoacclimation and photoinhibition in Ulva rotundata as influenced by nitrogen availability. Planta 184:235-43.
43. Hernández, I., Corzo, A., Gordillo, F. J., Robles, M. D., Saez, E., Fernández, J. A. & Niell, F. X. 1993. Seasonal cycle of the gametophytic form of Porphyra umbilicalis: nitrogen and carbon. Mar. Ecol. Prog. Ser. 99:301-11.
44. Hoyer, K., Karsten, U., Sawall, T. & Wiencke, C. 2001. Photoprotective substances in antarctic macroalgae and their variation with respect to depth distribution, different tissues and developmental stages. Mar. Ecol. Prog. Ser. 211:117-29.
45. Jassby, A. D. & Platt, T. 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21:540-7.
46. Kain, J. M. 1987. Seasonal growth and photoinhibition in Plocamium cartilagineum (Rhodophyta) of the Isle of Man. Phycologia 26:88-99.
47. Karsten, U., Franklin, L. A., Lüning, K. & Wiencke, C. 1998a. Natural ultraviolet and photosynthetic active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta 205:257-62.
48. Karsten, U., Sawall, T., Hanelt, D., Bischof, K., Figueroa, F. L., Flores-Moya, A. & Wiencke, C. 1998b. An inventory of UV-absorbing mycosporine-like amino acids in macroalgae from polar to warm-temperate regions. Bot. Mar. 41:443-53.
49. Karsten, U., Bischof, K., Hanelt, D., Tüg, H. & Wiencke, C. 1999. The effect of ultraviolet radiation on photosynthesis and ultraviolet-absorbing substances in the endemic arctic macroalga Devaleraea ramentacea (Rhodophyta). Physiol. Plant. 105:58-66.
50. 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. 155:407-15.
51. Karsten, U. & West, J. A. 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. 254:221-34.
52. Lesser, M. P. 1996. Elevated temperature and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol. Oceanogr. 41:271-83.
53. Litchman, E., Neale, P. J. & Banaszak, A. T. 2002. Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limnol. Oceanogr. 47:86-94.
54. Logan, B. A., Demmig-Adams, B. & Adams, W. W., III 1999. Acclimation of photosynthesis to the environment. In Singhal, G. S., Renger, G., Sopory, S. K., Irrgang, K.-D. & Govindjee, A [Eds.] Concepts in Photobiology: Photosynthesis and Photomorphogenesis. Narosa Publishing House, New Delhi, India, pp. 477-511.
55. Longstaff, B. J., Kildea, T., Runcie, J. W., Cheshire, A., Dennison, W C., Hurd, C., Kana, T., Raven, J. A. & Larkum, W. D. 2002. An in situ study of photosynthetic oxygen exchange and electron transport rate in marine macroalga Ulva lactuca (Chlorophyta). Photosynth. Res. 74:281-93.
56. Ló;pez-Figueroa, F. & Niell, F. X. 1991. Photocontrol of chlorophyll and biliprotein synthesis in seaweeds: possible photoreceptors and ecological considerations. Sci. Mar. 55:519-27.
57. Lôpez-Figueroa, F. 1992. Diurnal variation in pigment content in Porphyra laciniata and Chondrus crispus and its relation to the diurnal changes of underwater light quality and quantity. Mar. Ecol. 13:285-305.
58. Marchant, H. J., Davidson, A. T. & Kelly, G. J. 1991. UV-protecting compounds in the marine alga Phaeocystis pouchetti from Antarctica. Mar. Biol. 109:391-5.
59. Neale, P. J., Banaszak, A. T. & Jarriel, C. R. 1998. Ultraviolet sunscreens in Gymnodinium sangumeum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis. J. Phycol. 34:928-38.
60. Orce, V. L. & Helbling, E. W. 1997. Latitudinal UVR-measurement in Argentina: extent of the ozone hole. Global Planet. Change 15:113-21.
61. Pérez-Lloréns, J. L., Vergara, J. J., Pino, R. R., Hernández, I., Peralta, G. & Niell, F. X. 1996. The effect of photoacclimation on the photosynthetic physiology of Ulva curvata and Ulva rotundata (Ulvales, Chlorophyta). Eur. J. Phycol. 331:349-59.
62. Post, A. & Larkum, A. W. D. 1993. UV-absorbing pigments, photosynthesis and UV-exposure in Antarctica: comparison of terrestrial and marine algae. Aquat. Bot. 45:231-43.
63. Roy, S. 2000. Strategies for the minimisation of UV-induced damage. In de Mora, S. J., Demers, S. & Vernet, M. [Eds.] The Effects of UV Radiation in the Marine Environment. Cambridge University Press, Cambridge, pp. 177-205.
64. Schenk, H. E. A., Hanf, J. & Neu-Müller, M. 1983. The phycobiliproteins in Cyanophoraparadoxa as accessory pigments and nitrogen storage proteins. Z. Naturforsch 38:972-7.
65. 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.
66. 2 dependent electron flow, membrane energization and mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth. Res. 25:279-93.
67. Shick, J. M., Romaine-Lioud, S. D., Ferrier-Pages, C. & Gattuso, J.-P. 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. 44:1667-82.
68. Shick, J. M. & Dunlap, W. C. 2002. Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 64:223-62.
69. Sinha, R. P., Lebert, M., Kumar, D. & Häder, D.-P. 1995. Spectroscopic and biochemical analysis of UV effects on phycobiliprotein of Anabaena sp. and Nostoc carmium. Bot. Acta 108:87-92.
70. Sinha, R. P., Sinha, J. P., Gröniger, A. & Häder, D.-P. 2002. Polychromatic action spectrum for the induction of a mycosporine-like amino acid in a rice-field cyanobacterium, Anabaena sp. J. Photochem. Photob. B Biol. 66:47-53.
71. Takano, S., Uemura, D. & Hirata, Y. 1978a. Isolation and structure of a new amino acid, palythine, from the zoanthid Palythoa tuberculosa. Tetrahedr. Lett. 26:2299-300.
72. Takano, S., Uemura, D. & Hirata, Y. 1978b. Isolation and structure of two new amino acids, palythinol and palythene, from the zoanthid Palythoa tuberculosa. Tetrahedr. Lett. 26:4909-12.
73. Talarico, L. & Maranzana, G. 2000. Light and adaptive responses in red macroalgae: an overview. J. Photochem. Photobiol. 56:1-11.
74. Tandeau de Marsac, N. & Houmardd, J. 1993. Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol. Rev. 104:119-90.
75. 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. 23:65-8.
76. Turpin, D. H. 1991. Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J. Phycol. 27:14-20.
77. Villafañe, V., Sundbäck, K., Figueroa, F. L. & Helbling, E. W. 2002. Photosynthesis in the aquatic environment as affected by UVR. In Helbling, E. W. & Zagarase, H. [Eds.] UV Effects in Aquatic Organisms and Ecosystems. Comprehensive series in Photochemical and Photobiological Sciences. The Royal Society of Chemistry, Cambridge, pp. 357-97.
78. Wellburn, A. R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144:307-13.
79. Wood, W. F. 1989. Photoadaptive responses of the tropical red alga Eucheuma striatum Schmitz (Gigartinales) to ultraviolet radiation. Aquat. Bot. 33:41-51.
80. Wulff, A., Wängberg, S.-A., Sundbäck, K., Underwood, G. J. C. & Nilsson, C. 2000. Effects of UVB radiation on a marine microphytobenthic community growing on a sand-substratum under different nutrient conditions. Limnol. Oceanogr. 45:1144-52.
81. Yakovleva, I. M. & Titlyanov, E. A. 2001. Effect of high visible and UV irradiance on subtidal Chondrus crispus: stress, photoinhibition and protective mechanisms. Aquat. Bot. 71:47-61.