Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae

Journal of Photochemistry and Photobiology B: Biology

Volumn 47, Issue 2-3, 1998, Pages 83-94

  Sinha, R P ^a   Klisch, M ^a   Groniger A ^a   Hader D P ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Cyanobacteria; Macroalgae; Mycosporine like amino acids (MAAs); Phytoplankton; Scytonemin; Ultraviolet radiation

Indexed keywords

AMINO ACID; ANTIOXIDANT; CAROTENOID; MYCOSPORINE; PIGMENT; SCYTONEMIN; UNCLASSIFIED DRUG;

ALGA; BIOLOGY; CYANOBACTERIUM; DETOXIFICATION; DNA DAMAGE; LIGHT; LIGHT ABSORPTION; NONHUMAN; OZONE LAYER; PHOTOCHEMISTRY; PHOTOTOXICITY; PHYTOPLANKTON; PRIORITY JOURNAL; REVIEW; SCREENING; ULTRAVIOLET B RADIATION; ULTRAVIOLET RADIATION;

EID: 0032458772     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1011-1344(98)00198-5     Document Type: Review

References (126)

1. [1] M. Blumthaler, W. Ambach, Indication of increasing solar ultraviolet-B radiation flux in alpine regions, Science 248 (1990) 206-208.
2. [2] P.J. Crutzen, Ultraviolet on the increase, Nature 356 (1992) 104-105.
3. [3] J.B. Kerr, C.T. McElroy, Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion, Science 262 (1993) 1032-1034.
4. [4] D. Lubin, E.H. Jensen, Effects of clouds and stratospheric ozone depletion on ultraviolet radiation trends, Nature 377 (1995) 710-713.
5. [5] V.W.J.H. Kirchhoff, Evidence for an ozone hole perturbation at 30° south, Atmos. Environ. 30 (1996) 1481-1488.
6. [6] R.C. Smith, B.B. Prezelin, K.S. Baker, R.R. Bidigare, N.P. Boucher, T. Coley, D. Karentz, S. McIntyre, H.A. Matlick, D. Menzies, M. Ondrusek, Z. Wan, K.J. Waters, Ozone depletion: ultraviolet radiation and phytoplankton biology in Antarctic waters, Science 255 (1992) 952-959.
7. [7] D.J. Hoffman, T. Deshler, Evidence from balloon measurements for chemical depletion of stratospheric ozone in the Arctic winter of 1989-90, Nature 349 (1991) 300-305.
8. [8] P. von der Gathen, M. Rex, N.R.P. Harris, D. Lucic, B.M. Knudsen, G.O. Braathen, H. De Backer, R. Fabian, H. Fast, M. Gil, E. Kyrö, I.S. Mikkelsen, M. Rummukainen, J. Stähelin, C. Varotsos, Observational evidence for chemical ozone depletion over the Arctic in water 1991-1992, Nature 375 (1995) 131-134.
9. [9] R.W. Castenholz, Multiple strategies for UV tolerance in cyanobacteria, The Spectrum 10 (1997) 10-16.
10. [10] R.C. Smith, K.S. Baker, Penetration of UV-B and biologically effective dose-rates in natural waters, Photochem. Photobiol. 29 (1979) 311-323.
11. [11] D.-P. Häder, R.C. Worrest, H.D. Kumar, R.C. Smith, Effects of increased solar ultraviolet radiation on aquatic ecosystems, Ambio 24 (1995) 174-180.
12. [12] J.T.O. Kirk, Optics of UV-B radiation in natural waters, Arch. Hydrobiol. 43 (1994) 1-16.
13. [13] O.B. Toon, R.P. Turco, Polar stratospheric clouds and ozone depletion. Sci. Ann. 264 (1991) 68-74.
14. [14] J.W. Elkins, T.M. Thompson, T.H. Swanson, J.H. Butler, B.D. Hall, S.O. Cummings, D.A. Fisher, A.G. Raffo, Decrease in the growth rates of atmospheric chlorofluorocarbons 11 and 12, Nature 364 (1993) 780-783.
15. [15] S. Madronich, R.L. McKenzie, M.M. Caldwell, L.O. Björn, Changes in ultraviolet radiation reaching the Earth's surface, Ambio 24 (1995) 143-152.
16. [16] D. Karentz, J.E. Cleaver, D.L. Mitchell, DNA damage in the Antarctic, Nature 350 (1991) 28.
17. [17] W.F. Vincent, S. Roy, Solar ultraviolet-B radiation and aquatic primary production: damage, protection, and recovery, Environ. Rev. 1 (1993) 1-12.
18. [18] M.L. Bothwell, D.M.J. Sherbot, C.M. Pollock, Ecosystem response to solar ultraviolet-B radiation: influence of trophic-level interactions, Science 265 (1994) 97-100.
19. [19] C.E. Williamson, What role does UVB radiation play in freshwater ecosystems?, Limnol. Oceanogr. 40 (1995) 386-392.
20. [20] R.P. Sinha, D.-P. Häder, Photobiology and ecophysiology of rice field cyanobacteria, Photochem. Photobiol. 64 (1996) 887-896.
21. [21] R.P. Sinha, M. Lebert, A. Kumar, H.D. Kumar, D.-P. Hader, Spectroscopic and biochemical analyses of UV effects on phycobiliproteins of Anabaena sp. and Nostoc carmium, Bot. Acta 180 (1995) 87-92.
22. [22] R.P. Sinha, M. Lebert, A. Kumar, H.D. Kumar, D.-P. Häder, Disintegration of phycobilisomes in a rice field cyanobacterium Nostoc sp. following UV irradiation, Biochem. Mol. Biol. Int. 37 (1995) 697-706.
23. [23] R.P. Sinha, N. Singh, A. Kumar, H.D. Kumar, M. Häder, D.-P. Häder, Effects of UV-irradiation on certain physiological and biochemical processes in cyanobacteria, J. Photochem. Photobiol. B: Biol. 32 (1996) 107-113.
24. [24] R.P. Sinha, N. Singh, A. Kumar, H.D. Kumar, D.-P. Hader, Impacts of ultraviolet-B irradiation on nitrogen-fixing cyanobacteria of rice paddy fields, J. Plant Physiol. 150 (1997) 188-193.
25. [25] E.W. Helbling, V. Villafañe, M. Ferrario, O. Holm-Hansen, Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species, Mar. Ecol. Prog. Ser. 80 (1992) 89-100.
26. [26] M.P. Lesser, J.J. Cullen, P.J. Neale, Carbon uptake in a marine diatom during acute exposure to ultraviolet B radiation: relative importance of damage and repair, J. Phycol. 30 (1994) 183-192.
27. [27] A.B. Britt, Repair of DNA damage induced by ultraviolet radiation, Plant Physiol. 108 (1995) 891-896.
28. [28] S.-T. Kim, A. Sancar, Photorepair of nonadjacent pyrimidine dimers by DNA photolyase, Photochem. Photobiol. 61 (1995) 171-174.
29. [29] R. Mittler, E. Tel-Or, Oxidative stress responses in the unicellular cyanobacterium Synechococcus PCC7942, Free Radical Res. Commun. 12 (1991) 845-850.
30. [30] E.M. Middleton, A.H. Teramura, The role of flavonol glycosides and carotenoids in protecting soybean from ultraviolet-B damage, Plant Physiol. 103 (1993) 741-752.
31. [31] M. Tevini, J. Braun, G. Fieser, The protective function of the epidermal layer of rye seedlings against ultraviolet-B radiation, Photochem. Photobiol. 53 (1991) 329-333.
32. [32] A. Kootstra, Protection from UV-B induced DNA damage by flavonoids, Plant Molec. Biol. 26 (1994) 771-774.
33. [33] F. Garcia-Pichel, R.W. Castenholz, Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment, J. Phycol. 27 (1991) 395-409.
34. [34] F. Garcia-Pichel, C.E. Wingard, R.W. Castenholz, Evidence regarding the UV sunscreen role of a mycosporine-like compound in the cyanobacterium Gloeocapsa sp., Appl. Environ. Microbiol. 59 (1993) 170-176.
35. [35] D. Karentz, F.S. McEuen, M.C. Land, W.C. Dunlap, Survey of mycosporine-like amino acid compounds in Antarctic marine organism: potential protection from ultraviolet exposure, Mar. Biol. 108 (1991) 157-166.
36. [36] M. Ehling-Schulz, W. Bilger, S. Scherer, UV-B-induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune, J. Bacteriol. 179 (1997) 1940-1945.
37. [37] F. Xiong, J. Komenda, J. Kopecky, L. Nedbal, Strategies of ultraviolet-B protection in microscopic algae, Physiol. Plant. 100 (1997) 378-388.
38. [38] H. Nakamura, J. Kobayashi, Y. Hirata, Separation of mycososporine-like amino acids in marine organisms using reverse-phase high performance liquid chromatography, J. Chromatogr. 250 (1982) 113-118.
39. [39] J. Favre-Bonvin, N. Arpin, C. Brevard, Structure de la mycosporine (P 310), Can. J. Chem. 54 (1976) 1105-1113.
40. [40] T. Arai, M. Nishijima, K. Adachi, H. Sano, Isolation and structure of a UV absorbing substance from the marine bacterium Micrococcus sp. AK-334, MBI Report, Marine Biotechnology Institute, 2-35-10 Kongo, Bunkyo-ku, Tokyo 113, Japan, 1992, pp. 88-94.
41. [41] F. Garcia-Pichel, R.W. Castenholz, Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimation of their screening capacity, Appl. Environ. Microbiol. 59 (1993) 163-169.
42. [42] U. Karsten, F. Garcia-Pichel, Carotenoids and mycosporine-like amino acid compounds in members of the genus Microcoleus (Cyanobacteria): a chemosystematic study, Syst. Appl. Microbiol. 19 (1996) 285-294.
43. [43] L. Sekikawa, C. Kubota, T. Hiraoki, I. Tsujino, Isolation and structure of a 357 nm UV-absorbing substance, usujirene, from the red alga Palmaria palmata (L) O. Kintzie, Jpn. J. Phycol. 34 (1986) 185-188.
44. [44] J.I. Carreto, M.O. Carignan, G. Daleo, S.G. De Marco, Occurrence of mycosporine-like amino acids in the red tide dinoflagellate Alexandrium excavatum: UV-protective compounds?, J. Plankton Res. 12 (1990) 909-921.
45. [45] D. Karentz, J.E. Cleaver, D.L. Mitchell, Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation, J. Phycol. 27 (1991) 326-341.
46. [46] A.K. Carroll, J.M. Shick, Dietary accumulation of UV-absorbing mycosporine-like amino acids (MAAs) by the green sea urchin (Stronglocentrotus droebachiensis), Mar. Biol. 24 (1996) 561-569.
47. [47] M. Vernet, K. Whitehead, Release of ultraviolet-absorbing compounds by the red-tide dinoflagellate Lingulodinium polyedra, Mar. Biol. 127 (1996) 35-44.
48. [48] N. Shashar, A.T. Banaszak, M.P. Lesser, D. Amrani, Coral endolithic algae: life in a protected environment, Pac. Sci. 51 (1997) 167-173.
49. [49] U. Karsten, L. A. Franklin, K. Lüning, C. Wiencke, Natural ultraviolet radiation and photosynthetically active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta), Planta 205 (1998) 257-262.
50. [50] J.M. Shick, W.C. Dunlap, B.E. Chalker, A.T. Banaszak, T.K. Rosenzweig, Survey of ultraviolet radiation absorbing mycosporine-like amino acids in organs of coral reef holothuroids, Mar. Ecol. Prog. Ser. 90 (1992) 139-148.
51. [51] F. Chioccara, A. Della Gala, M. De Rosa, E. Novellino, G. Prota, Mycosporine amino acids and related compounds from the eggs of fishes. Bull. Soc. Chim. Belg. 89 (1980) 1101-1106.
52. [52] W.C. Dunlap, D.M. Williams, B.E. Chalker, A.T. Banaszak, Biochemical photoadaptations in vision: UV-absorbing pigments in fish eye tissues, Comp. Biochem. Physiol. 93 (1989) 601-607.
53. [53] A. Thorpe, R.H. Douglas, R.J.W. Truscott, Spectral transmission and short-wave absorbing pigments in the fish lens - I. Phylogenetic distribution and identity. Vison Res. 33 (1993) 289-300.
54. [54] W.C. Dunlap, Y. Yamamoto, Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine, Comp. Biochem. Physiol. 112 (1995) 105-114.
55. [55] J.J. Wu Won, J.A. Rideout, B.E. Chalker, Isolation and structure of a novel mycosporine-like amino acid from the reef-building corals Pocillopora damicornis and Stylophora pistillata, Tetrahedron Lett. 36 (1995) 5255-5256.
56. [56] W.M. Bandaranayake, J.E. Bemis, D.J. Bourne, Ultraviolet absorbing pigments from the marine sponge Dysidea herbacea: isolation and structure of a new mycosporine, Comp. Biochem. Physiol. 115 (1996) 281-286.
57. [57] J.B. McClintock, D. Karentz, Mycosporine-like amino acids in 38 species of subtidal marine organisms from McMurdo Sound, Antarctica, Antarc. Sci. 9 (1997) 392-398.
58. [58] J.H. Drollett, T. Teai, M. Faucon, P.M.V. Martin, Field study of compensatory changes in UV-absorbing compounds in the mucus of the solitary coral Fungia rapanda (Scleractinia:Fungiidae) in relation to solar UV radiation, sea-water temperature, and other coincident physico-chemical parameters. Mar. Freshwater Res. 48 (1997) 329-333.
59. [59] M. Ishikura, C. Kato, T. Maruyama, UV-absorbing substances in zooxanthellate and azooxanthellate clams, Mar. Biol. 128 (1997) 649-655.
60. [60] M.L. Dionisio-Sese, M. Ishikura, T. Maruyama, S. Miyachi, UV-absorbing substances in the tunic of a colonial ascidian protect its symbiont, Prochloron sp., from damage by UV-B radiation, Mar. Biol. 128 (1997) 455-461.
61. [61] T.H. Carefoot, M. Harris, B.E. Taylor, D. Donovan, D. Karentz, Mycosporine-like amino acids: possible UV protection in eggs of the sea hare Aplysia dactylomela, Mar. Biol. 130 (1998) 389-396.
62. [62] W.C. Dunlap, J.M. Shick, Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organism: a biochemical and environmental perspective, J. Phycol. 34 (1998) 418-430.
63. [63] C. Nägeli, Gattungen einzelliger Algen, physiologisch und systematisch bearbeitet, Neue Denkschrift, Allg. Schweiz. Natur Ges. 10 (1849) 1-138.
64. [64] L. Geitler, Cyanophyceae (Blaualgen), in: L. Rabenhorst (Ed.), Kryptogamen-Flora von Deutschland, Österreich und der Schweiz, vol. 14, Akademische Verlagsgesellschaft, Leipzig, 1932, pp. 1-1196.
65. [65] T.V. Desikachary, Cyanophyta, Indian Council of Agricultural Research, New Dehli, India, 1959, pp. 1-686.
66. [66] F. Garcia-Pichel, N.D. Sherry, R.W. Castenholz, Evidence for an ultraviolet sunscreen role of the extracellular pigment scytonemin in the terrestrial cyanobacterium Chlorogloeopsis sp., Photochem. Photobiol. 56 (1992) 17-23.
67. [67] P.J. Proteau, W.H. Gerwick, F. Garcia-Pichel, R.W. Castenholz, The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria, Experientia 49 (1993) 825-829.
68. [68] G.L. Helms, R.E. Moore, W.P. Niemczura, G.M.L. Patterson, K.B. Tomer, M.L. Gross, Scytonemin A, a novel calcium antagonist from a blue-green alga, J. Org. Chem. 53 (1988) 1298-1307.
69. 2-fixing cyanobacteria, Annu. Rev. Microbiol. 34 (1980) 497-536.
70. [70] M.R. Walter, J. Bauld, D.J. Des Marais, J.W. Schopf, A general comparison of microbial mats and microbial stromatolites: bridging the gap between the modern and the fossil, in: J. Schopf, C. Klein (Eds.), The Proterozoic Biosphere, Cambridge University Press, 1992, pp. 335-338.
71. [71] J.W. Schopf, Microfossils of the early archean chert: new evidence of the antiquity of life, Science 260 (1993) 640-646.
72. [72] N.R. Pace, A molecular view of microbial diversity and the biosphere, Science 276 (1997) 734-740.
73. [73] P. Fay, Oxygen relations of nitrogen fixation in cyanobacteria, Microbiol. Rev. 56 (1992) 340-373.
74. [74] N. Tandeau de Marsac, J. Houmard, Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms, FEMS Microbiol. Rev. 104 (1993) 119-190.
75. [75] A. Vaishampayan, R.P. Sinha, D.-P. Häder, Use of genetically improved nitrogen-fixing cyanobacteria in rice paddy fields: prospects as a source material for engineering herbicide sensitivity and resistance in plants, Bot. Acta 111 (1998) 176-190.
76. [76] T.A. Kuhlbusch, J.M. Lobert, P.J. Crutzen, P. Warneck, Molecular nitrogen emission. Trace nitrification during biomass burning, Nature 351 (1991) 135-137.
77. [77] B.C. Parker, L.E. Heiskell, W.J. Thompson, Nonbiogenic fixed nitrogen in Antarctica and some ecological implications, Nature 271 (1978) 651-652.
78. [78] V. Donkor, D.-P. Häder, Effects of solar and ultraviolet radiation on motility, photomovement and pigmentation in filamentous, gliding cyanobacteria, FEMS Microbiol. Ecol. 86 (1991) 159-168.
79. [79] A. Queseda, W.F. Vincent, Strategies of adaptation by Antarctic cyanobacteria to ultraviolet radiation, Eur. J. Phycol. 32 (1997) 335-342.
80. [80] D.-P. Häder, Photomovement, in: P. Fay, C. Van Baalen (Eds.), The Cyanobacteria, Elsevier, Amsterdam, 1987, pp. 325-345.
81. [81] D.-P. Häder, Phototensory behavior in procaryotes, Microbiol. Rev. 51 (1987) 1-21.
82. [82] B.M. Bedout, F. Garcia-Pichel, UV-B induced vertical migrations of cyanobacteria in a microbial mat, Appl. Environ. Microbiol. 61 (1995) 4215-4222.
83. [83] C.S. Reynolds, R.L. Oliver, A.E. Walsby, Cyanobacterial dominance: the role of buoyancy regulation in dynamic lake environments, NZ J. Mar. Freshwater Res. 21 (1987) 379-390.
84. [84] G.W. Burton, K.U. Ingold, β-Carotene: an unusual type of lipid antioxidant, Science 224 (1984) 569-573.
85. [85] W.F. Vincent, A. Quesada, Ultraviolet radiation effects on cyanobacteria: implication for Antarctic microbial ecosystems, in: C.S. Weiler, P.A. Penhale (Eds.), Ultraviolet Radiation in Antarctica: Measurements and Biological Effects, vol. 62, Antarctic Research Series, American Geophysical Union, Washington, DC, 1994, pp. 111-124.
86. [86] D.A. Christopher, J.E. Mullet, Separate photosensory pathways co-regulate blue light/ultraviolet-A-activated psbD-psbC transcription and light induced D2 and CP43 degradation in barley (Hordeum vulgare) chloroplasts, Plant Physiol. 104 (1994) 1119-1129.
87. [87] K. Shibata, Pigments and a UV-absorbing substance in corals and a blue-green alga living on the Great Barrier Reef, Plant Cell Physiol. 10 (1969) 325-335.
88. [88] J. Favre-Bonvin, J. Bernillon, N. Salin, N. Arpin, Biosynthesis of mycosporine: mycosporine glutaminol in Trichothecium roseum, Phytochem. 26 (1987) 2509-2514.
89. [89] B. Büdel, U. Karsten, F. Garcia-Pichel, Ultraviolet-absorbing scytonemin and mycosporine-like amino acids derivatives in exposed, rock-inhabiting cyanobacterial lichens, Oecologia 112 (1997) 165-172.
90. [90] A. Oren, Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria, Geomicrobiol. J. 14 (1997) 231-240.
91. [91] F. Garcia-Pichel, A model for internal self-shading in planktonic organims and its implications for the usefulness of ultraviolet sunscreens, Limnol. Oceanogr. 39 (1994) 1704-1717.
92. [92] G. A. Böhm, W. Pfleiderer, P. Böger, S. Scherer, Structure of a novel oligosaccharide-mycosporine-amino acid ultraviolet-A/B sunscreen pigment from the terrestrial cyanobacterium Nostoc commune, J. Biol. Chem. 270 (1995) 8536-8539.
93. [93] R.P. Sinha, M. Klisch, D.-P. Häder, Induction of a mycosporine-like amino acid (MAA) in the rice field cyanobacterium Anabaena sp. after UV irradiation, submitted for publication.
94. [94] A. Pentecost, Field relationships between scytonemin density, growth and irradiance in cyanobacteria occurring in low illumination regimes. Micro. Ecol. 26 (1993) 101-110.
95. [95] S. Brenowitz, R.W. Castenholz, Long-term effects of UV and visible irradiance on natural populations of a scytonemin-containing cyanobacterium (Calothrix sp.), FEMS Microbiol. Ecol. 24 (1997) 343-352.
96. [96] L. Birke, Marine blue-green algal mats, in: H.T. Odum, B.J. Copeland, E.A. McMahan (Eds.), Coastal Ecosystems in the United States, vol. 1, The Conservation Foundation, Washington, DC, 1983, pp. 331-345.
97. [97] S. Golubic, Distribution, taxonomy, and boring patterns of marine endolithic algae, Am. Zool. 9 (1969) 747-751.
98. [98] L.O. Sorensen, J.T. Conover, Algal mat communities of Lyngbya confervoides (C. Agardh) Gomont, Publ. Inst. Mar. Sci. Univ. Texas 8 (1962) 61-74.
99. [99] G. Turian, Primary colonisation of concrete walls by a UV-protectively pigmented Chrysocapsa (cyanobacteria), Saussurea 16 (1985) 43-48.
100. [100] S.N. Tripathi, E.R.S. Talpasayi, Sulphydrils and survival of subaerial blue-green algae, Curr. Sci. 49 (1980) 31-32.
101. [101] C. Sinclair, B.A. Whitton, Influence of nutrient deficiency on hair formation in the Rivulariaceae, Br. Phycol. J. 12 (1977) 297-313.
102. [102] R.P. Sinha, M. Klisch, A. Vaishampayan, D.-P. Häder, Biochemical and spectroscopic characterization of the cyanobacterium Lyngbya sp.: presence of an ultraviolet-absorbing pigment, scytonemin, submitted for publication.
103. [103] S. Scherer, T.W. Chen, P. Böger, A new UV-A/B protecting pigment in the terrestrial cyanobacterium Nostoc commune, Plant Physiol. 88 (1988) 1055-1057.
104. [104] N.M. de Chazal, G.D. Smith, Characterization of a brown Nostoc sp. from Java that is resistant to high light intensity and UV, Microbiology 140 (1994) 3183-3189.
105. 3 and certain cyanobacterial pigments, Photochem. Photobiol. 64 (1996) 321-325.
106. [106] A.J. Watson, P.S. Liss, Marine biological controls on climate via the carbon and sulphur geochemical cycles, Philos. Trans. R. Soc. Lond. B 353 (1998) 41-51.
107. [107] D.-P. Häder, Ecological consequences of photomovement in microorganisms, J. Photochem. Photobiol. B: Biol. 1 (1988) 385-414.
108. [108] E.W. Helbling, B.E. Chalker, W.C. Dunlap, O. Holm-Hansen, V.E. Villafañe, Photoacclimation of Antarctic diatoms to solar ultraviolet radiation, J. Exp. Mar. Biol. Ecol. 204 (1996) 85-101.
109. [109] W.C. Dunlap, G.A. Rae, E.W. Helbling, V.E. Villafañe, O. Holm-Hansen, UV-absorbing compounds in natural assemblages of Antarctic phytoplankton, Antarctic J. US 30 (1995) 323-326.
110. [110] E.W. Helbling, V.E. Villafañe, O. Holm-Hansen, Effects of ultraviolet radiation on Antarctic marine phytoplankton photosynthesis with particular attention to the influence of mixing, in: C.S. Weiler, P.A. Penhale (Eds.), Ultraviolet Radiation in Antarctica: Measurements and Biological Effects, Antarctic Res. Series 62 (1994) 207-227.
111. [111] M. Veraet, A. Neori, F.T. Haxo, Spectral properties and photosynthetic action in red-tide populations of Prorocentrum micans and Gonyaulax polyhedra, Mar. Biol. 103 (1989) 365-371.
112. [112] C.A. Llewellyn, R.F.C. Mantoura, A UV absorbing compound in HPLC pigment chromatograms obtained from Icelandic Basin phytoplankton, Mar. Ecol. Prog. Ser. 158 (1997) 283-287.
113. [113] J.I. Carreto, V.A. Lutz, S.G. De Marco, M.O. Carignan, Fluence and wavelength dependence of mycosporine-like amino acid synthesis in the dinoflagellate Alexandrium excavatum, in: E. Graneli, L. Edler, B. Sundström, D.M. Anderson (Eds.), Toxic Marine Phytoplankton, Elsevier, New York, 1990, pp. 275-279.
114. [114] M.P. Lesser, Acclimation of phytoplankton to UV-B radiation: oxidative stress and photoinhibition of photosynthesis are not prevented by UV-absorbing compounds in the dinoflagellate Prorocentrum micans, Mar. Ecol. Prog. Ser. 132 (1996) 287-297.
115. [115] H.J. Marchant, A.T. Davidson, G.J. Kelly, UV-B protecting compounds in the marine alga Phaeocystis pouchetti from Antarctica, Mar. Biol. 109 (1991) 391-395.
116. [116] V.E. Villafañe, E.W. Helbling, O. Holm-Hansen, B.E. Chalker, Acclimatization of Antarctic natural phytoplankton assemblages when exposed to solar ultraviolet radiation, J. Plankton Res. 17 (1995) 2295-2306.
117. [117] M. Vernet, E.A. Brody, O. Holm-Hansen, B.C. Mitchell, The response of Antarctic phytoplankton to ultraviolet radiation: absorption, photosynthesis, and taxonomic composition, in: C.S. Weiler, P.A. Penhale (Eds.), Ultraviolet Radiation in Antarctica: Measurements and Biological Effects, Antarctic Res. Series 62 (1994) 143-158.
118. [118] P.M. Sivalingam, T. Ikawa, Y. Yokohama, K. Nisizawa, Distribution of a 334 nm UV-absorbing substance in algae, with special regard of its possible physiological roles, Botanica Mar. 17 (1974) 23-29.
119. [119] R.P. Sinha, M. Klisch, A. Gröniger, D.-P. Häder, Mycosporine-like amino acids in the marine red alga Gracilaria cornea - effects of UV and heat, submitted for publication.
120. [120] A.T. Banaszak, R.K. Trench, Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses. II. The synthesis of mycosporine-like amino acids in response to exposure to UV in Anthopleura elegantissima and Cassiopeia xamachana, J. Exp. Mar. Bio. Ecol. 194 (1995) 233-250.
121. [121] J. Favre-Bonvin, J. Bernillon, N. Salin, N. Arpin, Biosynthesis of mycosporine glutaminol in Trichothecium roseum, Phytochem. 26 (1987) 2509-2514.
122. [122] D. Karentz, H.J. Spero, Response of a natural Phaeocystis population to ambient fluctuations of UV-B radiation caused by Antarctic ozone depletion, J. Plankton Res. 17 (1995) 1771-1789.
123. [123] P.M. Sivalingam, T. Ikawa, K. Nisizawa, Physiological roles of a substance 334 in algae, Bot. Mar. 19 (1976) 9-21.
124. [124] T. Yoshida, P.M. Sivalingam, Isolation and characterization of the 337 mμ UV-absorbing substance in red alga Porphyra yezoensis UEDA, Plant Cell Physiol. 11 (1970) 427-434.
125. [125] J.I. Carreto, S.G. De Marco, V.A. Lutz, UV-absorbing pigments in the dinoflagellates Alexandrium excavatum and Prorocentrum micans. Effects of light intensity, in: T. Okaichi, D.M. Anderson, T, Nemoto (Eds.), Red Tides, Biology, Environmental Science and Toxicology, Elsevier, New York, 1989, pp. 333-336.
126. [126] S.-À. Wängberg, A. Persson, B. Karlson, Effects of UV-B radiation on synthesis of mycosporine-like amino acids and growth in Heterocapsa triquetra (Dinophyceae), J. Photochem. Photobiol. B: Biol. 37 (1997) 141-146.