Abstract
Reports of bathymetric decrease in the total mycosporine-like amino acid (MAA) concentration of benthic invertebrates suggest that light gradients may be important determinants of MAA content. With the pronounced diel light changes, distinct temporal variations in MAA concentrations might also be expected. We examined the changes in the abundance of MAA in three shallow-water scleractinian corals, Pavona divaricata, Galaxea fascicularis and Montipora digitata from Okinawa, Japan, in relation to daily cycles in solar radiation and tested whether the species have different capabilities for protection against UVR depending on their MAA composition. The results show that symbiotic algae freshly isolated from the investigated coral species do not contain MAAs and that distribution of these compounds resided only within the animal tissue. Total MAA content in the tissue of P. divaricata, G. fascicularis and M. digitata rose rapidly at midday and significantly dropped at night. The observed variations were by a factor of two and, thus, very dramatic. For all the investigated coral species, total MAA concentrations were significantly correlated with the diurnal cycle in solar radiation, during both winter and summer seasons. Seawater temperature was significantly correlated with MAA levels only in the June experiment, but represented no more than 20% of the MAA variation in all three coral species, whereas solar radiation explained 60–70% of the MAA fluctuations. This suggests that MAAs are an integral component of the hard coral’s biochemical defense system against high solar irradiance stress. The diurnal increase in total MAA concentrations was due to an increase in the concentration of imino-MAA species of up to 2–2.5-fold of their pre-dawn values. In contrast, the oxocarbonyl-MAA mycosporine-glycine (Myc-Gly) showed the lowest (Tukey–Kramer HSD test: P<0.05) values at midday, compared to afternoon and night hours. Analysis of diel changes in chlorophyll fluorescence and chlorophyll a content of the investigated species revealed that P. divaricata and G. fascicularis were less sensitive to the high levels of ambient irradiance compared to M. digitata. In P. divaricata and G. fascicularis, Myc-Gly, an MAA with an antioxidant function, is the most abundant MAA, contributing about 70% to the total MAA pool, whereas the major MAA factions in M. digitata were represented by oxidatively robust imino-MAAs. We speculate that MAAs furnish scleractinian corals with protection from biologically damaging ultraviolet radiation through both the direct sunscreening activity of imino-MAAs and the antioxidant properties of oxocarbonyl-MAAs and suggest that the predominance, in the host tissue, of MAA species with an antioxidant ability may render corals more tolerant to high photosynthetically active and ultraviolet radiation.
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References
Adams NL, Shick JM (1996) Mycosporine-like amino acids provide protection against ultraviolet radiation in eggs of the green sea urchin Strongylocentrotus droebachiensis. Photochem Photobiol 64:149–158
Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ (ed) Photoinhibition. Elsevier, Amsterdam, pp 228–287
Baker KS, Smith RC, Green AES (1980) Middle ultraviolet radiation reaching the ocean surface. Photochem Photobiol 32:367–374
Banaszak AT, Lesser MP, Kuffner IB, Ondrusek M (1998) Relationship between ultraviolet (UV) radiation and mycosporine-like amino acids (MAAs) in marine organisms. Bull Mar Sci 63:617–628
Bandaranayake WM (1998) Mycosporines: are they nature’s sunscreens? Nat Prod Rep 15:159–172
Bandaranayake WM, Bourne DJ, Sim RG (1997) Chemical composition during maturing and spawning of the sponge Dysidea herbacea (Porifera: Demospongiae). Comp Biochem Physiol B 118:851–859
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brown BE (1997) Adaptations of reef corals to physical environmental stress. Adv Mar Biol 31:221–299
Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99–105
Brown BE, Downs CA, Dunne RP, Gibb SW (2002) Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling. J Exp Mar Biol Ecol 277:129–144
Carreto JI, De Marco SG, Lutz VA (1989) UV-absorbing pigments in the dinoflagellates Alexandrium excavatum and Prorocentrum micans. Effects of light intensity. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides, biology, environmental science and toxicology. Elsevier, New York, pp 333–336
Dionisio-Sese ML, Ishikura M, Maruyama T, Miyachi S (1997) UV-absorbing substances in the tunic of a colonial ascidia protect its symbiont, Prochloron sp., from damage by UV-B radiation. Mar Biol 128:455–461
Drollet JH, Teai T, Faucon M, Martin PMV (1997) Field study of compensatory changes in UV-absorbing compounds in the mucus of the solitary coral Fungia repanda (Sclectinia: Fungiidae) in relation to solar UV radiation, seawater temperature, and other coincident physico-chemical parameters. Mar Freshw Res 48:329–333
Dunlap WC, Chalker BE (1986) Identification and quantification of near-UV absorbing compounds (S-320) in a hermatypic scleractinian. Coral Reefs 5:155–159
Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34:418–430
Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol B 112:105–114
Dunlap WC, Shick JM, Yamamoto Y (1999) Sunscreens, oxidative stress and antioxidant functions in marine organisms of the Great Barrier Reef. Redox Rep 4:301–306
Dunlap WC, Shick JM, Yamamoto Y (2000) Ultraviolet (UV) protection in marine organisms. I. Sunscreens, oxidative stress and antioxidants. In: Yoshikawa S, Toyokuni S, Yamamoto Y, Naito Y (eds) Free radicals in chemistry, biology and medicine. OICA Int., London, pp 200–214
Dykens JA, Benoit C, Buettner GR, Winston GW (1992) Oxygen radical production in the sea anemone, Anthopleura elegantissima, and its endosymbiotic algae. J Exp Biol 168:219–241
Gleason DF (2001) Ultraviolet radiation and coral communities. In: Cockell CS, Blaustein AR (eds) Ecosystems, evolution and ultraviolet radiation. Springer, New York Heidelberg Berlin, pp 118–149
Gorbunov MY, Kolber ZS, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46:75–85
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86
Ishikura M, Kato C, Maruyama T (1997) UV-absorbing substances in zooxanthellate and azooxanthellate clams. Mar Biol 128:649–655
Johannes RE, Wiebe WJ (1970) A method for determination of coral tissue biomass and composition. Limnol Oceanogr 15:822–824
Karentz D, Dunlap WC, Bosch I (1997) Temporal and spatial occurrence of UV-absorbing mycosporine-like amino acids in tissue of the Antarctic sea urchin Sterechinus neumayeri during springtime ozone-depletion. Mar Biol 129:343–353
Karsten U, Sawall T, Wienske C (1998) A survey of the distribution of UV-absorbing substances in tropical macroalgae. Phycol Res 46:271–279
Kinzie III RA (1993) Effects of ambient levels of solar ultraviolet radiation on zooxanthellae and photosynthesis of the reef coral Montipora verrucosa. Mar Biol 116:319–327
Kuhl M, Cohen Y, Dalsgaard T, Jorgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2. Mar Ecol Prog Ser 117:159–172
LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. Phycologia 37:886–880
Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283
Lesser MP (2000) Depth-dependent photoacclimatization to solar ultraviolet radiation in the Caribbean coral Montastrea faveolata. Mar Ecol Prog Ser 192:137–151
Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232
Michalek-Wagner K (2001) Seasonal and sex-specific variations in level of photo-protecting mycosporine-like amino acids (MAAs) in soft corals. Mar Biol 139:651–660
Neale PJ, Banaszak AT, Jarriel CR (1998) Ultraviolet sunscreens in Gymnodimium sanguineum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis. J Phycol 34:928–938
Oquist G, Anderson JM, McCaffery S, Chow WS (1992) Mechanistic differences in photoinhibition of sun and shade plants. Planta 188:538–544
Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269
Salih A, Larcum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853
Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In: Schluze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin Heidelberg New York, pp 49–70
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, Dykens JA (1985) Oxygen detoxification in algal–invertebrate symbioses from the Great Barrier Reef. Oecologia 66:33–41
Shick JM, Dunlap WC, Chalker BE, Banaszak AT, Rosenzweig TK (1992) Survey of ultraviolet radiation-absorbing mycosporine-like amino acids in organs of coral reef holothuroids. Mar Ecol Prog Ser 90:139–148
Shick JM, Romaine-Lioud S, Ferrier-Pages C, Gattuso J-P (1999) Ultraviolet-B radiation 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
Shick JM, Dunlap WC, Buettne GR (2000) Ultraviolet (UV) protection in marine organisms. II. Biosynthesis, accumulation, and sunscreening function of mycosporine-like amino acids. In: Yoshikawa S, Toyokuni S, Yamamoto Y, Naito Y (eds) Free radicals in chemistry, biology and medicine. OICA Int., London, pp 215–228
Snedecor DU (1961) Statistical methods in application to the investigations in agriculture and biology (in Russian). High School Publisher, Moscow, pp 35–43
Stimson J, Kinzie RA (1991) The temporal pattern and rate of release zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74
Stimson J, Sakai K, Sembali H (2002) Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching induced mortality. Coral Reefs 21:409–421
Stochaj WR, Dunlap WC, Shick JM (1994) Two new UV-absorbing mycosporine-like amino acids from the sea anemone Anthopleura elegantissima and the effects of zooxanthellae and spectral irradiance on chemical composition and content. Mar Biol 118:149–156
Suh Hwa-Jin, Lee Hyun-Woo, Jung Jin (2003) Mycosporine glycine protects biological systems against photodynamic damage by quenching singlet oxygen with a high efficiency. Photochem Photobiol 78:109–113
Acknowledgements
This research was supported by a Grant-in-Aid for Scientific Research from the Japan Society for Promotion of Science to I.Y. We thank Dr. A. Takemura of the Sesoko Research Station for his invaluable assistance and advice in HPLC analysis. Comments from two anonymous reviewers significantly improved the manuscript.
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Communicated by T. Ikeda, Hakodate
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Yakovleva, I., Hidaka, M. Diel fluctuations of mycosporine-like amino acids in shallow-water scleractinian corals. Marine Biology 145, 863–873 (2004). https://doi.org/10.1007/s00227-004-1384-9
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DOI: https://doi.org/10.1007/s00227-004-1384-9