Abstract
Many tropical cnidarians living in shallow water contain a class of ultraviolet-A (UV-A, 320 to 400 nm) and ultraviolet-B (UV-B, 280 to 320 nm) absorbing compounds known as mycosporine-like amino acids (MAAs). These compounds may provide protection from the deleterious effects of solar UV radiation. Using a novel application of reverse-phase high performance liquid chromatography, we find that the temperate sea anemoneAnthopleura elegantissima (collected in 1988 from Bodega Bay, California, and in 1991 from Santa Barbara, California) contains four major MAAs: shinorine, porphyra-334, and two new compounds, mycosporine-taurine and mycosporine-2 glycine. Analysis of zooxanthellate (containing zooxanthellae) and naturally apozooxanthellate (lacking zooxanthellae) specimens acclimated in the presence and absence of UV for 28 d in the spring of 1988 suggests that this anemone, unlike some other anthozoans, does not regulate the concentration of its MAAs in response to UV radiation. The presence of similar concentration of MAAs in apozooxanthellate and zooxanthellate specimens indicates that symbiosis with algae is not required for these compounds to be present in the anemone. The total concentration of MAAs in the zooxanthellae is only about 12% of that in their host's tissues.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Analyt. Biochem. 72:248–254
Carreto, J. I., Carignan, M. O., Daleo, G., De Marco, S. G. (1990). Occurrence of mycosporine-like amino acids in the red-tide dinoflagellateAlexandrium excavatum: UV-photoprotective compounds? J. Plankton Res. 12:909–921
Cavanaugh, G. M. (1975). Formulae and methods VI of the Marine Biological Laboratory Chemical Room. Marine Biological Laboratory, Woods Hole, Massachussetts
Clark, E. D., Kimelsdorf, D. J. (1971). Behavioral reactions of the sea anemone,Anthopleura xanthogrammica, to ultraviolet and visible radiations. Radiat. Res. 45:166–175
Dunlap, W. C., Banaszak, A. T., Rosenzweig, T. T., Shick, J. M. (1991). Ultraviolet light-absorbing compounds in coral reef holothurians: organ distribution and possible sources. In: Yanagisawa, T., Yasumasu, I., Oguro, C., Suzuki, N., Motokawa, T. (eds.) Biology of Echinodermata. Proceedings of the Seventh International Echinoderm Conference. A.A. Balkema, Rotterdam, p. 560
Dunlap, W. C., Chalker, B. E. (1986). Identification and quantitation of near-UV absorbing compounds (S-320) in a hermatypic scleractinian. Coral Reefs 5:155–159
Dunlap, W. C., Chalker, B. E., Oliver, J. K. (1986). Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. III. UV-B absorbing compounds. J. exp. mar. Biol. Ecol. 104:239–248
Dunlap, W. C., Williams, D. McB., Chalker, B. E., Banaszak, A. T. (1989). Biochemical photoadaptations in vision: UV-absorbing pigments in fish eye tissues. Comp. Biochem. Physiol. 93B:601–607
Dykens, J. A., Shick, J. M., Benoit, C., Buettner, G. R., Winston, G. W. (1992). Oxygen radical production in the sea anemoneAnthopleura elegantissima and its endosymbiotic algae. J. exp. Biol. 168:219–241
Einarsson, S., Josefsson, B., Lagerkvist, S. (1983). Determination of amino acids with 9-fluorenylmethyl chloroformate and reversed-phase high-performance liquid chromatography. J. Chromat. 282:609–618
Favré-Bonvin, J., Bernillon, J., Salin, N., Arpin, N. (1987). Biosynthesis of mycosporines: mycosporine glutaminol inTrichothecium roseum. Phytochem. 26:2509–2514
Fleischmann, E. M. (1989). The measurement and penetration of ultraviolet radiation into tropical marine water. Limnol. Oceanogr. 34:1623–1629
Floss, H. G. (1979). The shikimate pathway. In: Swain, T., Harborne, J. B., van Sumene, C. F. (eds.) Recent advances in phytochemistry: biochemistry of plant phenolics, Vol. 12. Plenum Press, New York, p. 59–89
Frederick, J. E., Weatherhead, E. C., Haywood, E. K. (1991). Longterm variations in ultraviolet sunlight reaching the biosphere: calculations for the past three decades. Photochem Photobiol. 54:781–788
Gardner, W. S., Miller W. H., III. (1980). Rervese-phase liquid chromatographic analysis of amino acids after reaction witho-phthalaldehyde. Analyt. Biochem. 101:61–65
Gattuso, J.-P. (1987). Ecomorphologic, métabolisme, croissance et calcification du scléractiniare à zooxanthelles,Stylophora pistillata (Golfe d'Aquaba, Mer Rouge) — influence de l'éclairement. Thèse de Doctorat, Université d'Aix-Marseille II
Grant, P. T., Middleton, C., Plack, P. A., Thomson, R. H. (1985). The isolation of four aminocyclohexenimines (mycosporines) and a structurally related derivative of cyclohexane-1:3-dione (gadusol) from the brine shrimp,Artemia. Comp. Biochem. Physiol. 80B:755–759
Grant, P. T., Plack, P. A., Thomson, R. H. (1980). Gadusol, a metabolite from fish eggs. Tetrahedron Lett. 21:4043–4044
Harm, W. (1980). Biological effects of ultraviolet radiation. Cambridge University Press, Cambridge
Herndl, G. J., Velimirov, B. (1985). Bacteria in the coelenteron of Anthozoa: control of coelenteric bacterial density by the coelenteric fluid. J. exp. mar. Biol. Ecol. 93:115–130
Hirata, Y., Uemura, D., Ueda, K., Takano, S. (1979). Several compounds fromPalythoa tuberculosa (Coelenterata). Pure appl. Chem. 51:1875–1883
Ito, S., Hirata, Y. (1977). Isolation and structure of a mycosporine from the zoanthidPalythoa tuberculosa. Tetrahedron Lett. 28: 2429–2430
Jokiel, P. L. (1980) Solar ultraviolet radiation and coral reef epifauna. Science, N.Y. 207:1069–1071
Jokiel, P. L., York, R. H., Jr. (1982). Solar ultraviolet photobiology of the reef coralPocillopora damicornis and symbiotic zooxanthellae. Bull. mar. Sci. 32:301–315
karentz, D., McEuen, F. S., Land, M. C., Dunlap, W. C. (1991). Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: potential protection from ultraviolet exposure. Mar. Biol. 108:157–166
Kasschau, M. R., Skisak, C. M., Cook, J. P., Mills, W. R. (1984). β-alanine metabolism and high salinity stress in the sea anemone,Bunodosoma cavernata. J. comp. Physiol. (Sect. B) 154:181–186
Kyle, D. J. (1987) The biochemical basis for photoinhibition of photosystem II. In: Kyle, D. J., Osmond, C. B., Arntzen, C. J. (eds.) Photoinhibition. Elsevier Science Publishers, Amsterdam, p. 197–226
Lesser, M. P., Shick, J. M. (1989). Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae ofAiptasia pallida: primary production photoinhibition, and enzymic defenses against oxygen toxicity. Mar. Biol. 102:243–255
Male, K. B., Storey, K. B. (1983). Kinetic characterization of NADP specific glutamate dehydrogenase from the sea anemone,Anthopleura xanthogrammica: control of amino acid biosynthesis during osmotic stress. Comp. Biochem. Physiol. 76B:823–829
Maragos, J. E. (1972). A study of the ecology of Hawaiian reef corals. Doctoral Dissertation, University of Hawaii, Honolulu, Hawaii
Nakamura, H., Kobayashi, J., Hirata, Y. (1982). Separation of mycosporine-like amino acids in marine organisms using reverse-phase high-performance liquid chromatography. J. Chromat. 250:113–118
Palincsar, E. E., Jones, W. R. Palincsar, J. S., Glogowski, M. A., Jastro, J. L. (1989). Bacterial aggregates within the epidermis of the sea anemoneAiptasia pallida. Biol. Bull. mar. biol. Lab., Woods Hole 177:130–140
Pearse, V. B. (1974). Modification of sea anemone behavior by symbiotic zooxanthellae: phototaxis. Biol. Bull. mar. biol. Lab., Woods Hole 147:630–640
Renger, G., Voss, M., Grabe, P., Shulze, S. (1986). Effect of UV irradiance on different partial reactions of the primary process of photosynthesis. In: Worrest, R. C., Caldwell, M. M. (eds.) Stratospheric ozone reduction, solar ultraviolet radiation and plant life. Springer-Verlag, Berlin, p. 171–184
Scelfo, G. (1985). The effects of visible and ultraviolet solar radiation on a UV-absorbing compound and chlorophylla in a Hawaiian zoanthid. Proc. 5th int. coral Reef Congress 6:107–112 [Gabrié, C. et al. (eds.) Antenne Museum-EPHE, Moorea, French Polynesia]
Scelfo, G. (1986). Relationship between solar radiation and pigmentation of the coralMontipora verrucosa and its zooxanthellae. In: Jokiel, P. L., Richmond, R. H., Rogers, R. A. (eds.) Coral reef population biology. Hawaiian Institute of Marine Biology Technical Report No. 37, Honolulu, p. 440–451
Scelfo, G. M. (1988a). A study of the effects of visible and ultraviolet radiation on pigment and UV-absorbing compounds inAnthopleura elegantissima, Master of Science Thesis, University of California, Santa Cruz, California
Scelfo, G. M. (1988b). Ultraviolet-B absorbing compounds inAnthopleura elegantissima. Am. Zool. 28: 105A
Schumacher, H., Zibrowius, H. (1985). What is hermatypic? A redefinition of ecological groups in corals and other organisms. Coral Reefs 4:1–9
Secreast, S. L. (1991). Anion-exchange chromatography on selected silica-based reversed-phase high-performance liquid chromatographic columns. J. Chromat. 544:99–111
Shibata, K. (1969). Pigment and a UV-absorbing substance in corals and a blue-green alga living in the Great Barrier Reef. Pl. Cell Physiol., Tokyo 10:325–335
Shick, J. M. (1976). Ecological physiology and genetics of the colonizing actinarianHaliplanella luciae. In: Mackie, G. O. (ed). Coelenterate ecology and behavior. Plenum Press, New York, p. 137–146
Shick, J. M. (1991). A functional biology of sea anemones. Chapman & Hall, London
Shick, J. M. (1993). Solar UV and oxidative stress in algal-animal symbioses. In: Shima, A., Ichihashi, M., Fujiwara, Y., Takebe, H. (eds.) Frontiers of photobiology, Elsevier Science Publishers, Amsterdam, p. 561–564
Shick, J. M., Dunlap, W. C., Chalker, B. E., Banaszak, A. T., Rosenzweig, T. K. (1992). Survey of ultraviolet radiation-absorbing mycosporine-like acids in organs of coral reef holothuroids. Mar. Ecol. Prog. Ser. 90:139–148
Shick, J. M., Dykens, J. A. (1984). Photobiology of the symbiotic sea anemoneAnthopleura elegantissima: photosynthesis, respiration, and behavior under intertidal conditions. Biol. Bull. mar. biol. Lab., Woods Hole 166:608–619
Shick, J. M., Lesser, M. P., Stochaj, W. R. (1991) Ultraviolet radiation and photooxidative stress in zooxanthellate Anthozoa: the sea anemonePhyllodiscus semoni and the octocoralClavularia sp. Symbiosis 10:145–173
Siebeck, O. (1981). Photoreactivation and depth-dependent UV tolerance in reef corals in the Great Barrier Reef/Australia. Naturwissenschaften 68:426–428
Siebeck, O. (1988) Experimental investigation of UV tolerance in hermatypic corals (Scleractinia). Mar. Ecol. Prog. Ser. 43:95–103
Smith, R. C., Baker, K. S. (1979). Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem. Photobiol. 29:311–323
Sokal, R. R., Rohlf, F. J. (1981). Biometry, 2nd edn. W. H. Freeman and Co., San Francisco, California
Stochaj, W. R. (1989). Photoprotective mechanisms in cnidarians: UV-absorbing compounds and behavior. Master of Science Thesis, University of Maine, Orono, Maine
Stochaj, W. R., Shick, J. M., Dunlap, W. C. (1989). Bathymetric changes in the mycosporine-like amino acids of the scleractinian coralAcropora microphthalma and its zooxanthellae. Am. Zool. 29:82A
Takano, S., Nakanishi, A., Uemura, D., Hirata, Y. (1979). Isolation and structure of a 334 nm UV-absorbing substance, Porphyra-334 from the red algaPorphyra tenera Kjellman. Chem. Lett. 419–420
Towers, G. H. N., Subba Rao, P. V. (1972). Degradative metabolism of phenylalanine, tyrosine and DOPA. In: Runeckles, V. C. (ed.) Recent advances in phytochemistry, Vol. 4, Appleton-Century-Crofts, New York, p. 1–43
Tsujino, I., Yabe, K., Sekikawa, I. (1980). Isolation and structure of a new amino acid, shinorine, from the red algaChondrus yendoi Yamada et Mikami. Bot. Mar. 23:65–68
Worrest, R. C. (1982) Review of the literature concerning the impact of UV-B radiation upon marine organisms. In: Calkins, J. (ed.) The role of solar ultraviolet radiation in marine ecosystems. Plenum Press, New York, p. 429–457
Yoshida, S. (1969). Biosynthesis and conversion of aromatic amino acids in plants. A. Rev. Pl. Physiol. 20:41–62
Zar, J. H. (1984). Biostatistical analysis, 2nd edn. Prentice-Hall, Inc., Englewood Cliffs, New Jersey
Author information
Authors and Affiliations
Additional information
Communicated by J. P. Grassle, New Brunswick
Rights and permissions
About this article
Cite this article
Stochaj, W.R., Dunlap, W.C. & Shick, J.M. Two new UV-absorbing mycosporine-like amino acids from the sea anemoneAnthopleura elegantissima and the effects of zooxanthellae and spectral irradiance on chemical composition and content. Mar. Biol. 118, 149–156 (1994). https://doi.org/10.1007/BF00699229
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00699229