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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

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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.

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References

  1. 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

  2. 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

  3. Cavanaugh, G. M. (1975). Formulae and methods VI of the Marine Biological Laboratory Chemical Room. Marine Biological Laboratory, Woods Hole, Massachussetts

  4. 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

  5. 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

  6. 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

  7. 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

  8. 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

  9. 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

  10. 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

  11. Favré-Bonvin, J., Bernillon, J., Salin, N., Arpin, N. (1987). Biosynthesis of mycosporines: mycosporine glutaminol inTrichothecium roseum. Phytochem. 26:2509–2514

  12. Fleischmann, E. M. (1989). The measurement and penetration of ultraviolet radiation into tropical marine water. Limnol. Oceanogr. 34:1623–1629

  13. 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

  14. 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

  15. 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

  16. 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

  17. 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

  18. Grant, P. T., Plack, P. A., Thomson, R. H. (1980). Gadusol, a metabolite from fish eggs. Tetrahedron Lett. 21:4043–4044

  19. Harm, W. (1980). Biological effects of ultraviolet radiation. Cambridge University Press, Cambridge

  20. 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

  21. Hirata, Y., Uemura, D., Ueda, K., Takano, S. (1979). Several compounds fromPalythoa tuberculosa (Coelenterata). Pure appl. Chem. 51:1875–1883

  22. Ito, S., Hirata, Y. (1977). Isolation and structure of a mycosporine from the zoanthidPalythoa tuberculosa. Tetrahedron Lett. 28: 2429–2430

  23. Jokiel, P. L. (1980) Solar ultraviolet radiation and coral reef epifauna. Science, N.Y. 207:1069–1071

  24. 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

  25. 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

  26. 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

  27. 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

  28. 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

  29. 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

  30. Maragos, J. E. (1972). A study of the ecology of Hawaiian reef corals. Doctoral Dissertation, University of Hawaii, Honolulu, Hawaii

  31. 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

  32. 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

  33. Pearse, V. B. (1974). Modification of sea anemone behavior by symbiotic zooxanthellae: phototaxis. Biol. Bull. mar. biol. Lab., Woods Hole 147:630–640

  34. 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

  35. 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]

  36. 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

  37. 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

  38. Scelfo, G. M. (1988b). Ultraviolet-B absorbing compounds inAnthopleura elegantissima. Am. Zool. 28: 105A

  39. Schumacher, H., Zibrowius, H. (1985). What is hermatypic? A redefinition of ecological groups in corals and other organisms. Coral Reefs 4:1–9

  40. Secreast, S. L. (1991). Anion-exchange chromatography on selected silica-based reversed-phase high-performance liquid chromatographic columns. J. Chromat. 544:99–111

  41. 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

  42. 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

  43. Shick, J. M. (1991). A functional biology of sea anemones. Chapman & Hall, London

  44. 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

  45. 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

  46. 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

  47. 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

  48. Siebeck, O. (1981). Photoreactivation and depth-dependent UV tolerance in reef corals in the Great Barrier Reef/Australia. Naturwissenschaften 68:426–428

  49. Siebeck, O. (1988) Experimental investigation of UV tolerance in hermatypic corals (Scleractinia). Mar. Ecol. Prog. Ser. 43:95–103

  50. Smith, R. C., Baker, K. S. (1979). Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem. Photobiol. 29:311–323

  51. Sokal, R. R., Rohlf, F. J. (1981). Biometry, 2nd edn. W. H. Freeman and Co., San Francisco, California

  52. Stochaj, W. R. (1989). Photoprotective mechanisms in cnidarians: UV-absorbing compounds and behavior. Master of Science Thesis, University of Maine, Orono, Maine

  53. 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

  54. 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

  55. 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

  56. 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

  57. 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

  58. Yoshida, S. (1969). Biosynthesis and conversion of aromatic amino acids in plants. A. Rev. Pl. Physiol. 20:41–62

  59. Zar, J. H. (1984). Biostatistical analysis, 2nd edn. Prentice-Hall, Inc., Englewood Cliffs, New Jersey

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Correspondence to J. M. Shick.

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Communicated by J. P. Grassle, New Brunswick

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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

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Keywords

  • Radiation
  • Chromatography
  • High Performance Liquid Chromatography
  • Liquid Chromatography
  • Glycine