Abstract
Epiphytic red algae of the order Ceramiales from mangroves and salt marshes (nine species from Bostrychia, three from Stictosiphonia and four from Caloglossa) produce varying levels of the UV-absorbing compounds mycosporine-glycine, shinorine, porphyra-334, palythine, asterina-330 and palythinol, a suite of substances chemically assigned as mycosporine-like amino acids (MAAs). Mean MAA levels varied from 0.02 to 12.8 mg g−1 DW in field-collected and laboratory cultured specimens. While in field samples of Bostrychia montagneiHarvey, Bostrychia radicans (Montagne) Montagne and Caloglossa apomeiotica J.West et G.Zuccarello MAA concentrations were generally higher compared to cultured plants of the same taxa, Bostrychia tenella(Lamouroux) J.Agardh did not show such a difference. Catenella caespitosa (Withering) L.Irvine, Catenella impudica (Montagne) J.Agardh and Catenella nipae Zanardini (Gigartinales, Caulacanthaceae) produce two novel UV-absorbing compounds: MAA-1 (1.4–4.3 mg g −1 DW) and MAA-2 (0.1–1.0 mg g−1 DW), which absorb at 334 nm and 320 nm, respectively. In laboratory culture of Bostrychia moritziana when photosynthetically active radiation (PAR) was increased from 20 to 40 μmol photons m−2 s−1, the total level of palythinol increased by 85% (from 2.0 to 3.7 mg g−1 DW). In a culture of Caloglossa leprieurii when PAR was increased from 40 to 80 μmol m−2 s−1the porphyra-334 content increased by 77% (from 3.1 to 5.5 mg g−1 DW). Extremely high MAA contents of >30 mg g−1 DW were detected in mature tetrasporangial sori prepared from two isolates of laboratory-cultured reproductive Caloglossa apomeiotica compared to vegetative plants (about 10 mg MAAs g−1 DW) indicating tetraspores loaded up with UV-sunscreens. All data demonstrate that mangrove red algae contain high MAA concentrations, particularly the reproductive structures, and hence these compounds may act as biochemical photoprotectants against exposure to UV-radiation.
Similar content being viewed by others
References
Aguilera, J., U. Karsten, H. Lippert, E. Philip, B. Vögele, D. Hanelt &; C. Wiencke, 1999. Effects of solar radiation on growth, photosynthesis and respiration of marine macroalgae from the Arctic. Mar. Ecol. Prog. Ser. 191: 109–119.
Bandaranayake, W. M., 1998. Mycosporines: are they nature's sunscreens? Nat. Prod. Rep. 15: 159–172.
Britt, A. B., 1995. Repair of DNA damage induced by ultraviolet radiation. Plant Physiol. 108: 891–896.
Buma, A. G. J., E. J. Van Hannen, L. Roza, M. J. W. Veldhuis &; W. W. C. Gieskes, 1995. Monitoring ultraviolet-B-induced DNA damage in individual diatom cells by immunofluorescent thymine dimer detection. J. Phycol. 31: 314–321.
Buma, A. G. J., A. H. Engelen &; W. W. C. Gieskes, 1997. Wavelength-dependent induction ofthymine dimers and growth rate reduction in the marine diatom Cyclotella sp. exposed to ultraviolet radiation. Mar. Ecol. Prog. Ser. 153: 91–97.
Cullen, J. J., P. J. Neale &; M. P. Lesser, 1992. Biological weighting function for the inhibitionof phytoplankton photosynthesis by ultraviolet radiation. Science 258: 646–650.
Davidson, A. T., H. J. Marchant &; W. K. De la Mare, 1996. Natural UVB exposure changesthe species composition of Antarctic phytoplankton in mixed culture. Aquat. Microb. Ecol. 10: 299–305.
Dawes, C. J., 1996. Macroalgal diversity, standing stock and productivity in a northern mangalon the west coast of Florida. Nova Hedwigia 112: 525–535.
Dionisio-Sese, M. L., M. Ishikura, T. Maruyama &; S. Miyachi, 1997. UV-absorbingsubstances in the tunic of a colonial ascidian protect its symbiont, Prochloron sp., fromdamage by UV-B radiation. Mar. Biol. 128: 455–461.
Dunlap, W. C., B. E. Chalker &; J. K. Oliver, 1986. Bathymetric adaptions of the 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. &; Y. Yamamoto, 1995. Small-molecule antioxidants in marine organisms: Antioxidant activity of mycosporineglycine. Comp. Biochem. Physiol. 112B: 105–114.
Dunlap, W. C. &; J. M. Shick, 1998. Ultraviolet radiation-absorbing mycosporine-like aminoacids in coral reef organisms: a biochemical and environmental perspective. J. Phycol. 34: 418–430.
Fleischmann, E. M., 1989. The measurement and penetration of ultraviolet radiation into tropical marine water. Limnol. Oceanogr. 34: 1623–1629.
Forster, R. M. &; M. J. Dring, 1993. Influence of blue light on the photosynthetic capacity of marine plants from different taxonomic, ecological and morphological groups. Europ. J. Phycol. 29: 21–27.
Franklin, L. A. &; R. M. Forster, 1997. The changing irradiance environment: consequences formarine macrophyte physiology, productivity and ecology. Europ. J. Phycol. 32: 207–232.
Franklin, L. A., I. Yakovleva, U. Karsten &; K. Lüning, 1999. synthesis of mycosporine-likeamino acids in Chondrus crispus (Florideophyceae) and the consequences for sensitivity to ultraviolet B radiation. J. Phycol. 35: 682–693.
Garcia-Pichel, F., C. E. Wingard &; R. W. Castenholz, 1993. Evidence regarding the UVsunscreen role of a mycosporine-like compound in the cyanobacterium Gloeocapsa sp. Appl. Envir. Microbiol. 59: 170–6.
Gleason, D. F., 1993. Differential effects of ultraviolet radiation on green and brown morphsof the Carribean coral Porites astreoides. Limnol. Oceangr. 38: 1452–1463.
Häder, D. P. &; F. L. Figueroa, 1997. Photoecophysiology of marine macroalgae. Photochem. Photobiol. 66: 1–14.
Hannach, G. &; A. C. Sigleo, 1998. Photoinduction of UV-absorbing compounds in six speciesof marine phytoplankton. Mar. Ecol. Progr. Ser. 174: 207–222.
Helbing, E. W., B. E. Chalker, W. C. Dunlap, O. Holm-Hansen &; V. E. Villafane, 1996. Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation. J. exp. mar. Biol. Ecol. 204: 85–101.
Karentz, D., F. S. McEuen, M. C. Land &; W. C. Dunlap, 1991. Survey of mycosporine-like amino acid compounds in Antarctic organisms: potential protection from ultravioletexposure. Mar. Biol. 108: 157–166.
Karsten, U., J. A. West &; G. Zuccarello, 1992. Polyol content of Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta) from field and culture. Bot. Mar. 35: 11–19.
Karsten, U. &; J. A. West, 1993. Ecophysiological studies on six species of themangrove redalgal genus Caloglossa. Aust. J. Plant Physiol. 20: 729–739.
Karsten, U., J. A. West &; E. K. Ganesan, 1993. Comparative physiological ecology of Bostrychia moritziana (Ceramiales, Rhodophyta) from freshwater and marine habitats. Phycologia 32: 401–409.
Karsten, U. &; F. Garcia-Pichel, 1996. Carotenoids and mycosporine-like amino acidcompounds in members of the genus Microcoleus (Cyanobacteria): A chemosystematicstudy. Syst. Appl. Microbiol. 19: 285–294.
Karsten, U., T. Sawall, D. Hanelt, K. Bischof, F. L. Figueroa, A. Flores-Moya &; C. Wiencke, 1998a. An inventory of UV-absorbing mycosporine-like amino acids in macroalgae from polar to warm-temperate regions. Bot. Mar. 41: 443–453.
Karsten, U., L. A. Franklin, K. Lüning &; C. Wiencke, 1998b. Natural ultraviolet and photosynthetic active radiation induce formation of mycosporine-like amino acids inthe marine macroalga Chondrus crispus (Rhodophyta). Planta 205: 257–262.
Karsten, U., T. Sawall &; C. Wiencke, 1998c. A survey of the distribution of UV-absorbing substances in tropical macroalgae. Phycol. Res. 46: 271–279.
Karsten, U., K. Bischof, D. Hanelt, H. Tüg &; C. Wiencke, 1999. The effect of ultravioletradiation on photosynthesis and ultraviolet-absorbing substances in the endemic Arctic macroalga Devaleraea ramentacea (Rhodophyta). Physiol. Plant. 105: 58–66.
Karsten, U. &; C. Wiencke, 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: 407–415.
King, R. J. &; C. F. Puttock, 1989. The morphology and taxonomy of Bostrychia Montagne and Stictosiphonia J. Hooker et Harvey (Rhodomelaceae, Rhodophyta). Aust. Syst. Bot. 3: 1–73.
King, R. J. &; C. F. Puttock, 1994. Morphology and taxonomy of Caloglossa (Delesseriaceae, Rhodophyta). Aust. Syst. Bot. 7: 89–124.
Madronich, S., 1993. The atmosphere and UV-B radiation at ground level. In Young, A. R., L. O. Björn, J. Moan &; W. Nultsch (eds), Environmental UV Photobiology. Plenum Press, New York: 1–40.
Maegawa, M., M. Kunieda &; W. Kida, 1993. Difference of the amount of UV absorbing substance between shallow-and deep-water red algae. Jpn. J. Phycol. (Sorui) 41: 351–354.
Molina, X. &; V. Montecino, 1996. Acclimation to UV irradiance in Gracilaria chilensis Bird, McLachlan &; Oliveira (Gigartinales, Rhodophyta). Hydrobiologia 326/327 (Dev. Hydrobiol. 116): 415–420.
Nakamura, H., J. Kobayashi &; Y. Hirata, 1982. Separation of mycosporine-like amino acids inmarine organisms using reversed-phase high-performance liquid chromatography. J. Chromatogr. 250: 113–118.
Neale, P. J., A. T. Banaszak &; C. R. Jarriel, 1998. Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae): mycosporine-like amino acids protect against inhibitionof photosynthesis. J. Phycol. 34: 928–938.
Pedroche, F. P., J. A. West, G. Zuccarello, A. Senties &; U. Karsten, 1995. Marine red algae ofthe mangroves in south Pacific Mexico and Pacific Guatemala. Bot. Mar. 38: 111–119.
Post, E., 1963. Zur Verbreitung und Ökologie der Bostrychia-Caloglossa-Assoziation. Int. Rev. ges. Hydrobiol. 48: 47–152.
Post, E., 1968. Zur Verbreitungs-Ökologie des Bostrychietum. Hydrobiologia 31: 241–316.
Riegger, L. &; D. Robinson, 1997. Photoinduction of UV-absorbing compounds in Antarctic diatoms and Phaeocystis antarctica. Mar. Ecol. Prog. Ser. 160: 13–25.
Scheibe, R., 1990. Light/dark modulation: Regulation of chloroplast enzymes in a new light. Bot. Acta 103: 327–334.
Shick, J. M., M. P. Lesser, W. C. Dunlap, W. R. Stochaj, B. E. Chalker &; J. Wu Won, 1995. Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar. Biol. 122: 41–51.
Sinha, R. P., M. Klisch, A. Gröniger &; D. P. Häder, 1998. Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae. J. Photochem. Photobiol. B: Biol. 47: 83–94.
Sivalingam, P. M., T. Ikawa, Y. Yokohama &; K. Nisizawa, 1974. Distribution of a 334 UV-absorbing substance in algae, with special regard of ist possible physiological roles. Bot. Mar. 17: 23–29.
Sivalingam, P. M. &; K. Nisizawa, 1990. Ozone hole and ist correlation with the characteristic UV-absorbing substance in marine algae. Jpn. J. Phycol. 38: 365–370.
Smith, R. C., B. B. Prezelin, K. S. Baker, R. R. Bidigare, N. P. Boucher, T. Coley, D. Karentz, S. MacIntyre, H. A. Matlick, D. Menzies, M. Ondrusek, Z. Wan &; K. J. Waters, 1992. Ozone depletion: ultraviolet radiation and phytoplankton biology in Antarctic waters. Science 255: 952–959.
Starr, R. C. &; J. A. Zeikus, 1993. UTEX: The culture collection of algae at the University of Texas at Austin, 1993 list of cultures. J. Phycol. 29 (2) SUPPL.: 1–106
Takano, S., D. Uemura &; Y. Hirata, 1978a. Isolation and structure of a new amino acid, palythine, from the zoanthid Palythoa tuberculosa. Tetrahedron Lett. 26: 2299–2300.
Takano, S., D. Uemura &; Y. Hirata, 1978b. Isolation and structure of two new amino acids,palythinol and palythene, from the zoanthid Palythoa tuberculosa. Tetrahedron Lett. 26: 4909–4912.
Tsujino, I., K. Yabe, I. Sekekawa &; N. Hamanaka, 1978. Isolation and structure of amycosporine from the red alga Chondrus yendoi. Tetrahedron Lett. 16: 1401–1402.
Tsujino, I., K. Yabe &; I. Sekekawa, 1980. Isolation and structure of a new amino acid,shinorine, from the red alga Chondrus yendoi Yamada et Mikami. Bot. Mar. 23: 65–68.
West, J. A., G. Zuccarello, E. F. Pedroche &; U. Karsten, 1992. Marine red algae of the mangroves in Pacific Mexico and their polyol content. Bot. Mar. 35: 141–146.
Wiencke, C., I. Gomez, H. Pakker, A. Flores-Moya, M. Altamirano, D. Hanelt, K. Bischof &; F. Figueroa, 2000. Impact of UV radiation on viability, photosynthetic characteristics and DNA of brown algal zoospores: implications for depth zonation. Mar. Ecol. Prog. Ser. (in press).
Yakovleva, J. M., M. Dring &; E. A. Titlyanov, 1998. Tolerance of North Sea algae to UV andvisible radiation. Russ. J. Plant Physiol. 45: 45–54.
Yakovleva, J. M., 1999. Daily dynamics of accumulation of mycosporine-like amino acids as a light-protective response in marine macrophytes of the Sea of Japan. Russ. J. Mar. Biol. 25: 221–223.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Karsten, U., Sawall, T., West, J. et al. Ultraviolet sunscreen compounds in epiphytic red algae from mangroves. Hydrobiologia 432, 159–171 (2000). https://doi.org/10.1023/A:1004046909810
Issue Date:
DOI: https://doi.org/10.1023/A:1004046909810