Abstract
Short-term variations of mycosporine-like amino acids (MAAs) in Pyropia columbina (Montage) W.A. Nelson exposed to nitrate (NO3-) enrichment under different outdoor light treatments during the spring ozone depletion of 2008 in Punta Arenas (Chile) were investigated. Segments of P. columbina thalli were cultivated under three treatments of solar radiation without or with NO3- supply (0.38 mmol l-1): PAR (P), PAR+UVA (PA), and PAR+UVA+UVB (PAB). Samples were taken at 8:00 h (initial value), 9:30, 12:30, 15:30, and 18:00 h on November 8 and at 9:00 h on November 9 (recovery period). A complex dynamic of MAAs affected by light quality and NO3- supply was observed. During the light period, the highest content of MAAs was reached under PAB and NO3- enrichment, whereas MAAs increased during the recovery period in P and PAB with no NO3- supply. Five MAAs were identified: porphyra-334, shinorine, asterina-330, palythine, and mycosporine-glycine. The hourly accumulation of each MAA varied mainly according to the time of exposure and NO3- supply. In general, the percentage of porphrya-334 increased, whereas the other MAAs decreased during the exposure period. These results suggest that MAA content in P. columbina varied in the short-term (hours) and the changes were related to the solar irradiance received and NO3- availability.
This study was part of a PhD thesis by Nelso Navarro, who is also grateful for a doctoral fellowship to CONICYT-Chile. We thank José Barufi and César Cárdenas for the valuable suggestions and for scientific discussions. This work was financed in part by the Project CGL08-05407 C03-01.
References
Abdala-Díaz, R.T., A. Cabello-Pasini, E. Pérez-Rodríguez, R.M. Conde Álvarez and F.L. Figueroa. 2006. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar. Biol.148: 459–465.10.1007/s00227-005-0102-6Search in Google Scholar
Aguilera, J., A. Dummermuth, U. Karsten, R. Schriek and C. Wiencke. 2002. Enzymatic defences against photooxidative stress induced by ultraviolet radiation in Arctic marine macroalgae. Polar Biol. 25: 432–441.10.1007/s00300-002-0362-2Search in Google Scholar
Aracena, C., C.B. Lange, J.L. Iriarte, L. Rebolledo and S. Pantoja. 2011. Latitudinal patterns of export production recorded in surface sediments of the Chilean Patagonian fjords (41–55°S) as a response to water column productivity. Cont. Shelf. Res. 31: 340–355.10.1016/j.csr.2010.08.008Search in Google Scholar
Bischof, K., D. Hanelt and C. Wiencke. 2000. Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta. 211: 555–562.10.1007/s004250000313Search in Google Scholar PubMed
Bischof, K., I. Gómez, M. Molis, D. Hanelt, U. Karsten, U. Lüder, M.Y. Roleda, K. Zacher and C. Wiencke. 2006. Ultraviolet radiation shapes seaweed communities. Rev. Environ. Sci. Biotechnol.5: 141–166.10.1007/s11157-006-0002-3Search in Google Scholar
Bonomi-Barufi, J., N. Korbee, M. Oliveira and F.L. Figueroa. 2011. Effects of N supply on the accumulation of photosynthetic pigments and photoprotectors in Gracilaria tenuistipitata (Rhodophyta) cultured under N limitation. J. Appl. Phycol. 23: 457–466.10.1007/s10811-010-9603-xSearch in Google Scholar
Callone, A.I., M.O. Carignan, N.G. Montoya and J.I. Carreto. 2006. Biotransformation of mycosporine-like amino acids (MAAs) in the toxic dinoflagellate Alexandrium tamarense. J. Photochem. Photobiol. B: Biol. 84: 204–212.10.1016/j.jphotobiol.2006.03.001Search in Google Scholar PubMed
Carreto, J.I., M.O. Carignan, D. Daleo and S.G. De Marco. 1990. Occurrence of mycosporine-like amino acids in the red-tide dinoflagellate Alexandrium excavantum: UV-photoprotective compounds? J. Plankton Res.12: 909–922.10.1093/plankt/12.5.909Search in Google Scholar
Cockell, C.S. and J. Knowland. 1999. Ultraviolet radiation screening compounds. Biol. Rev. 74: 311–345.10.1017/S0006323199005356Search in Google Scholar
Conde, F.R., M.S. Churio and C.M. Previtali. 2004. The deactivation pathways of the excited-states of the mycosporine-like amino acids shinorine and porphyra-334 in aqueous solution. Photochem. Photobiol. Sci. 3: 960–967.10.1039/b405782aSearch in Google Scholar PubMed
Connan, S., F. Delisle, E. Deslandes and E. Ar Gall. 2006. Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot. Mar.49: 39–46.10.1515/BOT.2006.005Search in Google Scholar
De la Coba, F., J. Aguilera, F.L. Figu eroa, M.V. Gálvez and E. Herrera. 2009. Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J. Appl. Phycol.21: 161–169.10.1007/s10811-008-9345-1Search in Google Scholar
Dummermuth, A.L., U. Karsten, K.M. Fisch, G.M. König and C. Wiencke. 2003. Responses of marine macroalgae to hydrogen-peroxide stress. J. Exp. Mar. Biol. Ecol.289: 103–121.10.1016/S0022-0981(03)00042-XSearch in Google Scholar
Dunlap, W.C. and J.M. Shick. 1998. UV radiation absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J. Phycol. 34: 418–430.10.1046/j.1529-8817.1998.340418.xSearch in Google Scholar
Dunlap, W.C. and Y. Yamamoto. 1995. Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp. Biochem. Physiol. 112B: 105–114.10.1016/0305-0491(95)00086-NSearch in Google Scholar
Figueroa, F.L. and I. Gómez. 2001. Photosynthetic acclimation to solar UV radiation of marine red algae from warm-temperate coast of southern Spain: a review. J. Appl. Phycol. 13: 235–248.Search in Google Scholar
Figueroa, F.L., S. Salles, J. Aguilera, C. Jiménez, J. Mercado, B. Viñegla, A. Flores-Moya and M. Altamirano. 1997. Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta Thur. in Le Jol. Mar. Ecol. Prog. Ser. 151: 81–90.10.3354/meps151081Search in Google Scholar
Figueroa, F.L., A. Bueno, N. Korbee, R. Santos, L. Mata and A. Schuenhoff. 2008. Accumulation of mycosporine-like amino acids in Asparagopsis armata grown in tanks with fishpond effluents of gilthead sea bream Asparus aurata. J. World Aquacul. Soc.39: 692–699.10.1111/j.1749-7345.2008.00199.xSearch in Google Scholar
Figueroa, F.L., N. Korbee, R. Abadala, C. Jerez, M. López De La Torre, L. Güenaga, M.A. Larrubia and J.L. Gómez-Pinchetti. 2012. Biofiltration of fishpond effluents and accumulation of N-compounds (phycobiliproteins and mycosporine like amino acids) versus C compounds (polysaccharides) in Hydropuntia cornea (Rhodophyta). Mar. Poll.64: 310–318.10.1016/j.marpolbul.2011.11.012Search in Google Scholar
Flores-Moya, A., D. Hanelt, F.L. Figueroa, M. Altamirano, B. Viñegla and S. Salles. 1999. Involvement of solar UV-B radiation in recovery of inhibited photosynthesis in the brown alga Dictyota dichotoma (Hudson) Lamouroux. J. Photochem. Photobiol. B: Biol.49: 129–135.10.1016/S1011-1344(99)00046-9Search in Google Scholar
Franklin, L. and R. Forster. 1997. The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur. J. Phycol.32: 207–232.Search in Google Scholar
Franklin, L., I. Yakovleva, U. Karsten and K. Lüning. 1999. Synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae) and the consequences for sensitivity to ultraviolet B radiation. J. Phycol. 35: 682–693.10.1046/j.1529-8817.1999.3540682.xSearch in Google Scholar
Franklin, L.A., G. Kräbs and R. Kuhlenkamp. 2001. Blue light and UVA radiation control the synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae). J. Phycol. 37: 257–270.10.1046/j.1529-8817.2001.037002257.xSearch in Google Scholar
Gómez, I., E. Pérez-Rodríguez, B. Viñegla, F.L. Figueroa and U. Karsten. 1998. Effects of solar radiation on photosynthesis, UV-absorbing compounds and enzyme activities of the green alga Dasycladus vermicularis from southern Spain. J. Photochem. Photobiol. B: Biol.47: 46–57.Search in Google Scholar
Hanelt, D. and M.Y. Roleda. 2009. UVB radiation may ameliorate photoinhibition in specific shallow-water tropical marine macrophytes. Aquat. Bot. 91: 6–12.10.1016/j.aquabot.2008.12.005Search in Google Scholar
Hegglin, M.I. and T.V. Shepherd. 2009. Large climate induced changes in ultraviolet index and stratospheric to tropospheric flux. Nature Geosciences2: 687–691.10.1038/ngeo604Search in Google Scholar
Helbling, E.W., E.S. Barbieri, R.P. Sinha, V.E. Villafañe and D.P. Häder. 2004. Dynamics of potentially protective compounds in Rhodophyta species from Patagonia (Argentina) exposed to solar radiation. J. Photochem. Photobiol. B: Biol.75: 63–71.10.1016/j.jphotobiol.2004.05.006Search in Google Scholar PubMed
Hoyer, K., U. Karsten, T. Sawall and C. Wiencke. 2001. Photoprotective substances in Antarctic macroalgae and their variation with respect to depth distribution, different tissues and developmental stages. Mar. Ecol. Prog. Ser. 211: 117–129.Search in Google Scholar
Hoyer, K., U. Karsten and C. Wiencke. 2002. Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar. Biol. 41: 619–627.10.1007/s00227-002-0871-0Search in Google Scholar
Huovinen, P., I. Gómez, F.L. Figueroa, N. Ulloa, V. Morales and C. Lovengreen. 2004. Ultraviolet-absorbing mycosporine-like amino acids in red macroalgae from Chile. Bot. Mar. 47: 21–29.10.1515/BOT.2004.003Search in Google Scholar
Huovinen, P., J. Matos, I.S. Pinto and F.L. Figueroa. 2006. The role of ammonium in photoprotection against high irradiance in the red alga Grateloupia lanceola. Aquat. Bot. 24: 308–316.10.1016/j.aquabot.2005.12.002Search in Google Scholar
Jiang, H., K. Gao and E.W. Helbling. 2008. UV-Absorbing compounds in Porphyra haitanensis (Rhodophyta) with special reference to effects of desiccation. J. Appl. Phycol.20: 387–395.10.1007/s10811-007-9268-2Search in Google Scholar
Jones, L.W. and B. Kok. 1966. Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol. 41: 1037–1043.10.1104/pp.41.6.1037Search in Google Scholar PubMed PubMed Central
Karentz, D., J.E. Cleaver and D.L. Mitchell. 1991. Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. J. Phycol. 27: 326–341.10.1111/j.0022-3646.1991.00326.xSearch in Google Scholar
Karsten, U., T. Sawall, D. Hanelt, K. Bischof, F.L. Figueroa, A. Flores-Moya and C. Wiencke. 1998a. An inventory of UV-absorbing mycosporine-like amino acids in macroalgae from polar to warm-temperate regions. Bot. Mar. 41: 443–453.10.1515/botm.1998.41.1-6.443Search in Google Scholar
Karsten, U., L.A. Franklin, K. Lüning and C. Wiencke. 1998b. Natural ultraviolet radiation and photosynthetically active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta.205: 257–262.10.1007/s004250050319Search in Google Scholar
Karsten, U., A. Dummermuth, K. Hoyer and C. Wiencke. 2003. Interactive effects of ultraviolet radiation and salinity on the ecophysiology of two Arctic red algae from shallow waters. Polar Biol. 26: 249–258.10.1007/s00300-002-0462-zSearch in Google Scholar
Kirchhoff, V.W.J.H., F. Zamorano and C. Casiccia. 1997. UVB enhancements at Punta Arenas, Chile. J. Photochem. Photobiol. B: Biol.38: 174–177.Search in Google Scholar
Korbee, N., P. Huovinen, F.L. Figueroa, J. Aguilera and U. Karsten. 2005a. Availability of ammonium influences photosynthesis and the accumulation of mycosporine-like amino acids in two Porphyra species (Bangiales, Rhodophyta). Mar. Biol.146: 645–654.10.1007/s00227-004-1484-6Search in Google Scholar
Korbee, N., F.L. Figueroa and J. Aguilera. 2005b. Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J. Photochem. Photobiol. B: Biol.80: 71–78.10.1016/j.jphotobiol.2005.03.002Search in Google Scholar
Korbee, N., M.T. Mata and F.L. Figueroa. 2010. Photoprotection mechanisms against ultraviolet radiation in Heterocapsa sp. (Dinophyceae) are influenced by nitrogen availability: Mycosporine-like amino acids vs. xanthophyll cycle. Limnol Oceanogr 55: 899–908.10.4319/lo.2010.55.2.0899Search in Google Scholar
Korbee-Peinado, N., R. Abdala-Díaz and F.L. Figueroa. 2004. Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from Patagonia, Argentina. J. Phycol. 40: 248–259.Search in Google Scholar
Kräbs, G., K. Bischof, D. Hanelt, U. Karsten and C. Wiencke. 2002. Wavelength dependent induction of UV-absorbing mycosporine-like amino acids in the red alga Chondrus crispus under natural solar radiation. J. Exp. Mar. Biol. Ecol.268: 69–82.10.1016/S0022-0981(01)00380-XSearch in Google Scholar
Kräbs, G., M. Watanabe and C. Wiencke. 2004. A monochromatic action spectrum for the photoinduction of the UV-absorbing mycosporine-like amino acid shinorine in the red alga Chondrus crispus. Photochem. Photobiol. 79: 515–519.10.1562/2003-12-14-RA.1Search in Google Scholar PubMed
Lesser, M.P. 1996. 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: 287–297.10.3354/meps132287Search in Google Scholar
López-Figueroa, F. 1992. Diurnal variations in pigment contents in Porphyra laciniata and in Chondrus crispus and its relation to the diurnal changes of underwater light quality and quantity. Mar. Ecol. 13: 285–305.10.1111/j.1439-0485.1992.tb00356.xSearch in Google Scholar
López-Figueroa, F. and F.X. Niell. 1991. Photocontrol of chlorophyll and biliprotein synthesis in seaweeds: possible photoreceptors and ecological considerations. Sci. Mar.55: 519–527.Search in Google Scholar
McKenzie, R.L., P.J. Aucamp, A.F. Bais, L.O. Björn and M. Ilyas. 2007. Changes in biologically active ultraviolet radiation reaching the Earth’s surface. Photochem. Photobiol. Sci. 6: 218–231.10.1039/B700017KSearch in Google Scholar
Mitchell, D.L. and D. Karentz. 1993. The induction and repair of DNA photodamage in the environment. In: (A.R. Young, L.O. Björn, J. Moan and W. Nultsch, eds.), Environment UV Photobiology. Plenum Press, New York. pp. 345–377.Search in Google Scholar
Navarro, N.P., A. Mansilla and M. Palacios. 2008. UVB effects on early developmental stages of commercially important macroalgae in southern Chile. J. Appl. Phycol. 20: 897–906.10.1007/s10811-007-9276-2Search in Google Scholar
Orce, V.L. and W. Helbling. 1997. Latitudinal UVR-PAR measurements in Argentina: extent of the ozone hole. Glob Planet Change.15: 113–121.10.1016/S0921-8181(97)00007-6Search in Google Scholar
Pakker, H., C.A.C. Beekman and A. Breeman. 2000. Efficient photoreactivation of UVBR induced DNA damage in the sublittoral macroalga Rhodymenia pseudopalmata (Rhodophyta). Eur. J. Phycol. 35: 109–114.10.1080/09670260010001735691Search in Google Scholar
Rautenberger, R., A. Mansilla, I. Gómez, C. Wiencke and K. Bischof. 2009. Photosynthetic responses to UV-radiation of intertidal macroalgae from the Strait of Magellan (Chile). Rev. Chil. Hist. Nat. 82: 43–61.10.4067/S0716-078X2009000100003Search in Google Scholar
Roleda, M.Y., W.H. van de Poll, D. Hanelt and C. Wiencke. 2004. PAR and UVBR effects on photosynthesis, viability, growth and DNA in different life stages of two coexisting Gigartinales: implications for recruitment and zonation pattern. Mar. Ecol. Prog. Ser. 281: 37–50.Search in Google Scholar
Rüdiger, W. and F. López-Figueroa. 1992. Photoreceptors in algae. Photochem. Photobiol. 55: 949–954.10.1111/j.1751-1097.1992.tb08542.xSearch in Google Scholar
Rundel, R.D. 1983. Action spectra and estimation of biologically effective UV radiation. Physiol. Plant.58: 360–366.10.1111/j.1399-3054.1983.tb04195.xSearch in Google Scholar
Seckmeyer, G. and R.L. McKenzie. 1992. Increased ultraviolet radiation in New Zealand (45° S) relative to Germany (48° N). Nature.359: 135–137.10.1038/359135a0Search in Google Scholar
Setlow, R.B. 1974. The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Natl. Acad. Sci. USA71: 3363–3366.10.1073/pnas.71.9.3363Search in Google Scholar PubMed PubMed Central
Shick, J.M., S.D. Romaine-Lioud, C. Ferrier-Pages and J.P. Gattuso. 1999. Ultraviolet-B radiation stimulates 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: 1667–1682.10.4319/lo.1999.44.7.1667Search in Google Scholar
Sutherland, J.E., S.C. Lindstrom, W.A. Nelson, J. Brodie, M.D. Lynch, M.S. Hwang, H.G. Choi, M. Miyata, N. Kikuchi, M.C. Oliveira, T. Farr, C. Neefus, A. Mols-Mortensen, D. Milstein and K.M. Müller. 2011. A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J. Phycol.47: 1131–1151.10.1111/j.1529-8817.2011.01052.xSearch in Google Scholar
Talarico, L. and G. Maranzana. 2000. Light and adaptive responses in red macroalgae: an overview. J. Photochem. Photobiol. B: Biol.56: 1–11.10.1016/S1011-1344(00)00046-4Search in Google Scholar
Ursi, S. and E.M. Plastino. 2001. Crescimento in vitro de linhagens de coloração vermelha e verde clara de Gracilaria birdiae (Gracilariales, Rhodophyta) em dois meios de cultura: análise de diferentes estádios reprodutivos. Revta. Brasil. Bot. 24: 585–592.Search in Google Scholar
van de Poll, W., A. Eggert, A. Buma and A. Breeman. 2001. Effects of UV-B- induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-relates differences in UV-B tolerance. J. Phycol. 37: 30–37.10.1046/j.1529-8817.2001.037001030.xSearch in Google Scholar
Villafañe, V., K. Sundbäck, F.L. Figueroa and E.W. Helbling. 2002. Photosynthesis in the aquatic environment as affected by UVR. In: (E.W. Helbling and H. Zagarase, eds.), UV Effects in Aquatic Organisms and Ecosystems. Comprehensive Series in Photochemical and Photobiological Sciences. The Royal Society of Chemistry, Cambridge, pp. 357–397.Search in Google Scholar
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