Scientia Marina, Vol 76, No 1 (2012)

Effect of vertical mixing on short-term mycosporine-like amino acid synthesis in the Antarctic diatom, Thalasiossira sp.


https://doi.org/10.3989/scimar.03203.16D

Marcelo Pablo Hernando
Facultad de Medicina, Universidad de Morón, Argentina

Jose Ignacio Carreto
Instituto Nacional de Investigación y Desarrollo Pesquero, Argentina

Mario Carignan
Instituto Nacional de Investigación y Desarrollo Pesquero, Argentina

Gustavo Adolfo Ferreyra
Institut de Sciences de la Mer de Rimouski, Canada

Abstract


One of the adaptations whereby phytoplankton can alleviate damage induced by ultraviolet radiation (280-400 nm) is the synthesis of mycosporine-like amino acids (MAAs). The synthesis of MAAs was studied after exposure of the Antarctic diatom Thalassiosira sp. isolated from Potter Cove (South Shetland Is., Antarctica) to 2 treatments with a solar simulator: surface (Sfix) and vertical mixing (Mix) irradiance conditions. Light exposure was simulated in daily cycles with maximum irradiance at noon. Only 2 MAAs, Porphyra-334 (82-85%) and Shinorine (15-18%), were identified. The concentration of the two compounds increased during experimental light exposure (50-55%) and declined in the dark (10-15%). During the light period the synthesis rate of MAAs per unit of chlorophyll a was higher in the Sfix treatment (µ=0.17 h-1) than in the Mix treatment (µ=0.05 h-1). In spite of the higher MAA levels, low cell numbers were observed in the Sfix treatment, suggesting that the algae synthesized photoprotective compounds at the expense of growth. Our results document overlapping effects of both daily light cycles and vertical mixing affecting the synthesis of MAAs. This, and the high thermal dissipation of the ultraviolet B radiation energy (280-320 nm) absorbed by these substances, suggest a rapid photoadaptive response of Thalasiossira sp. upon exposure to elevated irradiance in a stratified water column, as well as the complementary role of vertical mixing in photo-protection.

Keywords


mycosporine-like amino acids; vertical mixing; Antarctic diatom; photoadaptive response; UV

Full Text:


PDF

References


Bandaranayake W. 1998. Mycosporines: are they nature’s sunscreens? Nat. Prod. Rep. 15: 159-172. PMid:9586224

Banaszak A. 2003. Photoprotective physiological and biochemical responses of aquatic organisms. In: Helbling E.W., Zagarese H.E. (eds.), UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp. 329-356. http://dx.doi.org/10.1039/9781847552266-00329

Bracher A., Wiencke C. 2000. Simulation of the effects of naturally enhanced UV radiation on photosynthesis of Antarctic phytoplankton. Mar. Ecol. Progr. Ser. 196: 127-141. http://dx.doi.org/10.3354/meps196127

Callone A., Carignan M., Montoya N., Carreto J. 2006. Biotransformation of mycosporine like amino acids (MAAs) in the toxic dinoflagellate Alexandrium tamarense. J. Photochem. Photobiol. B: Biol. 84: 204-212. http://dx.doi.org/10.1016/j.jphotobiol.2006.03.001 PMid:16697653

Carreto J., De Marco S., Lutz V. 1989. UV-absorbing pigments in the dinoflagellates Alexandrium excavatum and Prorocentrum micans. Effects of light intensity. In: Okaichi, T., Anderson, D., Nemoto, T. (eds.), Red Tides: Biology, Environmental Science and Toxicology. Elsevier Science Publishing Co. Inc. pp. 333-336.

Carreto J., Lutz V., De Marco S., Carignan M. 1990a. Fluence and wavelength dependence of mycosporine-like amino acid synthesis in the dinoflagellate Alexandrium excavatum. In: Graneli E., Edler L., Sundström B., Anderson D.M. (eds.), Toxic marine phytoplankton, Elsevier, New York, pp. 275-279.

Carreto J., Carignan M., Daleo G., De Marco S. 1990b. Occurrence of mycosporine-like aminoacids in the red-tide dinoflagellate Alexandrium excavatum: UV-photoprotective compounds? J. Plankton Res. 12: 909-921. http://dx.doi.org/10.1093/plankt/12.5.909

Carreto J., Carignan M., Montoya N. 2001. Comparative studies on mycosporine-like amino acids, paralytic shellfish toxins and pigment profiles of the toxic dinoflagellates Alexandrium tamarense, Alexandrium catenella and Alexandrium minutum. Mar. Ecol. Progr. Ser. 223: 49-60. http://dx.doi.org/10.3354/meps223049

Carreto J., Carignan M., Montoya N. 2002. Short term effects of ultraviolet radiation on the toxic dinoflagellate Alexandrium catenella. Pigment bleaching and MAAs synthesis inhibition. In Brest (ed.) Aquaculture, Environment and Marine Phytoplakton, Ifremer, Actes colloq. 21, pp. 173-189.

Conde F., Churio M., Previtali C. 2000. The photoprotector mechanism of mycosporine-like amino acids. Excited-state properties and photostability of Porphyra-334 in aqueous solution. J. Photochem. Photobiol. B. 56: 139-144. http://dx.doi.org/10.1016/S1011-1344(00)00066-X

Conde F., Churio M., Previtali C. 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. http://dx.doi.org/10.1039/b405782a

Cullen J., Lesser M. 1991. Inhibition of photosynthesis by ultraviolet radiation as a function of dose and dosage rate: Results for a marine diatom. Mar. Biol. 111: 183-190. http://dx.doi.org/10.1007/BF01319699

Davidson A., Bramich D., Marchant H., Mc Minn A. 1994. Effects of UVB irradiation on growth and survival of Antarctic marine diatoms. Mar. Biol. 119: 507-515. http://dx.doi.org/10.1007/BF00354312

Finkel Z., Beardal l., Flynn K., Quigg A., Alwyn Rees V., Raven J. 2010. Phytoplankton in a changing world: cell size and elemental stoichiometry. J. Plankton Res. 32(1): 119-137. http://dx.doi.org/10.1093/plankt/fbp098

Frame E. 2004. Mycosporine-like amino acids (MAAs) in bloom forming phytoplankton: the influence of nitrogen, ultraviolet radiation and species composition. PhD thesis. University of California, San Diego.

Guillard R., Ryther J. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula convervacea Cleve. Can. J. Microbiol. 8: 229-239. http://dx.doi.org/10.1139/m62-029 PMid:13902807

Helbling E., Chalker B., Dunlap W., Holm-Hansen O., Villafañe V. 1996. Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation. J. Exp. Mar. Biol. Ecol. 204: 85-101. http://dx.doi.org/10.1016/0022-0981(96)02591-9

Hernando M. 2011. Fitoplancton de altas latitudes en condiciones de ozono disminuido. Editorial Académica Española, Alemania, 300 pp.

Hernando M., Ferreyra G. 2005. The effects of UV radiation on photosynthesis in an Antarctic diatom (Thalassiosira sp.): does vertical mixing matter? J. Exp. Mar. Biol. Ecol. 325: 35-45 http://dx.doi.org/10.1016/j.jembe.2005.04.021

Hernando M., Carreto J., Carginan M., Ferryra G., Grob C. 2002. Effects of solar radiation on growth and mycosporine-like amino acids content in an Antarctic diatom. Pol. Biol. 25: 12-20. http://dx.doi.org/10.1007/s003000100306

Hughes K. 2003. Influence of seasonal environmental variables on the distribution of presumptive fecal coliforms around an Antarctic Research Station. Appl. and Environ. Microbiol. 69(8): 4884-4891. http://dx.doi.org/10.1128/AEM.69.8.4884-4891.2003 PMid:12902283    PMCid:169114

Holm-Hansen O., Lorenzen C., Holmes R., Strickland J. 1965. Fluorometric determination of chlorophyll. J. Cons. Int. Explor. Mer 30: 3-15.

Holm-Hansen O., Riemann B. 1978. Chlorophyll a determination: improvements in methodology. OIKOS 30: 438-447. http://dx.doi.org/10.2307/3543338

Ivanov A., Miskiewicz E., Clarke A., Greenberg B., Huner N. 2000. Protection of photosystem II against UV-A and UV-B radiation in the cyanobacterium Plectonema boryanum: The role of growth temperature and growth irradiance. Photochem. Photobiol. 72: 772-779. http://dx.doi.org/10.1562/0031-8655(2000)072<0772:POPIAU>2.0.CO;2

Jeffrey S., MacTavish H., Dunlap W., Vesk M., Groenewoud K. 1999. Occurrence of UVA and UVB-absorbing compounds in 152 species (206 strains) of marine microalgae. Mar. Ecol. Prog. Ser. 189: 35-51. http://dx.doi.org/10.3354/meps189035

Karsten U., Bischof K., Hanelt D., Tug H., Wiencke C. 1999. The effect of UV radiation on photosynthesis and UV-absorbing substances in the endemic Arctic macroalga Develaraea ramentacea (Rhodophyta). Physiol. Plant. 105: 58-66. http://dx.doi.org/10.1034/j.1399-3054.1999.105110.x

Kirk J. 1994. Light and photosynthesis in aquatic ecosystems, Cambridge University Press, New York. Great Britain 509 pp. http://dx.doi.org/10.1017/CBO9780511623370

Klisch M., Häder D. 2002. Wavelength dependence of mycosporine-like amino acid synthesis in Gyrodinium dorsum. J. Photochem. Photobiol. B. 66(1): 60-66. http://dx.doi.org/10.1016/S1011-1344(01)00276-7

Kräbs G., Bischof K., Hanelt D., Karsten U., Wiencke C. 2002. Wavelength-dependent induction of UV-absorbing mycosporine-like amino acids in the red alga Chondrus cryspus under natural solar radiation. J. Exp. Mar. Biol. Ecol. 268: 69-82. http://dx.doi.org/10.1016/S0022-0981(01)00380-X

Kräbs G., Watanabe M., Wiencke C. 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(6): 515-519. http://dx.doi.org/10.1562/2003-12-14-RA.1

Laurion I., Blouin F., Roy S. 2003. The quantitative filter technique for measuring phytoplankton absorption: Interference by MAAs in the UV waveband. Limnol. Oceanogr. Methods 1: 1-9. http://dx.doi.org/10.4319/lom.2011.1.1

Leu E., Wängberg S.A., Wulff A., Falk-Petersen S., Ørbæk J.B., Hessen D.O. 2006. Effects of changes in ambient PAR and UV radiation on the nutritional quality of an Arctic diatom (Thalassiosira antarctica var. borealis). J. Exp. Mar. Biol. Ecol. 337: 65-81. http://dx.doi.org/10.1016/j.jembe.2006.06.005

Lubin D., Frederick J., Booth C., Lucas T., Neuschuler D. 1989. Measurement of Enhanced Springtime Ultraviolet Radiation at Palmer Station Antarctica. Geophy. Res. Lett. 16: 783-785 http://dx.doi.org/10.1029/GL016i008p00783

MacDonald T., Dubois L., Smith L., Campbell D. 2003. Sensitivity of cyanobacterial antenna, reaction centre and CO2 assimila tion transcripts and proteins to moderate UVB: Light acclimation potentials resistance to UVB. Photochem. Photobiol. 77: 405-412. http://dx.doi.org/10.1562/0031-8655(2003)077<0405:SOCARC>2.0.CO;2

Meehl G., Stocker T., Collins W., Friedlingstein P., Gaye A., Gregory J., Kitoh A., Knutti R., Murphy J., Noda A., Raper S., Watterson I., Weaver A., Zhao Z. 2007. Global climate projections. In: Solomon S., Qin D., Manning M., Chen Z., Marquis M., Averyt K.B., Tignor M., Miller H. (eds.) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press: Cambridge, United Kingdom and New York, NY, USA. http://www.ipcc.ch/pdf/assessment-report/ar4/wg1/ar4-wg1-spm.pdf (2 April 2008).

Neale P., Banaszak A., Jarriel C. 1998a. Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae) Mycosporine-like amino acids protect against inhibition of photosynthesis. J. Phycol. 34: 928-938. http://dx.doi.org/10.1046/j.1529-8817.1998.340928.x

Neale P., Davis R., Cullen J. 1998b. Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton. Nature 392: 585-589. http://dx.doi.org/10.1038/33374

Portwich A., Garcia-Pichel F. 2000. A novel prokaryotic UVB photoreceptor in the cyanobacterium Chlorogloeopsis PCC 6912. Photochem. Photobiol. 71: 493-498. http://dx.doi.org/10.1562/0031-8655(2000)071<0493:ANPUPI>2.0.CO;2

Riegger L., Robinson D. 1997. Photoinduction of UV absorbing compounds in Antarctic diatoms and Phaeocystis antarctica. Mar. Ecol. Prog. Ser. 160: 13-25. http://dx.doi.org/10.3354/meps160013

Serreze M., Holland M., Stroeve J. 2007. Perspectives on the Arctic’s Shrinking Sea-Ice Cover. Science 315: 1533-1536. http://dx.doi.org/10.1126/science.1139426 PMid:17363664

Shick J., Lesser M., Jokiel P. 1996. Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biol. 2: 527-545. http://dx.doi.org/10.1111/j.1365-2486.1996.tb00065.x

Schloss I., Ferreyra G. 2002. Primary production, light and vertical mixing in Potter Cove, a shallow bay in the maritime Antarctic. Polar Biol. 25: 41-48. http://dx.doi.org/10.1007/s003000100309

Schloss I., Ferreyra G., González O., Atencio A., Fuentes V., Tosonotto G., Mercuri D., Sahade R., Tatián M., Abele D. 2008. Long-term hydrographic conditions and climate trends in Potter Cove. Rep. Pol. Mar. Res. 571: 382-389.

Sinha R.P., Richter P., Faddoul J., Braun M., Häder, D.-P. 2002. Effects of UV and visible light on cyanobacteria at the cellular level. Photochem. Photobiol. Sci. 1: 553-559. http://dx.doi.org/10.1039/b203955a

Taira H., Fukshima M., Hohsaka T., Sisido M. 2005. Four-base codon-mediated incorporation of no natural amino acids into proteins in a eukaryotic cell-free translation system. J. Biosci. Bioeng. 99(5): 473-476. http://dx.doi.org/10.1263/jbb.99.473 PMid:16233819

Takano S., Uemura D., Hirata Y. 1979. Isolation and structure of a 334 nm UV absorbing substance, Porphyra-334 from red alga Porphyra tenera Kjellman. Chemistry Lett. 419-420. http://dx.doi.org/10.1246/cl.1979.419

Tsujino I., Yabe K., Sekikawa I. 1980. Isolation and structure of a new aminoacid, Shinorine, from the red alga Chondrus yendoi Yamada et Mikami. Bot. Mar. 23: 65-68.

Vernet M. 2000. Effects of UV radiation on the physiology and ecology of marine phytoplankton. In: de Mora S., Demers S., Vernet M. (eds.) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp. 237-278. http://dx.doi.org/10.1017/CBO9780511535444.010

Villafañe V., Helbling E., Holm-Hansen O., Chalker B. 1995. Acclimatization of Antarctic natural phytoplankton assemblages when exposed to solar ultraviolet radiation. J. Plankton Res. 17: 2295-2306. http://dx.doi.org/10.1093/plankt/17.12.2295

Villafañe V., Reid F. 1995. Métodos de microscopía para la cuantificación del fitoplancton. In: Alveal K., Olivera E. de (eds.), Manual de Métodos Ficológicos. Universidad de Concepción, Concepción, Chile, pp. 169-185.

White A., Jahnke L. 2002. Contrasting Effects of UV-A and UV-B on Photosynthesis and Photoprotection of β-carotene in two Dunaliella spp. Plant Cell Physiol. 43(8): 877-884. http://dx.doi.org/10.1093/pcp/pcf105 PMid:12198190




Copyright (c) 2012 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es