Abstract
The effects of ultraviolet radiation (UVR) on the synthesis of mycosporine-like amino acids (MAAs) in sea-ice communities and on the other UV-absorption properties of sea ice were studied in a three-week long in situ experiment in the Gulf of Finland, Baltic Sea in March 2011. The untreated snow-covered ice and two snow-free ice treatments, one exposed to wavelengths > 400 nm (PAR) and the other to full solar spectrum (PAR + UVR), were analysed for MAAs and absorption coefficients of dissolved (aCDOM) and particulate (ap) fractions, the latter being further divided into non-algal (anap) and algal (aph) components. Our results showed that the diatom and dinoflagellate dominated sea-ice algal community responded to UVR down to 25–30 cm depth by increasing their MAA?:?chlorophyll-a ratio and by extending the composition of MAA pool from shinorine and palythine to porphyra-334 and an unknown compound with absorption peaks at ca. 335 and 360 nm. MAAs were the dominant absorbing components in algae in the top 10 cm of ice, and their contribution to total absorption became even more pronounced under UVR exposure. In addition to MAAs, the high absorption by chromophoric dissolved organic matter (CDOM) and by deposited atmospheric particles provided UV-protection for sea-ice organisms in the exposed ice. Efficient UV-protection will especially be of importance under the predicted future climate conditions with more frequent snow-free conditions.
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C. Belzile, S. Demers, G. A. Ferreyra, I. Schloss, C. Nozais, K. Lacoste, B. Mostajir, S. Roy, M. Gosselin, E. Pelletier, S. M. F. Gianesella and M. Vernet, UV effects on marine planktonic food webs: a synthesis of results from mesocosm studies, Photochem. Photobiol., 2006, 82, 850–856.
T. A. Moisan, J. Goes and P. J. Neale, Mycosporine-like amino acids in phytoplankton: biochemistry, physiology and optics, in Marine Phytoplankton, ed. W. T. Kersey and S. P. Munger, Nova Science Publishers, New York, 2009, pp.119–143.
J. I. Carreto and M. O. Carignan, Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects, Mar. Drugs, 2011, 9, 387–446.
J. I. Carreto, V. A. Lutz, S. G. De Marco and M. O. Carignan, Fluence and wavelength dependence of mycosporine-like amino acid synthesis in the dinoflagellate Alexandrium excavatum, in Toxic Marine Phytoplankton, ed. E. Granel, L. Edler and D. M. Anderson, Elsevier, New York, 1990, pp.275–279.
E. W. Helbling, B. E. Chalker, W. C. Dunlap, O. Holm-Hansen and V. E. Villafañe, Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation, J. Exp. Mar. Biol. Ecol., 1996, 204, 85–101.
L. Riegger and D. Robinson, Photoinduction of UV-absorbing compounds in Antarctic diatoms and Phaeocystis antartica, Mar. Ecol.: Prog. Ser., 1997, 160, 13–25.
M. Hernando, J. I. Carreto, M. O. Carignan, G. A. Ferreyra and C. Gross, Effects of solar radiation on growth and mycosporine-like amino acids content in Thalassiosira sp., an Antarctic diatom, Polar Biol., 2002, 25, 12–20.
D. Karentz, F. S. McEuen, M. C. Land and W. C. Dunlap, Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: potential protection from ultraviolet exposure, Mar. Biol., 1991, 108, 157–166.
S. W. Jeffrey, H. S. MacTavish, W. C. Dunlap, M. Vesk and K. Groenewould, Occurrence of UVA and UVB-absorbing compounds in 152 species (206 strains) of marine microalgae, Mar. Ecol.: Prog. Ser., 1999, 189, 35–51.
I. Laurion, F. Blouin and S. Roy, The quantitative filter technique for measuring phytoplankton absorption: Interference by MAAs in the UV waveband, Limnol. Oceanogr.: Methods, 2003, 1, 1–9.
R. P. Sinha, S. P. Singh and D. P. Häder, Database on mycosporines and mycosporine-like amino acids (MAAs) in fungi, cyanobacteria, macroalgae, phytoplankton and animals, J. Photochem. Photobiol., B, 2007, 89, 29–35.
A. Oren and N. Gunde-Cimerman, Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites?, FEMS Microbiol. Lett., 2007, 269, 1–10.
K. R. Arrigo and D. N. Thomas, Large scale importance of sea ice biology in the Southern Ocean, Antarct. Sci., 2004, 16, 471–486.
D. K. Perovich, A theoretical model of ultraviolet light transmission through Antarctic sea ice, J. Geophys. Res., [Atmos.], 1993, 98, 22579–22587.
J. Uusikivi, A. V. Vähätalo, M. A. Granskog and R. Sommaruga, Contribution of mycosporine-like amino acids and colored dissolved and particulate matter to sea ice optical properties and ultraviolet attenuation, Limnol. Oceanogr., 2010, 55, 703–713.
J. Piiparinen, Fast- and drift-ice communities in the Bothnian Bay and the impact of UVA radiation on the Baltic Sea ice ecology, Ph. D. Thesis, University of Helsinki, Walter and Andrée de Nottbeck Foundation Sci. Rep., 2011, 36, available at http://hdl.handle.net/10138/26547.
J. Ehn, M. A. Granskog, A. Reinart and A. Erm, Optical properties of melting landfast sea ice and underlying seawater in Santala Bay, Gulf of Finland, J. Geophys. Res., [Atmos.], 2004, 109(C9), C090003, 10.1029/2003JC002042.
C. J. Mundy, M. Gosselin, J. K. Ehn, C. Belzile, M. Poulin, E. Alou, S. Roy, H. Hop, S. Lessard, T. N. Papakyriakou, D. G. Barber and J. Stewart, Characteristics of two distinct high-light acclimated algal communities during advanced stages of sea ice melt, Polar Biol., 2011, 34, 1869–1886.
K. G. Ryan, A. McMinn, K. A. Mitchell and L. Trenerry, Mycosporine-like amino acids in Antarctic sea ice algae, and their response to UVB radiation, Z. Naturforsch., 2002, 57, 471–477.
IPCC, Climate change 2013: The physical science basis, Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change, Cambridge Univ. Press, New York, 2013.
HELCOM, Climate change in the Baltic Sea Area: HELCOM thematic assessment in 2013, Balt. Sea Environ. Proc., 2013, 137.
K. Meiners, J. Fehling, M. A. Granskog and M. Spindler, Abundance, biomass and composition of biota in Baltic sea ice and underlying water (March 2000), Polar Biol., 2002, 25, 761–770.
J. Piiparinen, H. Kuosa and J.-M. Rintala, Winter-time ecology in the Bothnian Bay, Baltic Sea: nutrients and algae in fast ice, Polar Biol., 2010, 33, 1445–1461.
J. Piiparinen and H. Kuosa, Impact of UVA radiation on algae and bacteria in Baltic Sea ice, Aquat. Microb. Ecol., 2011, 63, 75–87.
M. A. Granskog, M. Leppäranta, T. Kawamura, J. Ehn and K. Shirasawa, Seasonal development of the properties and composition of landfast sea ice in the Gulf of Finland, the Baltic Sea, J. Geophys. Res., [Atmos.], 2004, 109, C02020, 10.1029/2003JC001874.
J.-M. Rintala, J. Piiparinen, J. Blomster, M. Majaneva, S. Müller, J. Uusikivi and R. Autio, Fast direct melting of brackish sea ice samples results in biologically more accurate results than slow buffered melting, Polar Biol., 2014, 37, 1811–1822.
G. F. N. Cox and W. F. Weeks, Equations for determining the gas and brine volumes in sea ice samples, J. Glaciol., 1983, 29, 306–316.
M. Leppäranta and T. Manninen, The brine and gas content of sea ice with attention to low salinities and high temperatures, Finnish Institute of Marine Research Internal Report, 1988, 2.
H. Utermöhl, Zur Vervollkommnung der quantitativen Phytoplankton-Methodik, Mitt.–Int. Ver. Theor. Angew. Limnol., 1958, 9, 1–38.
B. Tartarotti and R. Sommaruga, The effect of different methanol concentrations and temperatures on the extraction of mycosporine-like amino acids (MAAs) in algae and zooplankton, Arch. Hydrobiol., 2002, 154, 691–703.
R. P. Sinha, M. Klisch, A. Gröniger and D.-P. Häder, Mycosporine-like amino acids in the marine red alga Gracilaria cornea–effects of UV and heat, Environ. Exp. Bot., 2000, 43, 33–43.
K. Whitehead and J. I. Hedges, Photodegradation and photosensitization of mycosporine-like amino acids, J. Photochem. Photobiol., B, 2005, 80, 115–121.
R. P. Rastogi and A. Incharoensakdi, UV radiation-induced biosynthesis, stability and antioxidant activity of mycosporine-like amino acids (MAAs) in a unicellular cyanobacterium Gloeocapsa sp. CU2556, J. Photochem. Photobiol., B, 2014, 130, 287–292.
S. Takano, D. Uemura and Y. Hirata, Isolation and structure of two new amino acids, palythinol and palythene, from the zoanthid Palythoa tuberculosa, Tetrahedron Lett., 1978, 49, 4909–4912.
S. Takano, D. Nakanashi, D. Uemura and Y. Hirata, Isolation and structure of a 334 nm UV-absorbing substance, Porphyra-334 from the red alga Porphyra tenera Kjellman, Chem. Lett., 1979, 419–420.
I. Tsujino, K. Yabe and I. Sekikawa, Isolation and structure of a new amino acid, shinorine, from the red alga Chondrus yendoi, Yamada et Mikami, Bot. Mar., 1980, 23, 65–68.
J. I. Carreto, M. O. Carignan and N. G. Montoya, Comparative studies on mycosporine-like amino acids, paralytic shellfish toxins and pigment profiles of the toxic dinoflagellates Alexandrium tamarense, A. catenella and A. minutum, Mar. Ecol.: Prog. Ser., 2001, 223, 49–60.
G. M. Ferrari and S. Tassan, A method using chemical oxidation to remove light absorption by phytoplankton pigments, J. Phycol., 1999, 35, 1090–1098.
S. Tassan and G. M. Ferrari, A sensitivity analysis of the ‘Transmittance–Reflectance’ method for measuring light absorption by aquatic particles, J. Plankton Res., 2002, 24, 757–774.
S. Tassan and G. M. Ferrari, An alternative approach to absorption measurements of aquatic particles retained on filters, Limnol. Oceanogr., 1995, 40, 1358–1368.
T. C. Grenfell and D. K. Perovich, Radiation absorption coefficients of polycrystalline ice from 400–1400 nm, J. Geophys. Res., [Atmos.], 1981, 86(C8), 7447–7450.
R. C. Smith and K. S. Baker, Optical properties of the clearest natural waters (200–800 nm), Appl. Opt., 1981, 20, 177–184.
D. K. Perovich and J. W. Govoni, Absorption coefficients of ice from 250 to 400 nm, Geophys. Res. Lett., 1991, 18, 1233–1235.
J. Uusikivi, On optical and physical properties of sea ice in the Baltic Sea, Ph. D. Thesis, University of Helsinki, Rep. Ser. Geophys.,2013, 73, available at http://hdl.handle.net/10138/39668..
T. C. Grenfell and G. A. Maykut, The optical properties of ice and snow in the Arctic basin, J. Glaciol., 1977, 18, 445–463.
J. M. Shick and W. C. Dunlap, Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms, Annu. Rev. Physiol., 2002, 64, 223–262.
I. Laurion, A. Lami and R. Sommaruga, Distribution of mycosporine-like amino acids and photoprotective carotenoids among freshwater phytoplankton assemblages, Aquat. Microb. Ecol., 2002, 26, 283–294.
B. Tartarotti and R. Sommaruga, Seasonal and ontogenetic changes of mycosporine-like amino acids in planktonic organisms from an alpine lake, Limnol. Oceanogr., 2006, 51, 1530–1541.
K. Oubelkheir, L. A. Clementson, G. F. Moore and G. H. Tilstone, Production of mycosporine-like amino acids by phytoplankton under ultraviolet radiation exposure in the Sub-Antarctic Zone south of Tasmania, Mar. Ecol.: Prog. Ser., 2013, 494, 41–63.
G. Hällfors, Checklist of Baltic Sea phytoplankton species, Balt. Sea Environ. Proc., 2004, 95.
F. Rindi, Diversity, distribution and ecology of green algae and cyanobacteria in urban habitats, in Algae and Cyanobacteria in Extreme Environments, ed. J. Seckbach, Springer, AA Dordrecht, 2007, pp.619–638.
C. Kitzing, T. Pröschold and U. Karsten, UV-induced effects on growth, photosynthetic performance and sunscreen contents in different populations of the green alga Klebsormidium fluitans (Streptophyta) from alpine soil crusts, Microb. Ecol., 2014, 67, 327–340.
J. I. Carreto, M. O. Carignan and N. G. Montoya, A high-resolution reverse-phase liquid chromatography method for the analysis of mycosporine-like amino acids (MAAs) in marine organisms, Mar. Biol., 2005, 146, 237–252.
E. Ingalls, K. Whitehead and M. C. Bridouxa, Tinted windows: The presence of the UV absorbing compounds called mycosporine-like amino acids embedded in the frustules of marine diatoms, Geochim. Cosmochim. Acta, 2010, 74, 104–115.
B. Sulzberger and E. Durisch-Kaiser, Chemical characterization of dissolved organic matter (DOM): A prerequisite for understanding UV-induced changes of DOM absorption properties and bioavailability, Aquat. Sci., 2009, 71, 104–126.
K. Whitehead and M. Vernet, Influence of mycosporine-like amino acids (MAAs) on UV absorption by particulate and dissolved organic matter in La Jolla Bay, Limnol. Oceanogr., 2000, 45, 1788–1796.
O. Järvinen and M. Leppäranta, Transmission of solar radiation through the snow cover on floating ice, J. Glaciol., 2011, 57, 861–870.
S. J. Doherty, S. G. Warren, T. C. Grenfell, A. D. Clarke and R. E. Brandt, Light-absorbing impurities in Arctic snow, Atmos. Chem. Phys., 2010, 10, 11647–11680.
N. Sokolik and O. B. Toon, Incorporation of mineralogical composition into models of the radiative properties of mineral aerosol from UV to IR wavelengths, J. Geophys. Res., [Atmos.], 1999, 104, 9423–9444.
M. Yang, S. G. Howell, J. Zhuang and B. J. Huebert, Attribution of aerosol light absorption to black carbon, brown carbon, and dust in China - interpretations of atmospheric measurements during EAST-AIRE, Atmos. Chem. Phys., 2009, 9, 2035–2050.
A.-P. Hyvärinen, P. Kolmonen, V.-M. Kerminen, A. Virkkula, A. Leskinen, M. Komppula, J. Hatakka, J. Burkhart, A. Stohl, P. Aalto, M. Kulmala, K. Lehtinen, Y. Viisanen and H. Lihavainen, Aerosol black carbon at five background measurement sites over Finland, a gateway to the Arctic, Atmos. Environ., 2011, 45, 4042–4050.
I. Hienola, J. P. Pietikäinen, D. Jacob, R. Pozdun, T. Petäjä, A. P. Hyvärinen, L. Sogacheva, V.-M. Kerminen, M. Kulmala and A. Laaksonen, Black carbon concentration and deposition estimations in Finland by the regional aerosol–climate model REMO-HAM, Atmos. Chem. Phys., 2013, 13, 4033–4055.
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Piiparinen, J., Enberg, S., Rintala, JM. et al. The contribution of mycosporine-like amino acids, chromophoric dissolved organic matter and particles to the UV protection of sea-ice organisms in the Baltic Sea. Photochem Photobiol Sci 14, 1025–1038 (2015). https://doi.org/10.1039/c4pp00342j
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DOI: https://doi.org/10.1039/c4pp00342j