Abstract
The UV-susceptibility of zoospores of the lower sublittoral kelp Laminaria digitata was studied in the laboratory under varying fluence of spectral irradiance consisting of photosynthetically active radiation (PAR, 400–700 nm; = P), PAR + UV-A radiation (UV-A, 320–400 nm; = PA), and PAR + UV-A + UV-B radiation (UV-B, 280–320 nm; = PAB). In vivo absorption of phlorotannin, localisation of phlorotannin-containing physodes, structural changes, DNA damage and repair, photosynthesis and germination of zoospores were measured after exposure treatments and after 2–6 days of recovery in dim white light. Photodegradation of phlorotannins was observed after extended exposure to ultraviolet radiation (UVR). The UV-protective function of extra- and intracellular phlorotannins was, therefore, observed only after 8 h, but not after 16-h UVR exposure. The energetic cost of photoprotection may have caused the delay in ontogenic development of zoospores after 8-h exposure to PA and PAB treatment; longer exposure time corresponding to 16-h PA and PAB treatment eventually lead to cell degeneration at 6 days post-cultivation. The formation of cyclobutane–pyrimidine dimers (CPDs), as indicator of DNA damage, was not blocked by the UV-absorbing phlorotannins during the 16-h PAB exposure and the inability for DNA damage repair was likely responsible for low photosynthetic recovery and spore mortality. The higher sensitivity of L. digitata zoospores to UVR compared to other kelps such as Saccorhiza dermatodea and Alaria esculenta confirmed our hypothesis that the depth distribution of adult sporophytes in the field correlates to the sensitivity of their corresponding early life history stages to different stress factors in general and UVR in particular.
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References
Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91
Arnold TM, Targett NM (2003) To grow and defend: lack of tradeoffs for brown algal phlorotannins. Oikos 100:406–408
Clayton MN (1992) Propagules of marine macroalgae: structure and development. Br Phycol J 27:219–232
Clayton MN, Ashburner CM (1994) Secretion of phenolic bodies following fertilisation in Durvillaea potatorum (Durvillaeales, Phaeophyta). Eur J Phycol 29:1–9
Dring MJ, Makarov V, Schoschina E, Lorenz M, Lüning K (1996) Influence of ultraviolet-radiation on chlorophyll fluorescence and growth in different life-history stages of three species of Laminaria (Phaeophyta). Mar Biol 126:183–191
Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717
Hanelt D, Tüg H, Bischof K, Groß C, Lippert H, Sawall T, Wiencke C (2001) Light regime in an arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Mar Biol 138:649–658
Henry BE, van Alstyne KL (2004) Effects of UV radiation on growth and phlorotannins in Fucus gardneri (Phaeophyceae) juveniles and embryos. J Phycol 40:527–533
Huovinen PS, Oikari AOJ, Soimasuo MR, Cherr GN (2000) Impact of UV radiation on the early development of the giant kelp (Macrocystis pyrifera) gametophytes. Photochem Photobiol 72:308–313
Jiang H, Gao K, Helbling EW (2007) Effects of solar UV radiation on germination of conchospores and morphogenesis of sporelings in Porphyra haitanensis. Mar Biol 151:1751–1759
Karsten U, Franklin LA, Lüning K, Wiencke C (1998) 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
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
Makarov MV, Voskoboinikov GM (2001) The influence of ultraviolet-B radiation on spore release and growth of the kelp Laminaria saccharina. Bot Mar 44:89–94
Müller R, Wiencke C, Bischof K, Krock B (2009) Zoospores of three Arctic Laminariales under different UV radiation and temperature conditions: exceptional spectral absorbance properties and lack of phlorotannin induction. Photochem Photobiol 85:970–977
Pakker H, Beekman CAC, Breeman AM (2000) Efficient photoreactivation of UVBR-induced DNA damage in the sublittoral macroalga Rhodymenia pseudopalmata (Rhodophyta). Eur J Phycol 35:109–114
Phillips JA, Clayton MN, Harvey AS (1994) Comparative studies on sporangial distribution and structure in species of Zonaria, Lobophora and Homoeostrichus (Dictyotales, Phaeophyceae) from Australia. Eur J Phycol 29:93–101
Ragan MA, Craigie JS (1980) Quantitative studies on brown algal phenols. IV. Ultraviolet spectrophotometry of extracted polyphenols and implications for measuring dissolved organic matter in sea water. J Exp Mar Biol Ecol 46:231–239
Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. In: Round FE, Chapman DJ (eds) Progress in Phycological Research, vol 4. Biopress Ltd, Bristol, pp 129–241
Raven JA (1991) Responses of aquatic photosynthetic organisms to increased solar UVB. J Photochem Photobiol B Biol 9:239–244
Roleda MY, Wiencke C, Hanelt D, van de Poll WH, Gruber A (2005a) Sensitivity of Laminariales zoospores from Helgoland (North Sea) to ultraviolet and photosynthetically active radiation: implications for depth distribution and seasonal reproduction. Plant Cell Environ 28:466–479
Roleda MY, Hanelt D, Wiencke C (2005b) Growth kinetics related to physiological parameters in young Saccorhiza dermatodea and Alaria esculenta sporophytes exposed to UV radiation. Polar Biol 28:539–549
Roleda MY, Wiencke C, Lüder UH (2006a) Impact of ultraviolet radiation on cell structure, UV-absorbing compounds, photosynthesis, DNA damage, and germination in zoospores of Arctic Saccorhiza dermatodea. J Exp Bot 57:3847–3856
Roleda MY, Clayton MN, Wiencke C (2006b) Screening capacity of UV-absorbing compounds in spores of Arctic Laminariales. J Exp Mar Biol Ecol 338:123–133
Roleda MY, Hanelt D, Wiencke C (2006c) Exposure to ultraviolet radiation delays photosynthetic recovery in Arctic kelp zoospores. Photosynth Res 88:311–322
Roleda MY, Wiencke C, Hanelt D (2006d) Thallus morphology and optical characteristics affect growth and DNA damage by UV radiation in juvenile Arctic Laminaria sporophytes. Planta 223:407–417
Roleda MY, Wiencke C, Hanelt D, Bischof K (2007) Sensitivity of the early life stages of macroalgae from the Northern Hemisphere to ultraviolet radiation. Photochem Photobiol 83:851–862
Roleda MY, Zacher K, Wulff A, Hanelt D, Wiencke C (2008) Susceptibility of spores of different ploidy levels from Antarctic Gigartina skottsbergii (Gigartinales, Rhodophyta) to ultraviolet radiation. Phycologia 47:361–370
Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125–139
Schoenwaelder MEA, Wiencke C (2000) Phenolic compounds in the embryo development of several of several northern hemisphere fucoids. Plant Biol 2:24–33
Schoenwaelder MEA, Wiencke C, Clayton MN, Glombitza KW (2003) The effect of elevated UV radiation on Fucus spp. (Fucales, Phaeophyta) zygote and embryo development. Plant Biol 5:366–377
Setlow RB (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc Natl Acad Sci USA 71:3363–3366
Sobrino C, Ward ML, Neale PJ (2008) Acclimation to elevated CO2 and ultraviolet radiation in the diatom Thalassiosira pseudonana: Effects on growth, photosynthesis and spectral sensitivity of photoinhibition. Limnol Oceanogr 56:494–505
Steinhoff FS, Wiencke C, Müller R, Bischof K (2008) Effects of ultraviolet radiation and temperature on the ultrastructure of zoospores of the brown macroalga Laminaria hyperborea. Plant Biol 10:388–397
Swanson AK, Druehl LD (2000) Differential meiospore size and tolerance of ultraviolet light stress within and among kelp species along a depth gradient. Mar Biol 136:657–664
Swanson AK, Druehl LD (2002) Induction, exudation and the UV protective role of kelp phlorotannins. Aquat Bot 73:241–253
Tala F, Vèliz K, Gòmez I, Edding M (2007) Early life stages of the South Pacific kelps Lessonia nigrescens and Lessonia trabeculata (Laminariales, Phaeophyceae) show recovery capacity following exposure to UV radiation. Phycologia 46:467–470
van de Poll WH, Eggert A, Buma AGJ, Breeman AM (2001) Effects of UV-B-induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-related differences in UV-B tolerance. J Phycol 37:30–37
van de Poll WH, Hanelt D, Hoyer K, Buma AGJ, Breeman AM (2002a) Ultraviolet-B-induced cyclobutane–pyrimidine dimer formation and repair in Arctic marine macrophytes. Photochem Photobiol 76:493–501
van de Poll WH, Eggert A, Buma AGJ, Breeman AM (2002b) Temperature dependence of UV radiation effects in Arctic and temperate isolates of three red macrophytes. Eur J Phycol 37:59–68
Vèliz K, Edding M, Tala F, Gòmez I (2006) Effects of ultraviolet radiation on different life cycle stages of the south Pacific kelps, Lessonia nigrescens and Lessonia trabeculata (Laminariales, Phaeophyceae). Mar Biol 149:1015–1024
Wiencke C, Clayton MN, Schoenwaelder M (2004) Sensitivity and acclimation to UV radiation of zoospores from five species of Laminariales from the Arctic. Mar Biol 145:31–39
Wiencke C, Roleda MY, Gruber A, Clayton MN, Bischof K (2006) Susceptibility of zoospores to UV radiation determines upper depth distribution limit of Arctic kelps: evidence through field experiments. J Ecol 94:455–463
Wiencke C, Lüder UH, Roleda MY (2007) Impact of ultraviolet radiation on physiology and development of zoospores of the brown alga Alaria esculenta from Spitsbergen. Physiol Plant 130:601–612
Acknowledgment
We thank C. Daniel and A. Gruber for laboratory assistance, the scuba-divers of the Spitsbergen 2004 field campaign, especially M. Schwanitz for collecting fertile plant material. Moreover, we thank the International Arctic Environmental Research and Monitoring Facility at Ny Ålesund, Svalbard, for support.
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Roleda, M.Y., Lüder, U.H. & Wiencke, C. UV-susceptibility of zoospores of the brown macroalga Laminaria digitata from Spitsbergen. Polar Biol 33, 577–588 (2010). https://doi.org/10.1007/s00300-009-0733-z
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DOI: https://doi.org/10.1007/s00300-009-0733-z