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The effect of ultraviolet radiation on cellular ultrastructure and photosystem II quantum yield of Alaria esculenta (L.) Greville from Spitsbergen (Norway)

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Abstract

Large brown seaweeds (kelps) represent ecologically important habitats in coastal systems. Along the western shores of the Svalbard archipelago, the kelp Alaria esculenta forms dense stands and provides habitat to a multitude of associated organisms. At the growth site in shallow waters, kelp sporophytes can be exposed to high irradiances of harmful ultraviolet (UV-B) radiation resulting from a thinning of the stratospheric ozone layer over the Arctic. Here, we tested to what extent UV-B-induced impairment of photophysiology is accompanied by changes in the cellular ultrastructure of A. esculenta and characterizes sites of cellular damage after UV exposure. Adverse effects on cellular components mostly manifest in chloroplast thylakoid membrane integrity, which is accompanied by a decrease in maximal quantum yield of photosystem II. At the applied irradiances of UV radiation, A. esculenta is stressed to an intermediate extent confirming its adaptability to a moderately increased UV-B climate.

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References

  • Bilger W, Rolland M, Nybakken L (2007) UV screening in higher plants induced by low temperature in the absence of UV-B radiation. Photochem Photobiol Sci 6:190–195

    Article  CAS  PubMed  Google Scholar 

  • Bischof K, Hanelt D, Tüg H, Karsten U, Brouwer PEM, Wiencke C (1998) Acclimation of brown algal photosynthesis to ultraviolet radiation in Arctic coastal waters (Spitsbergen, Norway). Polar Biol 20:388–395

    Article  Google Scholar 

  • Bischof K, Hanelt D, Wiencke C (1999) Acclimation of maximal quantum yield of photosynthesis in the brown alga Alaria esculenta under high light and UV radiation. Plant Biol 1:435–444

    Article  CAS  Google Scholar 

  • Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166

    Article  CAS  Google Scholar 

  • Björn LO, Callaghan TV, Gehrke C, Johanson U, Sonesson M (1999) Ozone depletion, ultraviolet radiation and plant life. Chemosph Global Change Sci 1:449–454

    Article  Google Scholar 

  • Caldwell MM (1971) Solar UV irradiation and the growth and development of higher plants. In: Giese AC (ed) Photophysiology, vol 6. Academic Press, New York, pp 131–177

    Chapter  Google Scholar 

  • Caldwell MM, Björn LO, Bornman JF, Flint SD, Kulandaivelu G, Teramura AH, Tevini M (1998) Effects of increased solar ultraviolet radiation on terrestrial ecosystems. Photochem Photobiol 46:40–52

    Article  CAS  Google Scholar 

  • Caldwell MM, Bornman JF, Ballaré CL, Flint SD, Kulandaivelu G (2007) Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors. Photochem Photobiol Sci 6:252–266

    Article  CAS  PubMed  Google Scholar 

  • Fagerberg WR, Dawes CJ (1977) Studies on Sargassum. II. Quantitative ultrastructural changes in differentiated stipe cells during wound regeneration and growth. Protoplasma 92:211–227

    Article  Google Scholar 

  • Fredersdorf J, Müller R, Becker S, Wiencke C, Bischof K (2009) Interactive effects of radiation, temperature and salinity on different life history stages of the Arctic kelp Alaria esculenta (Phaeophyceae). Oecologia 160:483–492

    Article  PubMed  Google Scholar 

  • Fredriksen S, Bartsch I, Wiencke C (2014) New additions to the benthic marine flora of Kongsfjord, western Svalbard, and comparison between 1996/1998 and 2012/2013. Bot Mar 57:203–216

    Article  Google Scholar 

  • Hanelt D, Melchersmann B, Wiencke C, Nultsch W (1997) Effects of high light stress on photosynthesis of polar macroalgae in relation to depth distribution. Mar Ecol Prog Ser 149:255–266

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Holzinger A, Lütz C (2006) Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron 37:190–207

    Article  PubMed  Google Scholar 

  • Holzinger A, Lütz C, Karsten U, Wiencke C (2004) The effect of ultraviolet radiation on ultrastructure and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia dentata from Arctic waters. Plant Biol 6:568–577

    Article  CAS  PubMed  Google Scholar 

  • Holzinger A, Karsten U, Lütz C, Wiencke C (2006) Ultrastructure and photosynthesis in the supralittoral green macroalga Prasiola Crispa (Lightfoot) Kützing from Spitsbergen (Norway) under UV exposure. Phycologia 45:168–177

    Article  Google Scholar 

  • Holzinger A, Di Piazza L, Lütz C, Roleda MY (2011) Sporogenic and vegetative tissues of Saccharina latissima (Laminariales, Phaeophyceae) exhibit distinctive sensitivity to experimentally enhanced ultraviolet radiation: photosynthetically active radiation ratio. Phycol Res 59:221–235

    Article  Google Scholar 

  • Hop H, Wiencke C, Vögele B, Kovaltchouk N (2012) Species composition, zonation, and biomass of marine benthic macroalgae in Kongsfjord, Svalbard. Bot Mar 55:399–414

    Article  Google Scholar 

  • Karsten U, Bischof K, Hanelt D, Tüg H, Wiencke C (1999) The effect of ultraviolet radiation on photosynthesis and ultraviolet-absorbing substances in the endemic Arctic macroalga Devaleraea ramentacea (Rhodophyta). Physiol Plant 105:58–66

    Article  CAS  Google Scholar 

  • Lüder UH, Clayton MN (2004) Induction of phlorotannins in the brown macroalga Ecklonia radiata (Laminariales, Phaeophyta) in response to simulated herbivory—the first microscopic study. Planta 218:928–937

    Article  PubMed  Google Scholar 

  • Lütz C (ed) (2012) Plants in alpine regions. Cell physiology of adaptation and survival strategies. Springer, Berlin

    Google Scholar 

  • Lütz C, Seidlitz H (2012) Physiological and ultrastructural changes in alpine plants exposed to high UV and to high ozone. In: Lütz C (ed) Plants in alpine regions: cell physiology of adaptation and survival strategies. Springer, Berlin, pp 29–42

    Chapter  Google Scholar 

  • Lütz C, Seidlitz HK, Meindl U (1997) Physiological and structural changes in the chloroplast of the green alga Micrasterias denticulata induced by UV-B simulation. Plant Ecol 128:54–64

    Article  Google Scholar 

  • Manney GL, Santee ML, Rex M, Livesey NJ, Pitts MC (2011) Unprecedented Arctic ozone loss in 2011. Nature 478:469–475

    Article  CAS  PubMed  Google Scholar 

  • Meindl U, Lütz C (1996) Effects of UV irradiation on cell development and ultrastructure of the green alga Micrasterias. J Photochem Photobiol 36:285–292

    Article  CAS  Google Scholar 

  • Müller R, Wiencke C, Bischof K (2008) Interactive effects of UV radiation and temperature on microstages of Laminariales (Phaeophyceae) from the Arctic and North Sea. Clim Res 37:203–213

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Oppeneiger C (2008) Einfluß von klimatischen Faktoren auf den Primär- und Sekundärstoffwechsel von Dryas octopetala L. Ph. D. Thesis, Lab Prof. Lütz, Univ. Innsbruck, Austria

  • Poppe F, Hanelt D, Wiencke C (2002) Changes in ultrastructure, photosynthetic activity and pigments in the Antarctic Red Alga Palmaria decipiens during acclimation to UV Radiation. Bot Mar 45:253–261

    Article  CAS  Google Scholar 

  • Poppe F, Schmidt RAM, Hanelt D, Wiencke C (2003) Effects of UV radiation on the ultrastructure of several red algae. Phycol Res 51:11–19

    Google Scholar 

  • Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:129–241

    CAS  Google Scholar 

  • Remias D, Albert A, Lütz C (2010) Effects of realistically simulated, elevated UV irradiation on photosynthesis and pigment composition of the alpine snow alga Chlamydomonas nivalis and the arctic soil alga Tetracystis sp. (Chlorophyceae). Photosynthetica 48:269–277

    Article  CAS  Google Scholar 

  • Rex M, Salawitch RJ, von der Gathen P, Harris NRP, Chipperfield MP, Naujokat B (2004) Arctic ozone loss and climate change. Geophys Res Let. doi:10.1029/2003GL018844

    Google Scholar 

  • Roleda MY, Hanelt D, Wiencke C (2005) Growth kinetics related to physiological parameters in young Saccorhiza dermatodea and Alaria esculenta sporophytes exposed to UV radiation. Polar Biol 28:539–549

    Article  Google Scholar 

  • Roleda MY, Wiencke C, Lüder UA (2006) 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rozema J, Boelen P, Blokker P (2005) Depletion of stratospheric ozone over the Antarctic and Arctic: responses of plants of polar terrestrial ecosystems to enhanced UV-B, an overview. Environ Pollut 137:428–442

    Article  CAS  PubMed  Google Scholar 

  • Schmidt ÉC, Scariot LA, Rover T, Bouzon ZL (2009) Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure. Micron 40:860–869

    Article  CAS  PubMed  Google Scholar 

  • Schmitz K, Srivastava LM (1974) Fine structure and development of sieve tubes in Laminaria groenlandica Rosenv. Cytobiologie 10:66–87

    Google Scholar 

  • Schoenwaelder MEA, Clayton MN (1998) Secretion of phenolic substances into the zygote wall and cell plate in embryos of Hormosira and Acrocarpia (Fucales, Pheophyceae). J Phycol 34:969–980

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. Ecol Stud 100:49–70

  • Shibata T, Kawaguchi S, Ham Y, Inagaki M, Yamaguchi K, Nakamura T (2004) Local and chemical distribution of phlorotannins in brown algae. J Appl Phycol 16:291–296

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. Freeman, New York

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vass I (1997) Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In: Pessarakli M (ed) Handbook of Photosynthesis. Dekker, New York, pp 931–949

    Google Scholar 

  • Wiencke C, Gómez I, Pakker H, Flores-Moya A, Altamirano M, Hanelt D, Bischof K, Figueroa FL (2000) Impact of UV radiation on viability, photosynthetic characteristics and DNA of brown algal zoospores: implications for depth zonation. Mar Ecol Prog Ser 197:217–229

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Christian Wiencke for his invaluable contribution to seaweed research in Kongsfjorden. We are also grateful to the continuous support by the AWIPEV station personnel and the AWI scientific diving team, in particular to Max Schwanitz. We also thank A. Holzinger and D. Remias for support during sampling and TEM analyses.

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Authors and Affiliations

  1. Institute of Botany, University of Innsbruck, Sternwartestrasse 15, 6020, Innsbruck, Austria

    C. Lütz & L. Di Piazza

  2. Marine Botany, University of Bremen, Leobener Str. NW2, 28359, Bremen, Germany

    J. Fredersdorf & K. Bischof

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  1. C. Lütz
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  2. L. Di Piazza
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  3. J. Fredersdorf
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  4. K. Bischof
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Correspondence to C. Lütz.

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This article belongs to the special issue on the “Kongsfjorden ecosystem—new views after more than a decade of research”, coordinated by Christian Wiencke and Haakon Hop.

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Lütz, C., Di Piazza, L., Fredersdorf, J. et al. The effect of ultraviolet radiation on cellular ultrastructure and photosystem II quantum yield of Alaria esculenta (L.) Greville from Spitsbergen (Norway). Polar Biol 39, 1957–1966 (2016). https://doi.org/10.1007/s00300-015-1659-2

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  • DOI: https://doi.org/10.1007/s00300-015-1659-2

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