Advertisement

Protoplasma

, Volume 243, Issue 1–4, pp 105–116 | Cite as

Physiological, biochemical, and ultrastructural responses of the green macroalga Urospora penicilliformis from Arctic Spitsbergen to UV radiation

  • Michael Y. RoledaEmail author
  • Ursula Lütz-Meindl
  • Christian Wiencke
  • Cornelius Lütz
Original Article

Abstract

Exposure of the filamentous turf green alga Urospora penicilliformis to ambient and artificial ultraviolet radiation (UVR) revealed a considerable resilient species. This explains the ability of this alga to thrive in the middle–upper intertidal zones of the Arctic sea where it is periodically exposed to environmental extremes. A transient UVR effect on photosynthesis under photosynthetically active radiation (PAR) + UV-A and PAR + UV-A + UV-B was found, but dynamic recovery of photoinhibition was observed immediately after reduction of the photon fluence rate of PAR in the absence or presence of background UVR under laboratory and natural solar radiation, respectively. Chlorophylls, carotenoids, and xanthophyll cycle pigments (violaxanthin, antheraxanthin, and zeaxanthin) concentrations were not significantly different between freshly collected samples and filaments exposed to additional laboratory radiation treatment. The ultrastructure of the U. penicilliformis gametophytes showed that the cells are well adapted to UVR. No significant ultrastructural alterations were observed in filaments exposed to different spectral irradiance in the laboratory compared to in situ acclimated specimen. The antioxidant α-tocopherol was detected in minute quantity while the search for flavonoid-like compounds was negative. Other UV screening strategies or certain genetically fixed physiological protective mechanism could be operating in this species responsible for their occurrence in higher shoreline and ecological success. Further molecular and biochemical studies are needed to elucidate the stress resistance in this turf alga. There is an indication that the extremely thick cell wall of U. penicilliformis gametophytes covered with mucilage sheath and dense layer of mineral depositions may provide a shield against unfavorable environmental conditions in general and against UVR in particular.

Keywords

α-Tocopherol Carotenoids Cell wall mineral deposition Chlorophyll PE curve Photosynthesis Ultrastructure Xanthophyll cycle pigments 

Notes

Acknowledgments

This study is supported by the AWI and performed at the International Arctic Environmental Research and Monitoring Facility at Ny Ålesund, Svalbard. We thank Mrs. Maria Blassnigg for expert technical assistance with the HPLC analyses, Ancuela Andosch for preparing the ultrathin sections, and the ARCFAC 026129-50 project support to C.L. and U. L.-M. to work in Ny-Ålesund.

References

  1. Altamirano M, Flores-Moya A, Figueroa F-L (2000) Long-term effects of natural sunlight under various ultraviolet radiation conditions on growth and photosynthesis of intertidal Ulva rigida (Chlorophyceae) cultivated in situ. Bot Mar 43:119–126. doi: 10.1515/BOT.2000.012 CrossRefGoogle Scholar
  2. Barber J, Andersson B (1992) Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem Sci 17:61–66. doi: S1011-1344(98)/0968-0004(92) 90503-2 CrossRefPubMedGoogle Scholar
  3. Beach KS, Smith CM (1996a) Ecophysiology of tropical rhodophytes. 1. Microscale acclimation in pigmentation. J Phycol 32:701–710. doi: 10.1111/j.0022-3646.1996.00701.x CrossRefGoogle Scholar
  4. Beach KS, Smith CM (1996b) Ecophysiology of tropical rhodophytes. 2. Microscale acclimation in photosynthesis. J Phycol 32:710–718. doi: 10.1111/j.0022-3646.1996.00710.x CrossRefGoogle Scholar
  5. Bilger W, Johnsen T, Schreiber U (2001) UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants. J Exp Bot 52:2007–2014. doi: 10.1093/jexbot/52.363.2007 CrossRefPubMedGoogle Scholar
  6. Bischoff B, Wiencke C (1995) Temperature adaption in strains of the amphi-equatorial green alga Urospora penicilliformis (Acrosiphoniales) biogeographical implications. Mar Biol (Berl) 122:681–688. doi: 10.1007/BF00350690 CrossRefGoogle Scholar
  7. Bischof K, Kräbs G, Wiencke C, Hanelt D (2002a) Solar ultraviolet radiation affects the activity of ribulose-1, 5-biphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215:502–509. doi: 10.1007/s00425-002-0774-9 CrossRefPubMedGoogle Scholar
  8. Bischof K, Peralta G, Kräbs G, van de Poll WH, Perez-Llorens JL, Breeman AM (2002b) Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. J Exp Bot 53:2411–2421. doi: 10.1093/jxb/erf091 CrossRefPubMedGoogle Scholar
  9. Bischof K, Rautenberger R, Brey L, Pérez-Lloréns JL (2006) Physiological acclimation to gradients of solar irradiance within mats of the filamentous green macroalga Chaetomorpha linum from southern Spain. Mar Ecol Prog Ser 306:165–175. doi: 10.3354/meps306165 CrossRefGoogle Scholar
  10. Björn LO, Callaghan TV, Gehrke C, Johanson U, Sonesson M (1999) Ozone depletion, ultraviolet radiation and plant life. Chemosphere, Glob Chang Sci 1:449–454. doi: S1011-1344(98)/S1465-9972(99)00038-0 CrossRefGoogle Scholar
  11. Caldwell MM, Björn LO, Bornman JF, Flint SD, Kulandaivelu G, Teramura AH, Tevini M (1998) Effects of increased solar ultraviolet radiation on terrestrial ecosystems. J Photochem Photobiol 46:40–52. doi: 10.1016/S1011-1344(98) 00184-5 CrossRefGoogle Scholar
  12. Choo KS, Snoeijs P, Pedersen M (2004) Oxidative stress tolerance in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana. J Exp Mar Biol Ecol 298:111–123. doi: 10.1016/j.jembe.2003.08.007 CrossRefGoogle Scholar
  13. Choo KS, Nilsson J, Pedersén M, Snoeijs P (2005) Photosynthesis, carbon uptake and antioxidant defence in two coexisting filamentous green algae under different stress conditions. Mar Ecol Prog Ser 292:127–138. doi: 10.3354/meps292127 CrossRefGoogle Scholar
  14. Cohen RA, Fong P (2004) Physiological response of a bloom-forming green macroalga to short-term change in salinity, nutrients, and light help explain its ecological success. Estuaries 27:209–216. doi: 10.1007/BF02803378 CrossRefGoogle Scholar
  15. Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211. doi: 10.1111/j.0022-3646.1996.00197.x CrossRefGoogle Scholar
  16. Ehling-Schulz M, Bilger W, Scherer S (1997) UV-B-induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune. J Bacteriol 179:1940–1945PubMedGoogle Scholar
  17. Fryer MJ (1992) The antioxidant effects of thylakoid vitamin-E (α-tocopherol). Plant Cell Environ 15:381–392. doi: 10.1111/j.1365-3040.1992.tb00988.x CrossRefGoogle Scholar
  18. Fukuda S, Zamakawa R, Hirai M, Kashino Y, Koike H (2008) Mechanisms to avoid photoinhibition in a desiccation-tolerant cyanobacterium, Nostoc commune. Plant Cell Physiol 49:488–492. doi: 10.1093/pcp/pcn018 CrossRefPubMedGoogle Scholar
  19. Häder DP, Figueroa FL (1997) Photoecophysiology of marine macroalgae. Photochem Photobiol 66:1–14. doi: 10.1111/j.1751-1097.1997.tb03132.x CrossRefGoogle Scholar
  20. Han Y-S, Han T (2005) UV-B induction of UV-B protection in Ulva pertusa (Chlorophyta). J Phycol 41:523–530. doi: 10.1111/j.1529-8817.2005.00072.x CrossRefGoogle Scholar
  21. Hanelt D, Roleda MY (2009) UVB radiation may ameliorate photoinhibition in specific shallow-water tropical marine macrophytes. Aquat Bot. doi: 10.1016/j.aquabot.2008.12.005
  22. Hanelt D, Tüg H, Bischof K, Groβ 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 (Berl) 138:649–658. doi: 10.1007/s002270000481 CrossRefGoogle Scholar
  23. Holzinger A, Lütz C (2006) Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron 37:190–207. doi: 10.1016/j.micron.2005.10.015 CrossRefPubMedGoogle Scholar
  24. 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. doi: 10.1055/s-2004-821003 CrossRefPubMedGoogle Scholar
  25. Holzinger A, Karsten U, Lütz C, Wiencke C (2006) Ultrastructure and photosynthesis in the supralittoral green macroalga Prasiola crispa from Spitsbergen (Norway) under UV exposure. Phycologia 45:168–177. doi: 10.2216/05-20.1 CrossRefGoogle Scholar
  26. Hunt LJH, Denny MW (2008) Desiccation protection and disruption: a trade-off for an intertidal marine alga. J Phycol 44:1164–1170. doi: 10.1111/j.1529-8817.2008.00578.x CrossRefGoogle Scholar
  27. Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547CrossRefGoogle Scholar
  28. Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol 41:1037–1043. doi: 10.1104/pp. 41.6.1037 CrossRefPubMedGoogle Scholar
  29. Jordan BR (2002) Molecular response of plant cells to UV-B stress. Funct Plant Biol 29:909–916. doi: 10.1071/FP02062 CrossRefGoogle Scholar
  30. Karsten U, Friedl T, Schumann R, Hoyer K, Lembcke S (2005) Mycosporine-like amino acids and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae (Chlorophyta). J Phycol 41:557–566. doi: 10.1111/j.1529-8817.2005.00081.x CrossRefGoogle Scholar
  31. Karsten U, Lembcke S, Schumann R (2007) The effects of ultraviolet radiation on photosynthetic performance, growth and sunscreen compounds in aeroterrestrial biofilm algae isolated from building facades. Planta 225:991–1000. doi: 10.1007/s00425-006-0406-x CrossRefPubMedGoogle Scholar
  32. Khotimchenko SV, Yakovleva IM (2004) Effect of solar irradiance on lipids of the green alga Ulva fenestrata Postels et Ruprecht. Bot Mar 47:395–401. doi: 10.1515/BOT.2004.050 CrossRefGoogle Scholar
  33. Kremb SG (2007) UV-induzierte Veränderungen der Genexpression bei marinen Makroalgen. PhD dissertation, Technische Universität München, Germany, 161 pp.Google Scholar
  34. Kreslavski VD, Carpentier R, Klimov VV, Murata N, Allakhverdiev SI (2007) Molecular mechanisms of stress resistance of the photosynthetic apparatus. Biol Membr 24:195–217Google Scholar
  35. Larkum AWD, Douglas SE, Raven JA (2003) Photosynthesis in algae. Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  36. Lokhorst GM, Trask BJ (1981) Taxonomic studies on Urospora (Acrosiphoniales, Chlorophyceae) in western Europe. Acta Bot Neerl 30:353–431Google Scholar
  37. 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 128:55–64. doi: 10.1023/A:1009754722357 CrossRefGoogle Scholar
  38. Lütz C, Blassnigg M, Remias D (2008) Different flavonoid patterns in Deschampsia antarctica and Colobanthus quitensis from the maritime Antarctic. Ber Polarforsch Meeresfrosch 571:192–199Google Scholar
  39. Meindl U, Lütz C (1996) Effects of UV irradiation on cell development and ultrastructure of the green alga Micrasterias. J Photochem Photobiol B 36:285–292. doi: 10.1016/S1011-1344(96) 07395-2 CrossRefGoogle Scholar
  40. Melis A (1999) Photosystem-II damage and repair cycle in chloroplast: what modulates the rate of photodamge in vivo? Trends Plant Sci 4:130–135. doi: 10.1016/S1360-1385(99) 01387-4 CrossRefPubMedGoogle Scholar
  41. Nybakken L, Bilger W, Johanson U, Björn LO, Zielke M, Solheim B (2004) Epidermal UV-screening in vascular plants from Svalbard (Norwegian Arctic). Polar Biol 27:383–390. doi: 10.1007/s00300-004-0602-8 CrossRefGoogle Scholar
  42. Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plant. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis from the molecular mechanisms to the field. BIOS Scientific, Oxford, pp 1–24Google Scholar
  43. Palozza P, Krinsky NI (1992) β-Carotene and α-tocopherol are synergistic antioxidants. Arch Biochem Biophys 297:184–187. doi: 10.1016/0003-9861(92) 90658-J CrossRefPubMedGoogle Scholar
  44. Pérez-Rodríguez E, Aguilera J, Gómez I, Figueroa F-L (2001) Excretion of coumarins by the Mediterranean green alga Dasycladus vermicularis in response to environmental stress. Mar Biol (Berl) 139:633–639. doi: 10.1007/s002270100588 CrossRefGoogle Scholar
  45. 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. doi: 10.1515/BOT.2002.024 CrossRefGoogle Scholar
  46. Poppe F, Schmidt RAM, Hanelt D, Wiencke C (2003) Effects of UV radiation on the ultrastructure of several red algae. Phycol Res 51:11–19Google Scholar
  47. Remias D, Lütz-Meindl U, Lütz C (2005) Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur J Phycol 40:259–268. doi: 10.1080/09670260500202148 CrossRefGoogle Scholar
  48. Roleda MY, Hanelt D, Wiencke C (2006) Exposure to ultraviolet radiation delays photosynthetic recovery in Arctic kelp zoospores. Photosynth Res 88:311–322. doi: 10.1007/s11120-006-9055-y CrossRefPubMedGoogle Scholar
  49. 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 83:851–862PubMedGoogle Scholar
  50. Roleda MY, Mohlin M, Pattanaik B, Wulff A (2008) Photosynthetic response of Nodularia spumigena to UV and photosynthetically active radiation depends on nutrient (N and P) availability. FEMS Microbiol Ecol 66:230–242. doi: 10.1111/j.1574-6941.2008.00572.x CrossRefPubMedGoogle Scholar
  51. Roleda MY, Campana G, Wiencke C, Hanelt D, Quartino ML, Wulff A (2009) Sensitivity of Antarctic Urospora penicilliformis (Ulotrichales, Chlorophyta) to ultraviolet radiation is life stage dependent. J Phycol 45:xxx–xxx (in press)Google Scholar
  52. Rozema J, van de Staaij J, Björn LO, Caldwell M (1997) UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol Evol 12:22–28. doi: 10.1016/S0169-5347(96) 10062-8 CrossRefGoogle Scholar
  53. Sicora C, Máté Z, Vass I (2003) The interaction of visible and UV-B light during photodamage and repair of photosystem II. Photosynth Res 75:127–137. doi: 10.1023/A:1022852631339 CrossRefPubMedGoogle Scholar
  54. 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. doi: 10.1111/j.1438-8677.2008.00049.x CrossRefPubMedGoogle Scholar
  55. Xiong F (2001) Evidence that UV-B tolerance of the photosynthetic apparatus in microalgae is related to the D1-turnover mediated repair cycle in vivo. J Plant Physiol 158:285–294. doi: 10.1078/0176-1617-00306 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Michael Y. Roleda
    • 1
    Email author
  • Ursula Lütz-Meindl
    • 2
  • Christian Wiencke
    • 3
  • Cornelius Lütz
    • 4
  1. 1.Institute for Polar EcologyUniversity of KielKielGermany
  2. 2.Plant Physiology Division, Cell Biology DepartmentUniversity of SalzburgSalzburgAustria
  3. 3.Section Functional Ecology, Department Seaweed BiologyAlfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany
  4. 4.Department Physiology and Cell Physiology of Alpine Plants, Institute of BotanyUniversity of InnsbruckInnsbruckAustria

Personalised recommendations