Marine Biology

, 165:132 | Cite as

Compensation of lack of UV screening by cellular tolerance in green macroalgae (Ulvophyceae) from the upper eulittoral

  • Frauke PescheckEmail author
  • Wolfgang Bilger
Original paper


Living side by side in the upper eulittoral of the Baltic different species of green macroalgae can be assumed to require similar resistance against solar ultraviolet-B radiation (UVB, 280–315 nm). Avoidance of UVB absorption by UV-screening pigments acts as a fundamental UVB resistance mechanism in the majority of phototrophs, including green macroalgae from the order Cladophorales. Contrastingly, other orders of green macroalgae, like the Ulvales, Ulotrichales, or Bryopsidales, lack UV screening. Field grown thalli of coexisting species representative for all four orders were exposed to experimental UVB radiation and photosystem II (PSII) and DNA damage and its repair were assessed. UV-screening Cladophora sp. showed only half as much UVB-induced damage in comparison with the non-screening species Acrosiphonia sp., Bryopsis hypnoides, and Ulva intestinalis. However, intrinsic UVB sensitivity of PSII and DNA was very similar in all species. We hypothesized that the non-screening species would compensate the lack of protection by increased repair rates. UVA-driven CPD removal was more than twice as fast in non-UV screening as in screening species. Recovery of PSII was very efficient in Acrosiphonia sp. and U. intestinalis but not in B. hypnoides or Cladophora sp.. We conclude that DNA and PSII repair are important cellular tolerance mechanisms which compensate for the lack of UV-screening compounds in the green macroalgae Acrosiphonia sp. and U. intestinalis. Bryopsis hypnoides turned out to be more sensitive than the other species and may avoid UVB damage by growing in greater depth.



Many thanks go to Susanne Wolf for skilled help with DNA extraction. Karin Krupinska is thankfully acknowledged for the opportunity to use a dark room. We thank the reviewers for their valuable comments.

Compliance with ethical standards

Ethical standards

We hereby declare that all applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

227_2018_3393_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 12 kb)


  1. Aguilera J, Karsten U, Lippert H, Vogele B, Philipp E, Hanelt D, Wiencke C (1999) Effects of solar radiation on growth, photosynthesis and respiration of marine macroalgae from the Arctic. Mar Ecol Prog Ser 191:109–119CrossRefGoogle Scholar
  2. Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage—repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta Bioenerg 1657:23–32. CrossRefGoogle Scholar
  3. Altamirano M, Flores-Moya A, Figueroa FL (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 43:119–126CrossRefGoogle Scholar
  4. Aro E, McCaffery S, Anderson J (1994) Recovery from photoinhibition in Peas (Pisum sativum L) acclimated to varying growth irradiances—role of D1 protein-turnover. Plant Physiol 104:1033–1041. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Biever JJ, Gardner G (2016) The relationship between multiple UV-B perception mechanisms and DNA repair pathways in plants. Environ Exp Bot 124:89–99. CrossRefGoogle Scholar
  6. Bischof K, Hanelt D, Wiencke C (1998) UV-radiation can affect depth-zonation of Antarctic macroalgae. Mar Biol 131:597–605CrossRefGoogle Scholar
  7. Bischof K, Hanelt D, Wiencke C (2000) Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta 211:555–562CrossRefPubMedGoogle Scholar
  8. Bischof K, Peralta G, Kräbs G, van de Poll WH, Pérez-Lloréns JL, Breeman AM (2002a) Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. J Exp Bot 53:2411–2421CrossRefPubMedGoogle Scholar
  9. Bischof K, Kräbs G, Wiencke C, Hanelt D (2002b) Solar ultraviolet radiation affects the activity of ribulose-1,5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215:502–509CrossRefPubMedGoogle Scholar
  10. Bischof K, Janknegt PJ, Buma AGJ, Rijstenbil JW, Peralta G, Breeman AM (2003) Oxidative stress and enzymatic scavenging of superoxide radicals induced by solar UV-B radiation in Ulva canopies from southern Spain. Sci Mar 67:353–359CrossRefGoogle Scholar
  11. Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda M, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166CrossRefGoogle Scholar
  12. Britt AB (2004) Repair of DNA damage induced by solar UV. Photosynth Res 81:105–112CrossRefGoogle Scholar
  13. Cadet J, Mouret S, Ravanat J-L, Douki T (2012) Photoinduced damage to cellular DNA: direct and photosensitized reactions. Photochem Photobiol 88:1048–1065. CrossRefPubMedGoogle Scholar
  14. Campbell DA, Tyystjärvi E (2012) Parameterization of photosystem II photoinactivation and repair. Biochim Biophys Acta Bioenerg 1817:258–265. CrossRefGoogle Scholar
  15. Cerovic ZG, Samson G, Morales F, Tremblay N, Moya I (1999) Ultraviolet-induced fluorescence for plant monitoring: present state and prospects. Agronomie 19:543–578. CrossRefGoogle Scholar
  16. Choo KS, Nilsson J, Pedersen M, Snoeijs P (2005) Photosynthesis, carbon uptake and antioxidant defence in two coexisting filamentous green algae under different stress conditions. Mar Ecol Prog Ser 292:127–138CrossRefGoogle Scholar
  17. Cockell CS, Knowland J (1999) Ultraviolet radiation screening compounds. Biol Rev 74:311–345CrossRefPubMedGoogle Scholar
  18. Cocquyt E, Verbruggen H, Leliaert F, De Clerck O (2010) Evolution and cytological diversification of the green seaweeds (Ulvophyceae). Mol Biol Evol 27:2052–2061CrossRefPubMedGoogle Scholar
  19. Dany A-L, Douki T, Triantaphylides C, Cadet J (2001) Repair of the main UV-induced thymine dimeric lesions within Arabidopsis thaliana DNA: evidence for the major involvement of photoreactivation pathways. J Photochem Photobiol B Biol 65:127–135. CrossRefGoogle Scholar
  20. Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211CrossRefGoogle Scholar
  21. Figueroa FL, Domínguez-González B, Korbee N (2014) Vulnerability and acclimation to increased UVB radiation in three intertidal macroalgae of different morpho-functional groups. Mar Environ Res 97:30–38. CrossRefPubMedGoogle Scholar
  22. Franklin LA, Forster RM (1997) The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32:207–232Google Scholar
  23. Ghetti F, Herrmann H, Häder DP, Seidlitz HK (1999) Spectral dependence of the inhibition of photosynthesis under simulated global radiation in the unicellular green alga Dunaliella salina. J Photochem Photobiol B Biol 48:166–173CrossRefGoogle Scholar
  24. Gocke K, Lenz J, Koppe R, Rheinheimer G, Hoppe H-G (2010) Bacterial activity and turnover rates of organic substances in the Kiel Canal. Hydrol Wasserbewirtsch 54:18–27Google Scholar
  25. Gómez I, Pérez-Rodríguez E, Vinegla B, Figueroa FL, Karsten U (1998) Effects of solar radiation on photosynthesis, UV-absorbing compounds and enzyme activities of the green alga Dasycladus vermicularis from southern Spain. J Photochem Photobiol B Biol 47(1):46–57CrossRefGoogle Scholar
  26. Goosen N, Moolenaar GF (2008) Repair of UV damage in bacteria. DNA Repair 7:353–379. CrossRefPubMedGoogle Scholar
  27. Hakala M, Tuominen I, Keranen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta Bioenerg 1706:68–80. CrossRefGoogle Scholar
  28. Halldal P (1964) Ultraviolet action spectra of photosynthesis and photosynthetic inhibition in a green and a red alga. Physiol Plant 17:414–421CrossRefGoogle Scholar
  29. He J, Chow WS (2003) The rate coefficient of repair of photosystem II after photoinactivation. Physiol Plant 118:297–304. CrossRefGoogle Scholar
  30. Hoyer K, Karsten U, Wiencke C (2002) Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar Biol 141:619–627CrossRefGoogle Scholar
  31. Huovinen P, Gómez I (2013) Photosynthetic characteristics and UV stress tolerance of Antarctic seaweeds along the depth gradient. Polar Biol 36:1319–1332. CrossRefGoogle Scholar
  32. Johansson G, Snoeijs P (2002) Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar Ecol Prog Ser 244:63–72. CrossRefGoogle Scholar
  33. Kang HS, Hidema J, Kumagai T (1998) Effects of light environment during culture on UV-induced cyclobutyl pyrimidine dimers and their photorepair in rice (Oryza sativa L.). Photochem Photobiol 68:71–77. CrossRefGoogle Scholar
  34. Karsten U, Sawall T, Hanelt D, Bischof K, Figueroa FL, Flores-Moya A, Wiencke C (1998) An inventory of UV-absorbing mycosporine-like amino acids in macroalgae from polar to warm-temperate regions. Bot Mar 41:443–453CrossRefGoogle Scholar
  35. Li N, Teranishi M, Yamaguchi H, Matsushita T, Watahiki MK, Tsuge T, Li S-S, Hidema J (2015) UV-B-induced CPD photolyase gene expression is regulated by UVR8-dependent and -independent pathways in Arabidopsis. Plant Cell Physiol. PubMedCentralCrossRefPubMedGoogle Scholar
  36. Molinier J, Lechner E, Dumbliauskas E, Genschik P (2008) Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet 4:e1000093. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46. CrossRefPubMedGoogle Scholar
  38. Pakker H, Martins RST, Boelen P, Buma AGJ, Nikaido O, Breeman AM (2000) Effects of temperature on the photoreactivation of ultraviolet-B-induced DNA damage in Palmaria palmata (Rhodophyta). J Phycol 36:334–341CrossRefGoogle Scholar
  39. Pescheck F, Bischof K, Bilger W (2010) Screening of ultraviolet-A and ultraviolet-B radiation in marine green macroalgae (Chlorophyta). J Phycol 46:444–455. CrossRefGoogle Scholar
  40. Pescheck F, Lohbeck KT, Roleda MY, Bilger W (2014) UVB-induced DNA and photosystem II damage in two intertidal green macroalgae: distinct survival strategies in UV-screening and non-screening Chlorophyta. J Photochem Photobiol B Biol 132:85–93. CrossRefGoogle Scholar
  41. Pescheck F, Campen H, Nichelmann L, Bilger W (2016) Relative sensitivity of DNA and photosystem II in Ulva intestinalis (Chlorophyta) under natural solar irradiation. Mar Ecol Prog Ser 555:95–107. CrossRefGoogle Scholar
  42. Provasoli L (1968) Media and prospects for cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Japanese Society of Plant Physiology, Tokyo, pp 47–74Google Scholar
  43. Ravanat J-L, Douki T, Cadet J (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B Biol 63:88–102CrossRefGoogle Scholar
  44. Roleda MY, Campana GL, 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 45:600–609. CrossRefPubMedGoogle Scholar
  45. Sancar A (2003) Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem Rev 103:2203–2237CrossRefPubMedGoogle Scholar
  46. Sauerbier W, Millette RL, Hackett PB Jr (1970) The effects of ultraviolet irradiation on the transcription of T4 DNA. Biochim Biophys Acta BBA Nucleic Acids Protein Synth 209:368–386. CrossRefGoogle Scholar
  47. Sfriso AA, Sfriso A (2017) In situ biomass production of Gracilariaceae and Ulva rigida: the Venice Lagoon as a study case. Bot Mar 60:271–283. CrossRefGoogle Scholar
  48. Tedetti M, Sempéré R (2006) Penetration of ultraviolet radiation in the marine environment. A review. Photochem Photobiol 82:389–397. CrossRefPubMedGoogle Scholar
  49. 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 37:30–37CrossRefGoogle Scholar
  50. van de Poll WH, Hanelt D, Hoyer K, Buma AGJ, Breeman AM (2002) Ultraviolet-B-induced cyclobutane–pyrimidine dimer formation and repair in arctic marine macrophytes. Photochem Photobiol 76:493–500CrossRefPubMedGoogle Scholar
  51. Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta Bioenerg 1817:209–217CrossRefGoogle Scholar
  52. Veit M, Bilger W, Mühlbauer T, Brummet W, Winter K (1996) Diurnal changes in flavonoids. J Plant Physiol 148:478–482CrossRefGoogle Scholar
  53. Wobbrock JO, Findlater L, Gergle D, Higgins JJ (2011) The aligned rank transform for nonparametric factorial analyses using only Anova procedures. In: Proceedings of the SIGCHI conference on human factors in computing systems. ACM, New York, NY, USA, pp 143–146Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Botanical InstituteChristian-Albrechts-University KielKielGermany

Personalised recommendations