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Effects of ultraviolet radiation on protein content, respiratory electron transport system (ETS) activity and superoxide dismutase (SOD) activity of Antarctic plankton

Polar Biology volume 30, pages 1159–1172 (2007)Cite this article

Abstract

Depletion of stratospheric ozone causes a significant increase in UV radiation in the Antarctic regions. Its effects include DNA damage, as well as impairment of photosynthesis, respiration, protein synthesis and other metabolic functions. Defence systems of cells are directed against free oxygen radicals liberated through UV radiation. One of their main components of defence systems are superoxide dismutases (SODs). The effects of ultraviolet radiation A and B (UVAR and UVBR) on protein synthesis, respiratory electron transfer (ETS) activity and superoxide dismutase (SOD) activity in Antarctic plankton were examined. Samples were taken in the Gerlache Strait (Antarctica). Three stations were situated in an area, which showed a Cryptomonas bloom. Two stations were located in areas having a bloom of green nanoflagellates. Samples were exposed for 3 h to photosynthetically active radiation (PAR), or to PAR + UVAR or to PAR + UVAR + UVBR, under fixed experimental irradiances. UVBR inhibited protein synthesis and ETS activity, and enhanced SOD activity. UVAR enhanced protein synthesis and ETS activity, and inhibited SOD activity. Samples, which had received more solar radiation prior to experiments showed less inhibition of protein synthesis by experimental UVBR, which suggests acclimation to ambient radiation. Cryptomonas-dominated stations showed less SOD activity than the green flagellate-dominated stations, which might be related to the protection conferred by their phycoerythrin.

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References

  • Aráoz R, Häder D-P (1999) Phycoerythrin synthesis is induced by solar UV-B in the cyanobacterium Nostoc. Plant Physiol Biochem 37:223–229

    Article  Google Scholar 

  • Arts M T, Rai H (1997) Effects of enhanced ultraviolet-B radiation on the production of lipid, polysaccharide and protein in three freshwater algal species. Freshw Biol 38:597–510

    Article  CAS  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arnzen ZJ (eds) Photoinhibition: topics in photosynthesis, vol 9. Elsevier, Amsterdam, pp 227–287

  • Beardall J, Burger-Wiesma T, Rijkeboer M, Sukenik A, Lemoalle J, Dubinsky Z, Fontvielle D (1994) Studies on enhanced post-illumination respiration in microalgae. J Plankton Res 16:1401–1410

    Article  Google Scholar 

  • Beardall J, Berman T, Markager S, Martínez R, Montecino V (1997) The effects of ultraviolet radiation on respiration and photosynthesis in two species of microalgae. Can Fish Aquat Sci 54:687–696

    Article  Google Scholar 

  • Behrenfeld MJ, Chapman JW, Hardy JT, Lee H (1993) Is there a common response to ultraviolet-B radiation by marine phytoplankton? Mar Ecol Prog Ser 102:59–68

    Google Scholar 

  • Behrenfeld MJ, Lean DRS, Lee HII (1995) Ultraviolet-B radiation effects on inorganic nitrogen uptake by natural assemblages of oceanic plankton. J Phycol 31:25-36

    Article  CAS  Google Scholar 

  • Britt A (1996) DNA damage and repair in plants. Ann Rev Plant Physiol Plant Mol Biol 47:75–100

    Article  CAS  Google Scholar 

  • Brosche M, Strid A (2003) Molecular events following perception of ultraviolet-B radiation by plants. Physiol Plant 117:1–10

    Article  CAS  Google Scholar 

  • Buma AGJ, Helbling WM, de Boer K, Villafañe VE (2001) Patterns of DNA damage and photoinhibition in temperate South-Atlantic picophytoplankton exposed to solar ultraviolet radiation. J Photochem Photobiol B Biol 62:9–18

    Article  CAS  Google Scholar 

  • Buma AGJ, van Oijen T, van de Poll W, Veldhuis M J W, Gieskes W W C (2000) On the high sensitivity of the marine Prymnesiophyte Emiliania Huxleyi to ultraviolet-B radiation. Phycol 36:296–303

    Article  CAS  Google Scholar 

  • Buma AJ, Zemmelink HJ, Sjollema K, Gieskes WWC (1996) UVB radiation modifies protein and photosynthetic pigment content, volume and ultrastructure of marine diatoms. Mar Ecol Prog Ser 142:47–54

    CAS  Google Scholar 

  • Butow BJ, Wynne D, Tel-Or E (1997) Antioxidative protection of Peridinium gatunense in Lake Kinneret: seasonal and daily variation. J Phycol 33:780–786

    Article  CAS  Google Scholar 

  • Carpenter RC (1985) Relationships between primary production and irradiance in coral reef algal communities. Limnol Oceanogr 30:784–793

    Google Scholar 

  • Cockell CS, Southern A, Herrera A (2000) Lack of UV radiation in Biosphere 2—practical and theoretical effects on plants. Ecol Eng 16:293–299

    Article  Google Scholar 

  • Cullen JJ, Lesser MP (1991) Inhibition of photosynthesis by ultraviolet radiation as a function of dose and dosage rate: results for a marine diatom. Mar Biol 111:183–190

    Article  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegen F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    PubMed  Article  CAS  Google Scholar 

  • Ewing JF, Janero DR (1995) Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal Biochem 232:243–248

    PubMed  Article  CAS  Google Scholar 

  • Fauchot J, Gosselin M, Levasseur M, Mostajir B, Belzile C, Demers S, Roy S, Zulema P (2000) Influence of UV-B radiation on nitrogen utilization by a natural assemblage of phytoplankton, J Phycol 36:484–496

    Article  CAS  Google Scholar 

  • Figueroa FL, Blanco JM, Jiménez-Gómez F, J Rodríguez J (1997) Effects of ultraviolet radiation on carbon fixation in Antarctic nannophytoflagellates. Photochem Photobiol 66:185–189

  • Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247:1–11

    PubMed  Article  CAS  Google Scholar 

  • Fridovich I (1997) Superoxide anion radical (O −2 ), superoxide dismutases and related matters. J Biol Chem 272:18515–18517

    PubMed  Article  CAS  Google Scholar 

  • Gerber S, Häder DP (1992) UV efects on photosynthesis, protein and pigmentation in the flagellate Euglena gracilis: biochemical and spectroscopic observations. Biochem Syst Ecol 20:485–492

    Article  CAS  Google Scholar 

  • Häder DP (1997) Effects of UV radiation on phytoplankton. Adv Microb Ecol 15:1–26

    Google Scholar 

  • Häder DP, Worrest RC (1991) Effects of enhanced solar-ultraviolet radiation on aquatic ecosystems. Photochem Photobiol 53:717–725

    Article  Google Scholar 

  • Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241

    PubMed  Article  Google Scholar 

  • He Y-Y, Häder D-P (2002) UV-B induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-l-cysteine. J Photochem Photobiol 66:115–124

    Article  CAS  Google Scholar 

  • Helsper JPFG, Ric de Vos CH, Maas FM, Jonker HH, van den Broeck HC, Jordi W, Pot CS, Keizer LCP, Schapendonk AHCM (2003) Response of selected antioxidants and pigments in tissues of Rosa hybrida and Fuchsia hybrida to supplemental UV-A exposure. Physiol Plant 117:171–178

    Article  CAS  Google Scholar 

  • Heraud Ph, Beardall J (2002) Ultraviolet radiation has no effect on respiratory oxygen consumption or enhanced post-illumination respiration in three species of microalgae. J Photochem Photobiol B Biol 68:109–116

    Article  Google Scholar 

  • Herndl GJ, Daley J, Jasper S (1993) Major role of ultraviolet-B in controlling bacterioplankton growth in the surface layer of the ocean. Nature 361:717–719

    Article  Google Scholar 

  • Jacquet S, Bratbak G (2003) Effects of ultraviolet radiation on marine virus–phytoplankton interactions. FEMS Microbiol Ecol 44:279–289

    Article  CAS  PubMed  Google Scholar 

  • Kaiser E, Herndl GJ (1997) Rapid recovery of marine bacterioplankton activity after inhibition by UV radiation in coastal waters. Appl Environ Microbiol 63:4026–4031

    PubMed  CAS  Google Scholar 

  • Karentz DJ, Cleaver E, Mitchell DL (1991) DNA damage in the Antarctic. Nature 350:28

    Article  Google Scholar 

  • Kenner RA, Ahmed SI (1975) Measurement of electron transport activities in marine plankton. Mar Biol 33:119–128

    Article  CAS  Google Scholar 

  • Korbee N, Abdala RT, Figueroa FL, Helbling EW (2004) Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from Patagonia, Argentina. J Phycol 40:248–259

    Article  CAS  Google Scholar 

  • Kumar A, Sinha RP, Häder D-P (1996) Effect of UV-B on enzymes of nitrogen metabolism in the cyanobacterium Nostoc calcicola. J Plant Physiol 148:86–91

    CAS  Google Scholar 

  • Larkum AWD, Wood WF (1993) The effect of UV-B radiation on photosynthesis and respiration of phytoplankton, benthic macroalgae and seagrasses. Photosynthesis Res 36:17–23

    Article  CAS  Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in simbiotic dinoflagellates. Limnol Oceanogr 41:271–283

    CAS  Article  Google Scholar 

  • Lesser MP, Shick JM (1989) Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition and enzymic defenses against oxygen toxicity. Mar Biol 102:243–255

    Article  Google Scholar 

  • Lesser MP, Cullen JJ, Neale PJ (1994) Carbon uptake in a marine diatom during acute exposure to ultraviolet B radiation: relative importance of damage and repair. J Phycol 30:183–192

    Article  CAS  Google Scholar 

  • MacFadyen EJ, Williamson CE, Grad G, Lowery M, Jeffrey WH, Mitchell DL (2004) Molecular response to climate change: temperature dependence of UV-induced DNA damage and repair in the freshwater crustacean Daphnia pulicaria. Global Change Biol 10:408–416

    Article  Google Scholar 

  • Mackerness SAH, Surplus SL, Jordan BR, Thomas B (1998) Effects of supplementary ultraviolet-B radiation on photosynthetic transcripts at different stages of leaf development and light levels in pea (Pisum sativum L.): role of active oxygen species and antioxidant enzymes. Photochem Photobiol 68:88–96

    Article  CAS  Google Scholar 

  • Mackerness SAH, John CF, Jordan B, Thomas B (2001) Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett 489:237–242

    Article  CAS  Google Scholar 

  • Malanga G, Puntarulo S (1995) Oxidative stress and antioxidant content in Chlorella vulgaris after exposure to ultraviolet-B radiation. Physiol Plant 94:672–679

    Article  CAS  Google Scholar 

  • Martínez R (1996) Psychrophylic and psychrotrophic respiratory metabolism in Antarctic microplankton. Polar Biol 16:483–489

    Article  Google Scholar 

  • Masaki H, Sakurai H (1997) Increased generation of hydrogen peroxide possibly from mitochondrial respiratory chain after UV irradiation of murine fibroblasts. J Dermatol Sci 14:207–216

    PubMed  Article  CAS  Google Scholar 

  • Nishikimi M, Rao NA, Yagi K (1972) The occurrence of the superoxide anion in the reaction of reduced phenazine methosulphate and molecular oxygen. Biochem Biophys Res Commun 46:849–854

    PubMed  Article  CAS  Google Scholar 

  • Packard TT (1971) Measurement of electron transport system activity in marine plankton. J Mar Res 29:235–244

    Google Scholar 

  • Pakker H, Beekman C, Breeman A (2000a) Efficient photoreactivation of UVBR-induced damage in the sublittoral macroalga Rhodymenia pseudopalmata (Rhodophyta). Eur J Phycol 35:109–114

    Article  Google Scholar 

  • Pakker H, Martins RST, Boelen P, Buma AGJ, Nikaido O, Breeman AM (2000b) Effects of temperature on the photoreactivation of ultraviolet-B-induced DNA damage in Palmaria palmata (Rhodophyta). J Phycol 36:334–341

    Article  CAS  Google Scholar 

  • Perelman A, Dubinsky Z, Martínez R (2006) Effect of low temperature on superoxide dismutase activity in plankton. J Exp J Mar Biol Ecol 334: 229–235

    Article  CAS  Google Scholar 

  • Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356

    PubMed  Article  CAS  Google Scholar 

  • Pinto E, Sigaud-Kutner CSS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018

    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 

  • Quesada A, Mouget JL, Vincent WF (1995) Growth of Antarctic cyanobacteria under ultraviolet radiation: UVA counteracts UVB inhibition. J Phycol 31:242–248

    Article  Google Scholar 

  • Rao MV, Paliyat G, Ormrod P (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136

    PubMed  Article  CAS  Google Scholar 

  • Reitner B, Herndl GJ, Herzig A (1997) Role of ultraviolet-B radiation on photochemical and microbial oxygen consumption in a humic-rich shallow lake. Limnol Oceanogr 42:950–960

    CAS  Article  Google Scholar 

  • Rijstenbil JW (2003) Effects of UVB radiation and salt stress on growth, pigments and antioxidative defence of the marine diatom Cylindrotheca closterium. Mar Ecol Prog Ser 254:37–48

    CAS  Google Scholar 

  • Rodriguez F, Varela M, Zapata M (2002) Phytoplankton assemblages in the Gerlache and Bransfield Straits (Antarctic Peninsula) determined by light microscopy and CHEMTAX analysis of HPLC pigment data. Deep Sea II 49:723–747

    Article  CAS  Google Scholar 

  • Selby CP, Sancar A (2006) A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proc Natl Acad Sci USA 103:17696–17700

    PubMed  Article  CAS  Google Scholar 

  • Schäffer J, Sebastian C, Häder D-P (1992) Effects of solar radiation on motility, orientation, pigmentation and photosynthesis in a green dinoflagellate Gymnodinium. Acta Protozool 33:59–65

    Google Scholar 

  • Shick xJM, Lesser MP, Jokiel PJ (1996) Effects of ultraviolet radiation in corals and other coral reef organisms. Glob Change Biol 2:527–545

    Article  Google Scholar 

  • Sommaruga R, Buma AGJ (2000) UV-induced cell damage is species-specific among aquatic phagotrophic protists. J Eukaryot Microbiol 47:450–455

    PubMed  Article  CAS  Google Scholar 

  • Smith RC (1989) Ozone, middle ultraviolet radiation and the aquatic environment. Photochem Photobiol 50:459–468

    CAS  Google Scholar 

  • Solomon S (1990) Progress towards a quantitative understanding of Antarctic ozone depletion. Nature 347:347–354

    Article  CAS  Google Scholar 

  • Tyagi R, Srinwas G, Vyas D, Kumar A, Kumar HD (1992) Differential effects of ultraviolet-B Wyman, M, Gregory RPF, Carr NG (1985) Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Science 230:818–820

    Google Scholar 

  • Tyystjärvi T, Tuominen I, Herranen M, Aro E-M, Tyystjärvi E (2002) Action spectrum of psbA gene transcription is similar to that of photoinhibition in Synechocystis sp. PCC 6803. FEBS 516:167–171

    Article  Google Scholar 

  • Van Donk E, Hessen DO (1995) Reduced digestibility of UV-stressed and nutrient-limited algae by Daphnia magna. Hydrobiologia 307:147–151

    Article  Google Scholar 

  • Varela M, Fernandez E, Serret P (2002) Size-fractionated phytoplankton biomass and primary production in the Gerlache and south Bransfield Straits (Antarctic Peninsula) in Austral summer 1995–1996. Deep Sea Res II:749–768

    Google Scholar 

  • Vincent WF, Roy S (1993) Solar UV-B and aquatic primary production: damage, protection and recovery. Environ Rev 1:1–12

    CAS  Google Scholar 

  • Weiler SC, Penhale PA (1994) Ultraviolet radiation in Antarctica: measurements and biological effects. American Geophysical Union, Washington

    Google Scholar 

  • Williamson CE, Zagarese HE, Schulze PC, Hargreaves BR, Seva J (1994) The impact of short-term exposure to UV-B radiation on zooplankton communities in north temperate lakes. J Plankton Res 16:205–218

    Article  Google Scholar 

  • Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41:453–465

    Article  CAS  Google Scholar 

  • Wyman M, Gregory RPF, Carr NG (1985) Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Science 230:818–820

    Article  CAS  PubMed  Google Scholar 

  • Xenopoulos MA, Schindler DW (2003) Differential responses to UV by bacterioplankton and phytoplankton from the surface and the base of the mixed layer. Fresh Biol 48:108–122

    Article  CAS  Google Scholar 

  • Xue L, Zhang Y, Zhang T, An L, Wang X (2005) Effects of enhanced ultraviolet-B radiation on algae and cyanobacteria. Crit Rev Microbiol 31:79–89

    PubMed  Article  CAS  Google Scholar 

  • Yao N, Tada Y, Sakamoto M, Nakayashiki H, Park P, Tosa Y, Mayama S (2002) Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J 30:567–579

    Google Scholar 

  • Zagarese HE, Feldman M, Williamson CE (1997) UV-B induced damage and photoreactivation in three species of Boeckella (Copepoda, Calanoida). J Plankton Res 19:357–367

    Article  Google Scholar 

  • Zhang P-Y, Yu J, Tang X-X (2005) UV-B radiation supresses the growth and antioxidant systems of two marine microalgae, Platymonas subcordiformis (Wille) Hazen and Nitzschia closterium (Ehrenb.) W. Sm. J Integr Plant Biol 47:683–691

    CAS  Article  Google Scholar 

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Acknowledgments

This work was funded by the CICYT (Spanish Ministry of Education and Science) Project ANT94-1010. I thank the crew of the R/V Hesperides for help on board and my scientific colleagues for fruitful cooperation. I am indebted to F.L. Figueroa for providing radiation data. J. Beardall and two anonymous referees provided helpful comments and suggestions that substantially improved an earlier manuscript version.

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  1. Departamento de Ciencias y Técnicas del Agua, Universidad de Cantabria, Los Castros s/n, 39005, Santander, Spain

    Rosa Martínez

  2. School of Aquaculture, University of Tasmania, Locked Bag 1370, Launceston, 7250, TAS, Australia

    Rosa Martínez

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Martínez, R. Effects of ultraviolet radiation on protein content, respiratory electron transport system (ETS) activity and superoxide dismutase (SOD) activity of Antarctic plankton. Polar Biol 30, 1159–1172 (2007). https://doi.org/10.1007/s00300-007-0273-3

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  • DOI: https://doi.org/10.1007/s00300-007-0273-3

Keywords

  • Antarctic plankton
  • Respiratory ETS
  • UV radiation effect
  • Superoxide dismutase activity