Skip to main content
SpringerLink
Log in

UV damage to plant life in a photobiologically dynamic environment: the case of marine phytoplankton

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

The effect of UV-B radiation on growth of marine phytoplankton was investigated in relation to DNA damage induced by a range of biologically effective doses (BEDs). Emiliania huxleyi (Prymnesiophyceae) was chosen as a model organism of the ocean's phytoplankton because of its importance in global biogeochemical cycling of carbon and sulphur, elements that influence the world's climate as components of the trace gases carbon dioxide (CO2) and dimethylsulfide (DMS). A marine diatom, Cyclotella, was studied for its capacity to repair the DNA damage, quantified as thymine dimers by the application of a monoclonal antibody against these photoproducts. DNA repair was shown to be complete after just a few hours of exposure to visible light; the repair rate increased with PAR intensity. E. huxleyi appeared to be most sensitive to UV-B radiation: growth was already affected above a dose of 100 J m-2 d-1 (biologically effective radiation, weighted with Setlow's DNA action spectrum), probably through effects on the cell cycle related to damage to nuclear DNA: mean specific growth rates were inversely correlated with thymine dimer contents in cells. Near the ocean's surface UV-B radiation conditions that induce the changes observed by us in cultures can be expected during the growing season of phytoplankton, not only in the tropics but also at higher latitudes. Nevertheles, blooms of species such as E. huxleyi are often excessive in the field. It is suggested that exposure duration of cells near the surface of the ocean can be shorter than our artificial 3 h in the laboratory due to vertical mixing, a phenomenon that is typical for the ocean's upper 50–100 m. When mixing reaches depths greater than the layer where most UV-B is attenuated, negative effects on cells through UV-A-induced inhibition of photosynthesis may prevail over DNA damage, the action spectrum of which has been shown to be limited to the UV-B part of the spectrum. Moreover, the radiation wavelengths that induce DNA damage repair (UV-A and visible) are attenuated vertically much less than UV-B. The photobiological situation in the upper ocean is much more complicated than on land, and effects of UV radiation on plankton biota can only be modelled realistically here when both the spectrally differential attenuation in the UV and visual part of the spectrum and the rate of vertical mixing are taken into account. Action spectra of both damage and repair of DNA and of photosynthesis inhibition of representative microalgal species are the second conditio sine qua non if we want to predict the effect of stratospheric ozone depletion on marine phytoplankton performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Austin, J., Butchart, N. & Shine, K. P. 1992. Possibility of an arctic ozone hole in a doubled CO2 climate. Nature 360: 221–225.

    Google Scholar 

  • Behrenfeld, M. J., Hardy, J. T., Gucinski, H., Hanneman, A., Lee, H. & Wones, A. 1993. Effects of ultraviolet-B radiation on primary production along latitudinal transects in the South Pacific Ocean. Marine Environ. Res. 35: 349–363.

    Google Scholar 

  • Berg, R. J. W., de Gruijl, F. R., Roza, L. & van der Leun, J. C. 1993. Flow cytometric immunofluorescence assay for quantification of cyclobutyldithymine dimers in separate phases of the cell cycle. Carcinogenesis 14: 103–106.

    PubMed  Google Scholar 

  • Blumthaler, M. & Almbach, W. 1990. Indication of increasing solar ultraviolet-B radiation flux in alpine regions. Science 248: 206–208.

    PubMed  Google Scholar 

  • Bornman, J. F. & Teramura, A. H. 1993. Effects of ultraviolet-B radiation on terrestrial plants. In: Young, A. et al. (eds) Environmental UV Photobiology, pp. 427–471. Plenum Press. Stratospheric ozone reduction, solar UV-B radiation, and terrestrial ecosystems. Climatic Change 28: 375–394.

    Google Scholar 

  • Bothwell, M. L., Sherbot, D., Roberg, A. C. & Daley, R. J. 1993. Influence of natural ultraviolet radiation on phytic periphytic diatom communities. J. Phycol. 29: 24–35.

    Google Scholar 

  • Bron, S. 1972. Ultraviolet inactivation and excision-repair in Bacillus subtilis. Ph.D. Thesis, University of Groningen, the Netherlands.

    Google Scholar 

  • Brown, C.W. 1995. Global distribution of Coccolithophore blooms. Oceanography 8: 59–60.

    Google Scholar 

  • Buma, A. G. J., van Hannen, E. J., Veldhuis, M. J. W. & Gieskes, W.W. C. 1996. UV-B induces DNA damage and DNA synthesis delay in the marine diatom Cyclotella sp. Sci. Marina 60: 101–105.

    Google Scholar 

  • Buma, A. G. J., van Hannen, E. J., Roza, J., Veldhuis, M. J. W. & Gieskes, W. W. C. 1995. Monitoring ultraviolet-B induced DNA damage in diatom cells by immunofluorescent thymine dimer detection. J. Phycol. 31: 314–321.

    Google Scholar 

  • Buma, A. G. J., Zemmelink, H. J., Sjollema, K. & Gieskes, W. W. C. 1996. UV-B radiation affects protein and photosynthetic pigment content, volume and ultrastructure of marine diatoms. Marine Ecol. Progress Ser. (In press).

  • Calkins, J. & Thordardottir, T. 1980. Ecological significance of solar UV radiation on aquatic organisms. Nature 283: 563–566.

    Google Scholar 

  • Calkins, J. (ed.) 1982. The role of solar ultraviolet radiation in marine ecosystems. NATO Conf. Ser. 4, Marine Sciences Vol. 7. Plenum Press, New York.

  • Carreto, J. I., Carignan, M. O., Daeo, G. & de Marco, S. G. 1990. Occurrence of mycosporine-like amino acids in the red tide dino-flagellate Alexandrium excavatum. UV-protective compounds? J. Plankton Res. 12: 909–921.

    Google Scholar 

  • Cloud, P. E. 1968. Atmospheric & hydrospheric evolution on primitive earth. Science 160: 729–736.

    PubMed  Google Scholar 

  • Coohill, T. P., Peak, M. J. & Peak, J. G. 1987. The effects of the ultraviolet wavelengths of radiation present in sunlight on human cells in vitro. Photochem. Photobiol. 46: 1043–1050.

    PubMed  Google Scholar 

  • Coohill, T. P. 1991. Action spectra again? Photochem. Photobiol. 54: 859–870.

    PubMed  Google Scholar 

  • Cullen, J. J. & Lesser, M. P. 1991. Inhibition of photosynthesis by ultraviolet radiation as a function of dose and dosage rate: results from a marine diatom. Marine Biol. 111: 183–190.

    Google Scholar 

  • Cullen J. J. & Neale, P. J. 1994. Ultraviolet radiation, ozone depletion, and marine photosynthesis. Photosynthetic Res. 39: 303–320.

    Google Scholar 

  • Cullen, J. J., Neale, P. J. & Lesser, M. P. 1992. Biological weighting function for the inhibition of phytoplankton photosynthesis by ultraviolet radiation. Science 258: 646–650.

    Google Scholar 

  • Döhler, G. 1991. Uptake of 15 N-ammonium and 15N-nitrate by Arctic diatoms: dependence on the daytime and effect of UV-B radiation. Biochem. Physiol. Pflanzen 187: 347–355.

    Google Scholar 

  • Doniger, J., Jacobson, E. D., Krell, K. & DiPaolo, J. A. 1981. Ultraviolet light action spectra for neoplastic transformation and lethality of Syrian hamster embryo cells correlate with spectrum for pyrimidine dimer formation in cellular DNA. Proc. Nat. Acad. Sci. USA 78: 2378–2382.

    PubMed  Google Scholar 

  • Ekelund, N. G. A. 1990. Effects of UV-B (290–320 nm) radiation on photosynthesis-mediated uptake of N-15 ammonia and N-15 nitrate of several marine diatoms. Bioch. Physiol. Pflanzen 181: 533–539.

    Google Scholar 

  • Falkowski, P. G., Kim, Y., Kolber, Z., Wilson, C., Wirick, C. & Cess, R. 1992. Natural versus anthropogenic factors affecting low-level cloud albedo over the North Atlantic. Science 256: 1311–1313.

    Google Scholar 

  • Friso, G., Spetea, C., Giacometti, G. J., Vass, I. & Barbato, R. 1994. Degradation of photosystem II reaction center D1-protein induced by UV-B radiation in isolated thylakoids. Identification and characterisation of C-and N-terminal breakdown products. Biochim. Biophys. Acta 1184: 78–84.

    Google Scholar 

  • Garcia-Pichel, F., Sherry, N. D. & Castenholz, R. W. 1992. Evidence for an ultraviolet sunscreen role of the extracellular pigment scytonemin in Chlorogloeopsis sp. Photochem. Photobiol. 56: 17–23.

    PubMed  Google Scholar 

  • Gieskes, W. W. C., Veth, C., Woehrmann, A. & Graefe, M. 1987. Secchi Disc visibility world record shattered. EOS 68: 123.

    Google Scholar 

  • Gieskes, W.W. C. & Kraay, G.W. 1982. Effect of enclosure in large plastic bags on diurnal change in oxygen concentration in tropical ocean water. Marine Biol. 70: 99–104.

    Google Scholar 

  • Gleason, J. F., Bhartia, P. K., Herman, J. R., McPeters, R., Newman, P., Stolarski, R. S., Flynn, L., Labow, G., Larko, D., Seftor, C., Welemeyer, R., Komhyr, W. D., Miller, A. J. & Planet, W. 1993. Record low global ozone in 1992. Science 260: 523–526.

    Google Scholar 

  • Greenberg, B. M., Gaba, V., Canaani, O., Malkin, S., Matoo, A. K. & Edelman, M. 1989. Separate photosensitizers mediate degradation of the 32-kDa photosystem II reaction center protein in the visible and UV spectral regions. Proc. Nat. Acad. Sci. USA 86: 6617–6620.

    PubMed  Google Scholar 

  • Guillard, R. R. L. 1975. Culture of phytoplankton for feeding marine invertebrates, pp. 29–60. In: Smith and Chanley (eds) Culture of marine invertebrate animals. Plenum, New York.

    Google Scholar 

  • Häder, D. P. 1993. Effects of enhanced solar ultraviolet radiation on aquatic ecosystems, pp. 155–192. In: Tevini, M. (ed.) UV-B radiation and ozone depletion. Lewis Publishers, Boca Raton.

    Google Scholar 

  • Helbling, E. W., Villafañe, V., Ferrario, M. & Holm-Hansen, O. 1992. Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species. Marine Ecol. Progr. Ser. 80: 89–100.

    Google Scholar 

  • Helbling, E. W., Villafañe, V. and Holm-Hansen, O. 1994. Effects of ultraviolet radiation on Antarctic marine phytoplankton photosynthesis with particular attention to the influence of mixing. Antarctic Res. Ser. 62: 207–227.

    Google Scholar 

  • Holm-Hansen, O., Lubin, D. & Helbling, E. W. 1993. Ultraviolet radiation and its effects on organisms in aquatic environments, pp. 379–425. In: Young A. et al. (eds.): Environmental UV Photobiology, 379–425. Plenum Press, New York.

    Google Scholar 

  • Jokiel, P. L. & York, R. H. 1984. Importance of ultraviolet radiation in photoinhibition of microalgal growth. Limnol. Oceanogr. 29: 192–199.

    Google Scholar 

  • Jordan, B. R., James, P. E., Strid, A. & Anthony, R. G. 1994. The effect of ultraviolet-B radiation on gene expression and pigment composition in etiolated and green pea leaf tissue: UV-B induced changes are gene-specific and dependent on the developmental stage. Plant Cell Environ. 17: 45–54.

    Google Scholar 

  • Karentz, D., Cleaver, J. E. & Mitchell, D. M. 1991. Cell survival charcteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation exposure. J. Phycol. 27: 326–341.

    Article  Google Scholar 

  • Karentz, D., Bothwell, M. L., Coffin, R. B., Hanson, A., Herndl, G. J., Kilham, S. S., Lesser, M. P., Lindell, M., Moeller, R. E., Morris, D. P., Neale, P. J., Sanders, R. W., Weiler C. S. & Wetze, R. G. 1994. Impact of UV-B radiation on pelagic freshwater ecosystems: report of working group on bacteria and phytoplankton. Arch. Hydrobiol. Beihefte Ergeb. Limnol. 43: 31–69.

    Google Scholar 

  • Kasting, J. F. 1993. Earth's early atmosphere. Science 259: 920–926.

    PubMed  Google Scholar 

  • Lorenzen, C. J. 1979. Ultraviolet light radiation and phytoplankton photosynthesis. Limnol. Oceanogr. 24: 1117–1120.

    Google Scholar 

  • McElroy, M. B. & Salawitch, R. J. 1989. Changing composition of the global stratosphere. Science 243: 763–770.

    Google Scholar 

  • Melis, A., Nemson, J. A. & Harrison, M. A. 1992. Damage to functional components and partial degradation of photosystem II reaction center proteins upon chloroplast exposure to ultraviolet-B radiation. Biochim. Biophys. Acta 1100: 312–320.

    Google Scholar 

  • Mizuno, T., Matsunaga, T., Ihara, M. & Nikaido, O. 1991. Establishment of a monoclonal antibody recognizing cyclobutane type thymine dimers in DNA. Mutation Res. 254: 175–184.

    PubMed  Google Scholar 

  • Mori, T., Matsunaga, T., Hirose, T. & Nikaido, O. 1988. Establishment of a monoclonal antibody recognizing ultraviolet light-induced (6–4) photoproducts. Mutation Res. 194: 263–270.

    PubMed  Google Scholar 

  • Nachtwey, D. S., Caldwell, M. J. & Biggs, R. H. (eds) 1975. Impacts of climate change on the biosphere. CIAP Monogr. 5, 1: Ultraviolet radiation effects. U.S. Department of Transport, Climate Assessment Program, Washington D.C.

  • Palenik, B., Price N. M. & Morel, F. M. M. 1993. Potential effects of UV-B on the chemical environment of marine organisms: a review. Environ. Pollut. 70: 117–130.

    Google Scholar 

  • Peletier, H., Gieskes, W.W. C. & Buma, A. G. J. 1996. Ultraviolet-B radiation resistance of benthic diatoms isolated from tidal glats in the Dutch Wadden Sea. Marine Ecol. Progr. Ser. 135: 163–168.

    Google Scholar 

  • Quaite, F. E., Sutherland, B. M. & Sutherland, J. C. 1992. Action spectrum for DNA damage in alfalfa lavers predicted impact of ozone depletion. Nature 358: 576–578.

    Article  Google Scholar 

  • Quesada, A., Mouget, J. L. & Vincent, W. F. 1995. Growth of Antarctic cyanobacteria under ultraviolet radiation: UV-A counteracts UV-B inhibition. J. Phycol. 31: 242–248.

    Google Scholar 

  • Rasmussen, R. A. & Khalil, M. A. K. 1993. The history and probable future of CFC-11 in the earth's atmosphere. EOS (Transactions of the American Geophysical Union, Fall Meeting). Abstract A12B-6.

  • Regan, J. D., Carrier, W. L., Gucinski, H., Olla, B. L., Yoshida, H., Fuyimura, R. K. & Wicklund, R. I. 1992. DNA as a solar dosimeter in the ocean. Photochem. Photobiol. 56: 35–42.

    Google Scholar 

  • Roza, L., van der Wulp, K. J. M., MacFarlane, S. J., Lohman, P. H. M. & Baan, R. A. 1988. Detection of cyclobutane thymine dimers in DNA of human cells with monoclonal antibodies raised against a thymine dimer containing tetranucleotide. Photochem. Photobiol. 48: 627–633.

    PubMed  Google Scholar 

  • Sancar, A. & Sancar, G. B. 1988. DNA repair enzymes. Annu. Rev. Biochem. 57: 29–67.

    Article  PubMed  Google Scholar 

  • Setlow, R. B. 1974. The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Nat. Acad. Sci. 71: 3363–3366.

    PubMed  Google Scholar 

  • Smith, K. C. 1969. DNA synthesis in sensitive and resistant mutants of Escherichia coli B after UV radiation. Mutation Res. 8: 481–495.

    PubMed  Google Scholar 

  • Smith, R. C. & Baker, K. S. 1979. Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem. Photobiol. 29: 311–323.

    Google Scholar 

  • Smith, R. C., Baker, K. S., Holm-Hansen, O. & Olson, R. 1980. Photoinhibition of photosynthesis and middle ultraviolet light radiation in natural waters. Photochem. Photobiol. 31: 585–592.

    Google Scholar 

  • Strid, A., Chow, W. S. & Anderson, J. J. 1990. Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. Biochim. Biophys. Acta 1020: 260–268.

    Google Scholar 

  • Sullivan, J. H., Teramura, A. H. & Ziska, L. H. 1992. Variation in UV-B sensitivity in plants from a 3000 m elevational gradient in Hawaii. Am. J. Bot. 79: 734–743.

    Google Scholar 

  • Sverdrup, H. U. 1953. On conditions for the vernal blooming of phytoplankton. J. Cons. Int. Explor. Mer 18: 287–295.

    Google Scholar 

  • Towe, K. J. 1992. Stratospheric ozone trends. Science 257–727.

  • Tyrell, R. J. 1986. Repair of genetic damage induced by UV-B (290- 320 nm) radiation, pp. 139–149. In: Worrest, R. C. & Caldwell, M. M. (eds) Stratospheric ozone reduction, solar UV radiation and plant life NATO ASI series G8. Springer-Verlag, Berlin.

    Google Scholar 

  • Veen, A., Buma, A. G. J., Gieskes, W. W. C. & van Liere, L. 1995. Effects of ozone related UV-B enhancement on aquatic ecosystems. R.I.V.M. Report 731054002: 1–121.

    Google Scholar 

  • Vincent, W. & Quesada, A. 1994. Ulraviolet radiation effects on cyanobacteria: implications for Antarcticmicrobial systems. Antarctica Res. Ser. 62: 111–124. American Geophysical Union, Washington D.C.

    Google Scholar 

  • Vincent, W. F. & Roy, S. 1993. Solar ultraviolet-B radiation and aquatic primary production: damage, protection and recovery. Environ. Rev. 1: 1–12.

    Google Scholar 

  • Warnock, R. E., van Laar, S. & Gieskes, W.W. C. 1997. Absorption by yellow substance in the Southern North Sea. J. Sea Res. (In press).

  • Weinert, T. & Hartwell, L. 1989. Control of G2 delay by the RAD9 gene of Saccharomyces cerevisiae. J. Cell Sci., Suppl. 12: 145–148.

    Google Scholar 

  • Zafiriou, O. C. 1988. Is there ameasurable netmarine photoreaction? Appl. Geochem. 3: 67.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Marine Biology, University of Groningen, 9750 AA, Haren, The Netherlands

    W.W.C. Gieskes & A.G.J. Buma

Authors
  1. W.W.C. Gieskes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A.G.J. Buma
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gieskes, W., Buma, A. UV damage to plant life in a photobiologically dynamic environment: the case of marine phytoplankton. Plant Ecology 128, 17–25 (1997). https://doi.org/10.1023/A:1009750621449

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1009750621449

Search

Navigation