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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Austin, J., Butchart, N. & Shine, K. P. 1992. Possibility of an arctic ozone hole in a doubled CO2 climate. Nature 360: 221–225.
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.
Berg, R. J.W., de Gruijl, F. R., Roza, L. & van der Leun, J. C. 1993. Flow cytometric immunofiuorescence assay for quantification of cyclobutyldithymine dimers in separate phases of the cell cycle. Carcinogenesis 14: 103–106.
Blumthaler, M. & Almbach, W. 1990. Indication of increasing solar ultraviolet-B radiation flux in alpine regions. Science 248: 206–208.
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.
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.
Bron, S. 1972. Ultraviolet inactivation and excision-repair in Bacillus subtilis. Ph.D. Thesis, University of Groningen, the Netherlands.
Brown, C. W. 1995. Global distribution of Coccolithophore blooms. Oceanography 8: 59–60.
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.
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.
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.
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.
Cloud, P. E. 1968. Atmospheric & hydrospheric evolution on primitive earth. Science 160: 729–736.
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.
Coohill, T. P. 1991. Action spectra again? Photochem. Photobiol. 54: 859–870.
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.
Cullen J. J. & Neale, P. J. 1994. Ultraviolet radiation, ozone depletion, and marine photosynthesis. Photosynthetic Res. 39: 303–320.
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.
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.
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.
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.
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.
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.
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.
Gieskes, W. W. C., Veth, C., Woehrmann, A. & Graefe, M. 1987. Secchi Disc visibility world record shattered. EOS 68: 123.
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.
Gleason, J. F., Bhartia, P. K., Herman, J. R., McPeters, R., Newman, P., Stolarski, R. S., Flynn, L., Labow, G., Larko, D., Seft-or, C., Welemeyer, R., Komhyr, W. D., Miller, A. J. & Planet, W. 1993. Record low global ozone in 1992. Science 260: 523–526.
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.
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.
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.
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.
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.
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.
Jokiel, P. L. & York, R. H. 1984. Importance of ultraviolet radiation in photoinhibition of microalgal growth. Limnol. Oceanogr. 29: 192–199.
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.
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.
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.
Kasting, J. F. 1993. Earth’s early atmosphere. Science 259: 920–926.
Lorenzen, C. J. 1979. Ultraviolet light radiation and phytoplankton photosynthesis. Limnol. Oceanogr. 24: 1117–1120.
McElroy, M. B. & Salawitch, R. J. 1989. Changing composition of the global stratosphere. Science 243: 763–770.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Sancar, A. & Sancar, G. B. 1988. DNA repair enzymes. Annu. Rev. Biochem. 57: 29–67.
Setlow, R. B. 1974. The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Nat. Acad. Sci. 71: 3363–3366.
Smith, K. C. 1969. DNA synthesis in sensitive and resistant mutants of Escherichia coli B after UV radiation. Mutation Res. 8: 481–495.
Smith, R. C. & Baker, K. S. 1979. Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem. Photobiol. 29: 311–323.
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.
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.
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.
Sverdrup, H. U. 1953. On conditions for the vernal blooming of phytoplankton. J. Cons. Int. Explor. Mer 18: 287–295.
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.
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.
Vincent, W. & Quesada, A. 1994. Ulraviolet radiation effects on cyanobacteria: implications for Antarctic microbial systems. Antarctica Res. Ser. 62: 111–124. American Geophysical Union, Washington D.C.
Vincent, W. F. & Roy, S. 1993. Solar ultraviolet-B radiation and aquatic primary production: damage, protection and recovery. Environ. Rev. 1: 1–12.
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.
Zafiriou, O. C. 1988. Is there a measurable net marine photoreaction? Appl. Geochem. 3: 67.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1997 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Gieskes, W.W.C., Buma, A.G.J. (1997). UV damage to plant life in a photobiologically dynamic environment: the case of marine phytoplankton. In: Rozema, J., Gieskes, W.W.C., Van De Geijn, S.C., Nolan, C., De Boois, H. (eds) UV-B and Biosphere. Advances in vegetation science, vol 17. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5718-6_2
Download citation
DOI: https://doi.org/10.1007/978-94-011-5718-6_2
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-010-6411-8
Online ISBN: 978-94-011-5718-6
eBook Packages: Springer Book Archive