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Mechanism of toxicity of ionic copper and copper complexes to algae

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The mechanism of toxicity of ionic copper and copper complexes to growth, photosynthesis, respiration, ATP levels and mitochondrial electron-transport chain-activity in two marine diatoms, Nitzschia closterium (Ehrenberg) W. Smith (Hasle, 1964) and Asterionella glacialis Castracane, and one freshwater green alga, Chlorella pyrenoidosa Chick was investigated. Copper ions depressed both cell division and photosynthesis in A. glacialis and C. pyrenoidosa, whereas ionic copper concentrations which were inhibitory to cell division in N. closterium had no effect on photosynthesis, respiration, ATP production, electron transport or membrane ultrastructure. This suggests that in N. closterium, copper does not act on the chloroplast, the mitochondrion, or the cell membrane, since if it did, the above parameters should be affected. Copper-ethylxanthogenate was exceptional amongst the copper complexes in that it stimulated respiration, mitochondrial electrontransport and ATP formation in N. closterium under conditions of strongly inhibited cell division and slightly stimulated photosynthesis. Ionic copper toxicity may result from an intracellular reaction between copper and reduced glutathione (GSH), leading to a lowering of the GSH:GSSG ratio and suppression of mitosis. In addition, copper inhibits the enzyme catalase and reduces cell defence mechanisms against H2O2 and oxygen-free radicals. Lipid-soluble copper complexes are more toxic than ionic copper because both the metal and the ligand are introduced into the cell. Toxicity of ionic copper is ameliorated by trivalent metal ions in the growth medium, including those of Mn, Co, Al, Fe and Cr which form a layer of metal (III) hydroxide around the algal cell, adsorb copper and reduce its penetration into the cell. The degree of insolubility of the metal (III) hydroxide is related to its ability to protect against copper toxicity. In addition, manganese and cobalt catalytically scavenge damaging H2O2 and superoxide radicals, respectively, produced by the cell.

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Literature cited

  • Ahsanullah, M. and T. M. Florence: Toxicity of copper to the marine amphipod Allorchestes compressa in the presence of water-and lipid-soluble ligands. Mar. Biol. 84, 41–45 (1984)

    Google Scholar 

  • Cedeno-Maldonado, A. and J. A. Swader: Studies on the mechanism of copper toxicity in Chlorella. Weed Sci. 22, 443–449 (1974)

    Google Scholar 

  • Davies, A. G.: An assessment of the basis of mercury tolerance in Dunaliella tertiolecta. J. mar. biol. Ass. UK. 56, 39–57 (1976)

    Google Scholar 

  • Erickson, S. J.: Toxicity of copper to Thalassiosira pseudonana in unenriched inshore seawater. J. Phycol. 8, 318–323 (1972)

    Google Scholar 

  • Fisher, N. S. and G. J. Jones: Effects of copper and zinc on growth, morphology and metabolism of Asterionella japonica (Cleve). J. exp. mar. Biol. Ecol. 51, 37–56 (1981)

    Google Scholar 

  • Florence, T. M.: Development of physico-chemical speciation procedures to investigate the toxicity of copper, lead, cadmium and zinc towards aquatic biota. Analytica chim. Acta 141, 73–94 (1982)

    Google Scholar 

  • Florence, T. M.: The production of hydroxyl radical from hydrogen peroxide. J. inorg. Biochem. 22, 221–230 (1984)

    Google Scholar 

  • Florence, T. M., B. G. Lumsden and J. J. Fardy: Evaluation of some physico-chemical techniques for the determination of the fraction of dissolved copper toxic to the marine diatom, Nitzschia closterium. Analytica chim. Acta 151, 281–295 (1983)

    Google Scholar 

  • Florence, T. M., B. G. Lumsden and J. J. Fardy: Algae as indicators of copper speciation. In: Complexation of trace metals in natural waters, pp 411–418. Ed. by C. J. M. Kramer and J. C. Duinker. The Hague: Martinus Nijhoff/Dr. W. Junk Publishers 1984

    Google Scholar 

  • Florence, T. M. and J. L. Stauber: Toxicity of copper complexes to the marine diatom Nitzschia closterium. Aquat. Toxic. 8, 11–26 (1986)

    Google Scholar 

  • Florence, T. M., J. L. Stauber and K. J. Mann: The reaction of copper-2,9-dimethyl-1, 10-phenanthroline with hydrogen peroxide. J. inorg. Biochem. 24, 243–254 (1985)

    Google Scholar 

  • Gavis, J.: Toxic binding of cupric ion by marine phytoplankton. J. mar. Res. 41, 53–63 (1983)

    Google Scholar 

  • Guillard, R. R. L. and J. H. Ryther: Studies of marine planktonic diatoms. I. Cyclotella nana and Detonula confervaceae Hustedt (Cleve) Gran. Can. J. Microbiol. 8, 229–239 (1962)

    Google Scholar 

  • Hare, T. A. and R. R. Schmidt: Synthesis of reduced glutathione from an endogenous source of sulfur immediately prior to nuclear division in synchronized Chlorella. Biochim. biophys. Acta 192, 537–539 (1969)

    Google Scholar 

  • Hasle, G. R.: Nitzschia and Fragilariopsis species studied in the light and electron microscopes. I. Some marine species of the groups Nitzschiella and Lanceolatae, Skr. norske Vidensk-Akad. Mat.-naturv. K1 (N.S) 16, 1–48 (1964)

    Google Scholar 

  • Holm-Hansen, O. and C. R. Booth: The measurement of adenosine triphosphate in the ocean and its ecological significance. Limnol. Oceanogr. 11, 510–519 (1966)

    Google Scholar 

  • Kenner, R. A. and S. I. Ahmed: Measurements of electron transport activities in marine phytoplankton. Mar. Biol. 33, 119–127 (1975)

    Google Scholar 

  • Kosower, N. S. and E. M. Kosower: The glutathione status of cells. Int. Rev. Cytol. 54, 109–160 (1978)

    Google Scholar 

  • Lumsden, B. G. and T. M. Florence: A new algal assay procedure for the determination of the toxicity of copper species in sea water. Envir. Technol. Lett. (U.K.) 4, 271–276 (1983)

    Google Scholar 

  • McBrien, D. C. H. and K. A. Hassall: The effect of toxic doses of copper upon respiration, photosynthesis and growth of Chlorella vulgaris. Physiologia Pl. 20, 113–117 (1967)

    Google Scholar 

  • Magnuson, V. R., D. K. Harris, M. S. Sun, D. K. Taylor and G. E. Glass: Relationships of activities of metal-ligand species to aquatic toxicity. In: Chemical modelling in aqueous systems, pp 635–656. Ed. by E. A. Jenne. Washington D.C.: American Chemical Society 1979

    Google Scholar 

  • Onfelt, A.: Spindle disturbances in mammalian cells. I. Changes in the quantity of free sulphydryl groups in relation to survival and c-mitosis in V79 chinese hamster cells after treatment with colcemid, diamide, carbaryl and methyl-mercury. Chem. biol. Interactions 46, 201–217 (1983)

    Google Scholar 

  • Overnell, J.: The effect of heavy metals on photosynthesis and loss of cell potassium in two species of marine algae, dunaliella tertiolecta and Phaeodactylum tricornutum. Mar. Biol. 29, 99–103 (1975)

    Google Scholar 

  • Ringbom, A.: Complexation in analytical chemistry, 395 pp. New York: Wiley Interscience 1963

    Google Scholar 

  • Samuel, J. C.: The effects of copper on two species of unicellular marine algae, 125 pp. MSc. Thesis, University of Sydney 1976

  • Silio, F. and M. D. Angulo: Reversion of colchicine induced c-mitosis by indolylacetic acid-coenzyme A. In: Mechanism of mutation and inducing factors, pp 423–426. Ed. by Z. Landa. Prague: Academia 1967

    Google Scholar 

  • Stauber, J. L. and T. M. Florence: The influence of iron on copper toxicity to the marine diatom, Nitzschia closterium (Ehrenberg) W. Smith. Aquat. Toxic. 6, 297–305 (1985a)

    Google Scholar 

  • Stauber, J. L. and T. M. Florence: Interactions of copper and manganese: a mechanism by which manganese alleviates copper toxicity to the marine diatom, Nitzschia closterium (Ehrenberg) W. Smith. Aquat. Toxic. 7, 241–254 (1985b)

    Google Scholar 

  • Stauber, J. L. and T. M. Florence: Reversibility of copper-thiol binding in Nitzschia closterium and Chlorella pyrenoidosa. Aquat. Toxic. 8, 223–229 (1986)

    Google Scholar 

  • Steeman Nielsen, E. and L. Kamp-Nielsen: Influence of deleterious concentrations of copper on the growth of Chlorella pyrenoidosa. Physiologia Pl. 23, 828–840 (1970)

    Google Scholar 

  • Steemann Nielsen, E., L. Kamp-Nielsen and S. Wium-Andersen: Influence of deleterious concentrations of copper on the photosynthesis of Chlorella pyrenoidosa. Physiologia Pl. 22, 1121–1133 (1969)

    Google Scholar 

  • Stein, J. R.: Handbook of phycological methods. Culture methods and growth measurements. 448 pp. Cambridge: University Press 1973

    Google Scholar 

  • Sunda, W. G. and S. A. Huntsman: Effect of competitive interactions between manganese and copper on cellular manganese and growth in estuarine and oceanic species of the diatom Thalassiosira. Limnol. Oceanogr. 28, 924–934 (1983)

    Google Scholar 

  • Viarengo, A., M. Pertica, G. Mancinell, R. Capell and M. Orunesu: Effects of copper on the uptake of amino acids, on protein synthesis and on ATP content in different tissues of Mytilus galloprovincialis. Mar. envirl Res. 4, 145–152 (1981)

    Google Scholar 

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Communicated by G.F. Humphrey, Sydney

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Stauber, J.L., Florence, T.M. Mechanism of toxicity of ionic copper and copper complexes to algae. Mar. Biol. 94, 511–519 (1987). https://doi.org/10.1007/BF00431397

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