Biometals

, Volume 19, Issue 1, pp 51–60

Effects of Metal Combinations on the Production of Phytochelatins and Glutathione by the Marine Diatom Phaeodactylum tricornutum

  • Silvia K. Kawakami
  • Martha Gledhill
  • Eric P. Achterberg
Article

Abstract

Copper, Cd and Zn can be found at elevated concentrations in contaminated estuarine and coastal waters and have potential toxic effects on phytoplankton species. In this study, the effects of these metals on the intracellular production of the polypeptides phytochelatin and glutathione by the marine diatom Phaeodactylum tricornutum were examined in laboratory cultures. Single additions of Cu and Cd (0.4 μM Cu2 and 0.45 μM Cd2+) to the culture medium induced the production of short-chained phytochelatins ((γ-Glu-Cys)n-Gly where n = 2–5), whereas a single addition of Zn (2.2 μM Zn2+) did not stimulate phytochelatin production. Combination of Zn with Cu resulted in a similar phytochelatin production compared with a single Cu addition. The simultaneous exposure to Zn and Cd led to an antagonistic effect on phytochelatin production, which was probably caused by metal competition for cellular binding sites. Glutathione concentrations were affected only upon exposure to Cd (85% increase) or the combination of Cd with Zn (65% decrease), relative to the control experiment. Ratios of phytochelatins to glutathione indicated a pronounced metal stress in response to exposures to Cu or Cd combined with Zn. This study indicates that variabilities in phytochelatin and glutathione production in the field can be explained in part by metal competition for cellular binding sites.

Keywords

glutathione metal toxicity metal stress Phaeodactylum tricornutum phytochelatins thiols 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ahner, BA, Kong, S, Morel, FMM 1995Phytochelatin production in marine-algae. 1. An Interspecies ComparisonLimnol Oceanogr40649657Google Scholar
  2. Ahner, BA, Morel, FMM 1995Phytochelatin production in marine-algae 2. Induction by various metalsLimnol Oceanogr40658665Google Scholar
  3. Ahner, BA, Wei, LP, Oleson, JR, Ogura, N 2002Glutathione and other low molecular weight thiols in marine phytoplankton under metal stressMar Ecol Prog Ser23293103Google Scholar
  4. Cid, A, Herrero, C, Torres, E, Abalde, J 1995Copper toxicity on the marine microalga Phaeodactylum tricornutum – effects on photosynthesis and related parametersAquat Toxicol31165174CrossRefGoogle Scholar
  5. Cobbett, CS 2000Phytochelatins and their roles in heavy metal detoxificationPlant Physiol123825832CrossRefPubMedGoogle Scholar
  6. Croot, PL, Moffett, JW, Brand, LE 2000Production of extracellular Cu complexing ligands by eucaryotic phytoplankton in response to Cu stressLimnol Oceanogr45619627Google Scholar
  7. Da Silva JJRF, Williams RJP. 1991 The Biological Chemistry of the Elements. Clarendon, 561 pp.Google Scholar
  8. Faheay, RC, Buschbacher, RM, Newton, GL 1987The evolution of glutathione metabolism in phototrophic microorganismsJ Mol Evol258188Google Scholar
  9. Fox, TC, Guerinot, ML 1998Molecular biology of cation transport in plantsAnnu Rev Physiol Plant Mol Biol49669696Google Scholar
  10. Grill, E, Winnacker, EL, Zenk, MH 1985Phytochelatins – the principal heavy-metal complexing peptides of higher-plantsScience230674676Google Scholar
  11. Knauer, K, Ahner, B, Xue, HB, Sigg, L 1998Metal and phytochelatin content in phytoplankton from freshwater lakes with different metal concentrationsEnviron Toxicol Chem1724442452CrossRefGoogle Scholar
  12. Lee, JG, Ahner, BA, Morel, FMM 1996Export of cadmium and phytochelatin by the marine diatom Thalassiosira weissflogiiEnviron Sci Technol3018141821Google Scholar
  13. Morel, FMM, Rueter, JG, Anderson, DM, Guillard, RRL 1979Aquil: a chemically defined phytoplankton culture medium for trace metal studiesJ Phycol15135145CrossRefGoogle Scholar
  14. Morelli, E, Pratesi, E 1997Production of phytochelatins in the marine diatom Phaeodactylum tricornutum in response to copper and cadmium exposureBull Environ Contam Toxicol59657664CrossRefPubMedGoogle Scholar
  15. Morelli, E, Scarano, G 1995Cadmium-induced phytochelatins in marine alga Phaeodactylum tricornutum – effect of metal speciationChem Spec Bioavail74347Google Scholar
  16. Morelli, E, Scarano, G 2001Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutumMar Environ Res52383395CrossRefPubMedGoogle Scholar
  17. Morelli, E, Scarano, G 2004Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutumPlant Sci167289296CrossRefGoogle Scholar
  18. Okamoto, OK, Pinto, E, Latorre, LR, Bechara, EJH, Colepicolo, P 2001Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplastsArch Environ Contam Toxicol401824PubMedGoogle Scholar
  19. Price, NM, Harrison, GI, Hering, JG, Hudson, RJ, Nirel, PMV, Palenki, B, Morel, FMM 1988Preparation and chemistry of the artificial algal culture medium AquilBiol Oceanogr6443461Google Scholar
  20. Rauser, WE 1990PhytochelatinsAnnu Rev Biochem596186CrossRefPubMedGoogle Scholar
  21. Rijstenbil, JW, Wijnholds, JA 1996HPLC analysis of nonprotein thiols in planktonic diatoms: Pool size, redox state and response to copper and cadmium exposureMar Biol1274554CrossRefGoogle Scholar
  22. Scarano, G, Morelli, E 2002Characterization of cadmium- and lead-phytochelatin complexes formed in a marine microalga in response to metal exposureBiometals15145151CrossRefPubMedGoogle Scholar
  23. Schecher, WD, Mcavoy, DC 1992Mineql+ – A software environment for chemical-equilibrium modelingComp Environ Urban Syst166576Google Scholar
  24. Serkiz, SM, Allison, JD, Perdue, EM, Allen, HE, Brown, DS 1996Correcting errors in the thermodynamic database for the equilibrium speciation model MINTEQA2Water Res3019301933CrossRefGoogle Scholar
  25. Sunda, WG, Huntsman, SA 1996Antagonisms between cadmium and zinc toxicity and manganese limitation in a coastal diatomLimnol Oceanogr41373387Google Scholar
  26. Tang, DG, Hung, CC, Warnken, KW, Santschi, PH 2000The distribution of biogenic thiols in surface waters of Galveston BayLimnol Oceanogr4512891297Google Scholar
  27. Torres, E, Cid, A, Fidalgo, P, Herrero, C, Abalde, J 1997Long-chain class III metallothioneins as a mechanism of cadmium tolerance in the marine diatom Phaeodactylum tricornutum BohlinAquat Toxicol39231246CrossRefGoogle Scholar
  28. Torres, E, Cid, A, Herrero, C, Abalde, J 2000Effect of cadmium on growth, ATP content, carbon fixation and ultrastructure in the marine diatom Phaeodactylum tricornutum BohlinWater Air Soil Pollution117114CrossRefGoogle Scholar
  29. Twiss, MR, Errecalde, O, Fortin, C, Campbell, PGC, Jumarie, C, Denizeau, F, Berkelaar, E, Hale, B, Rees, K 2001Coupling the use of computer chemical speciation models and culture techniques in laboratory investigations of trace metal toxicityChem Spec Bioavailab13924Google Scholar
  30. Wei, LP, Donat, JR, Fones, G, Ahner, BA 2003Interactions between Cd, and Cu, and Zn influence particulate phytochelatin concentrations in marine phytoplankton: laboratory results and preliminary field dataEnviron Sci Technol3736093618PubMedGoogle Scholar
  31. Williams, LE, Pitman, JK, Hall, JL 2000Emerging mechanisms for heavy metal transport in plantsBiochim Biophys Acta1465104126PubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Silvia K. Kawakami
    • 1
  • Martha Gledhill
    • 2
  • Eric P. Achterberg
    • 2
  1. 1.School of Earth, Ocean and Environmental ScienceUniversity of PlymouthPlymouthUK
  2. 2.School of Ocean and Earth ScienceUniversity of Southampton, National Oceanography Centre SouthamptonSouthamptonUK

Personalised recommendations