Effects of Metal Combinations on the Production of Phytochelatins and Glutathione by the Marine Diatom Phaeodactylum tricornutum
Received: 21 February 2005 Accepted: 06 April 2005 DOI:
Cite this article as: Kawakami, S.K., Gledhill, M. & Achterberg, E.P. Biometals (2006) 19: 51. doi:10.1007/s10534-005-5115-6 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 Cu 2 and 0.45 μM Cd 2+) to the culture medium induced the production of short-chained phytochelatins (( γ-Glu-Cys) -Gly where n n = 2–5), whereas a single addition of Zn (2.2 μM Zn 2+) 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 References Ahner, BA, Kong, S, Morel, FMM 1995 Phytochelatin production in marine-algae. 1. An Interspecies Comparison Limnol Oceanogr 40 649 657 Google Scholar Ahner, BA, Morel, FMM 1995 Phytochelatin production in marine-algae 2. Induction by various metals Limnol Oceanogr 40 658 665 Google Scholar Ahner, BA, Wei, LP, Oleson, JR, Ogura, N 2002 Glutathione and other low molecular weight thiols in marine phytoplankton under metal stress Mar Ecol Prog Ser 232 93 103 Google Scholar Cid, A, Herrero, C, Torres, E, Abalde, J 1995 Copper toxicity on the marine microalga Phaeodactylum tricornutum – effects on photosynthesis and related parameters Aquat Toxicol 31 165 174 CrossRef Google Scholar Cobbett, CS 2000 Phytochelatins and their roles in heavy metal detoxification Plant Physiol 123 825 832 CrossRef PubMed Google Scholar Croot, PL, Moffett, JW, Brand, LE 2000 Production of extracellular Cu complexing ligands by eucaryotic phytoplankton in response to Cu stress Limnol Oceanogr 45 619 627 Google Scholar
Da Silva JJRF, Williams RJP. 1991 The Biological Chemistry of the Elements. Clarendon, 561 pp.
Faheay, RC, Buschbacher, RM, Newton, GL 1987 The evolution of glutathione metabolism in phototrophic microorganisms J Mol Evol 25 81 88 Google Scholar Fox, TC, Guerinot, ML 1998 Molecular biology of cation transport in plants Annu Rev Physiol Plant Mol Biol 49 669 696 Google Scholar Grill, E, Winnacker, EL, Zenk, MH 1985 Phytochelatins – the principal heavy-metal complexing peptides of higher-plants Science 230 674 676 Google Scholar Knauer, K, Ahner, B, Xue, HB, Sigg, L 1998 Metal and phytochelatin content in phytoplankton from freshwater lakes with different metal concentrations Environ Toxicol Chem 17 2444 2452 CrossRef Google Scholar Lee, JG, Ahner, BA, Morel, FMM 1996 Export of cadmium and phytochelatin by the marine diatom Thalassiosira weissflogii Environ Sci Technol 30 1814 1821 Google Scholar Morel, FMM, Rueter, JG, Anderson, DM, Guillard, RRL 1979 Aquil: a chemically defined phytoplankton culture medium for trace metal studies J Phycol 15 135 145 CrossRef Google Scholar Morelli, E, Pratesi, E 1997 Production of phytochelatins in the marine diatom Phaeodactylum tricornutum in response to copper and cadmium exposure Bull Environ Contam Toxicol 59 657 664 CrossRef PubMed Google Scholar Morelli, E, Scarano, G 1995 Cadmium-induced phytochelatins in marine alga Phaeodactylum tricornutum – effect of metal speciation Chem Spec Bioavail 7 43 47 Google Scholar Morelli, E, Scarano, G 2001 Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutum Mar Environ Res 52 383 395 CrossRef PubMed Google Scholar Morelli, E, Scarano, G 2004 Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutum Plant Sci 167 289 296 CrossRef Google Scholar Okamoto, OK, Pinto, E, Latorre, LR, Bechara, EJH, Colepicolo, P 2001 Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts Arch Environ Contam Toxicol 40 18 24 PubMed Google Scholar Price, NM, Harrison, GI, Hering, JG, Hudson, RJ, Nirel, PMV, Palenki, B, Morel, FMM 1988 Preparation and chemistry of the artificial algal culture medium Aquil Biol Oceanogr 6 443 461 Google Scholar Rauser, WE 1990 Phytochelatins Annu Rev Biochem 59 61 86 CrossRef PubMed Google Scholar Rijstenbil, JW, Wijnholds, JA 1996 HPLC analysis of nonprotein thiols in planktonic diatoms: Pool size, redox state and response to copper and cadmium exposure Mar Biol 127 45 54 CrossRef Google Scholar Scarano, G, Morelli, E 2002 Characterization of cadmium- and lead-phytochelatin complexes formed in a marine microalga in response to metal exposure Biometals 15 145 151 CrossRef PubMed Google Scholar Schecher, WD, Mcavoy, DC 1992 Mineql+ – A software environment for chemical-equilibrium modeling Comp Environ Urban Syst 16 65 76 Google Scholar Serkiz, SM, Allison, JD, Perdue, EM, Allen, HE, Brown, DS 1996 Correcting errors in the thermodynamic database for the equilibrium speciation model MINTEQA2 Water Res 30 1930 1933 CrossRef Google Scholar Sunda, WG, Huntsman, SA 1996 Antagonisms between cadmium and zinc toxicity and manganese limitation in a coastal diatom Limnol Oceanogr 41 373 387 Google Scholar Tang, DG, Hung, CC, Warnken, KW, Santschi, PH 2000 The distribution of biogenic thiols in surface waters of Galveston Bay Limnol Oceanogr 45 1289 1297 Google Scholar Torres, E, Cid, A, Fidalgo, P, Herrero, C, Abalde, J 1997 Long-chain class III metallothioneins as a mechanism of cadmium tolerance in the marine diatom Phaeodactylum tricornutum Bohlin Aquat Toxicol 39 231 246 CrossRef Google Scholar Torres, E, Cid, A, Herrero, C, Abalde, J 2000 Effect of cadmium on growth, ATP content, carbon fixation and ultrastructure in the marine diatom Phaeodactylum tricornutum Bohlin Water Air Soil Pollution 117 1 14 CrossRef Google Scholar Twiss, MR, Errecalde, O, Fortin, C, Campbell, PGC, Jumarie, C, Denizeau, F, Berkelaar, E, Hale, B, Rees, K 2001 Coupling the use of computer chemical speciation models and culture techniques in laboratory investigations of trace metal toxicity Chem Spec Bioavailab 13 9 24 Google Scholar Wei, LP, Donat, JR, Fones, G, Ahner, BA 2003 Interactions between Cd, and Cu, and Zn influence particulate phytochelatin concentrations in marine phytoplankton: laboratory results and preliminary field data Environ Sci Technol 37 3609 3618 PubMed Google Scholar Williams, LE, Pitman, JK, Hall, JL 2000 Emerging mechanisms for heavy metal transport in plants Biochim Biophys Acta 1465 104 126 PubMed Google Scholar