Abstract
The thiol peptide phytochelatins (PC2; the polymer with n = 2) are efficient metal-chelating compounds produced by phytoplankton and higher plants. Both PC2 and their precursor glutathione (GSH) are related to detoxification mechanisms. GSH and PC2 were quantified using liquid chromatography with fluorescent detection and observed in the particulate phase along a salinity gradient of the Tamar Estuary (SW UK), a heavily metal impacted site, at concentrations up to 274 and 16.5 μmol (g chl a)−1, respectively. The peptides predominated within low (0–5) and mid-salinities (5–20). Down-estuary, at sites farther from metal sources and salinities higher than 20, PC2 showed a sharp decrease or were not detected. High PC2/GSH ratios indicated areas with augmented concentrations of bioavailable metals at the tidal limit, near Cu mines and the mid-estuary where resuspension of sediments occurs. By following typical partitioning patterns previously reported for dissolved Cu and Zn, the production of thiol peptides, notably PC2, reflected a rapid interaction between the particulate and dissolved phases.
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References
Ackroyd, D.R., A.J. Bale, R.J.M. Howland, S. Knox, G.E. Millward, and A.W. Morris. 1986. Distributions and behaviour of dissolved Cu, Zn and Mn in the Tamar Estuary. Estuarine, Coastal and Shelf Science 23: 621–640.
Ahner, B.A., and F.M.M. Morel. 1995. Phytochelatin production in marine algae. 2. Induction by various metals. Limnology and Oceanography 40: 658–665.
Ahner, B.A., N.M. Price, and F.M.M. Morel. 1994. Phytochelatin production by marine-phytoplankton at low free metal-ion concentrations—laboratory studies and field data from Massachusetts Bay. Proceedings of the National Academy Sciences of the USA 91: 8433–8436.
Ahner, B.A., F.M.M. Morel, and J.M. Moffett. 1997. Trace metal control of phytochelatin production in coastal waters. Limnology and Oceanography 42: 601–608.
Ahner, B.A., J.G. Lee, N.M. Price, and F.M.M. Morel. 1998. Phytochelatin concentrations in the equatorial Pacific. Deep‐Sea Res. I. 45: 1779–1796.
Brand, L.E., W.G. Sunda, and R.R.L. Guillard. 1986. Reduction of marine phytoplankton reproduction rates by copper and cadmium. Marine Biology and Ecology 96: 225–250.
Braungardt, C.B., E.P. Achterberg, F. Elbaz-Poulichet, and N.H. Morley. 2003. Metal geochemistry in a mine-polluted estuarine system in Spain. Applied Geochemistry 18: 1757–1771.
Cid, A., C. Herrero, E. Torres, and J. Abalde. 1995. Copper toxicity on the marine microalga Phaeodactylum tricornutum: effects on photosynthesis and related parameters. Aquatic Toxicology 31: 165–174.
Dupont, C.L., T.J. Goepfert, P. Lo, L. Wei, and B.A. Ahner. 2004. Diurnal cycling of glutathione in marine phytoplankton: field and culture studies. Limnology and Oceanography 49: 991–996.
Elliott, M., and V. Quintino. 2007. The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin 54: 640–645.
Grill, E., S. Loffler, E.L. Winnacker, and M.H. Zenk. 1989. Phytochelatins, the heavy metal binding peptides of plants, are synthesized from glutathione by a specific g-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proceedings of the National Academy of Science USA 86: 6838–6842.
Howeel, K.A., E.P. Achterberg, A.D. Tappin, and P.J. Worsfold. 2006. Colloidal metals in the Tamar Estuary and their influence on metal fractionation by membrane filtration. Environmental Chemistry 3: 199–207.
Kawakami, S.K. 2004. Production of particulate phytochelatins as a metal stress indication in natural waters. Ph.D. thesis, University of Plymouth, Faculty of Sciences.
Kawakami, S.K., M. Gledhill, and E.P. Achterberg. 2006a. Determination of phytochelatins and glutathione in phytoplankton from natural waters using HPLC with fluorescence detection. TrAC. Trends in Analytical Chemistry 25: 133–142.
Kawakami, S.K., M. Gledhill, and E.P. Achterberg. 2006b. Production of phytochelatins and glutathione by marine phytoplankton in response to metal stress. Journal of Phycology 42: 975–989.
Kawakami, S.K., M. Gledhill, and E.P. Achterberg. 2006c. Effects of metal combinations on phytochelatins and glutathione production by the marine diatom Phaeodactylum tricornutum. Biometals 19: 51–60.
Knauer, K., B. Ahner, H.B. Xue, and L. Sigg 1998. Metal and phytochelatin content in phytoplankton from freshwater lakes with different metal concentrations. Environmental Toxicology and Chemistry. 17: 2444–2452.
Langston, W. J., Chesman, B.S., Burt, G.R., Hawkins, S.J., Readman, J., and Worsfold, P., 2003. Characterisation of European Marine Sites. Plymouth Sound and Estuaries (candidate) special area of conservation. Marine Biological Association of the UK. Occasional publication 9, 160 pp
Leal, M.F.C., M.T.S.D. Vasconcelos, and C.M.C. van den Berg. 1999. Copper-induced release of complexing ligands similar to thiols by Emiliania huxleyi in seawater cultures. Limnology and Oceanography 44: 1750–1762.
Matrai, P.A., and R.D. Vetter. 1988. Particulate thiols in coastal waters—the effect of light and nutrients on their planktonic production. Limnology and Oceanography 33: 624–631.
Mighanetara, K., C.B. Braungardt, J.S. Rieuwerts, and F. Azizi. 2009. Contaminant fluxes from point and diffuse sources from abandoned mines in the River Tamar catchment, UK. Journal of Geochemical Exploration 100: 116–124.
Noctor, G., and C.H. Foyer. 1998. Ascorbate and glutathione: keeping reactive oxygen under control. Annual Review in Plant Physiology and Molecular Biology 49: 249–279.
Parsons, T.R., Y. Maita, and C.M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. Oxford: Pergamon.
Richards, C.L., S.N. White, M.A. McGuire, S.J. Franks, L.A. Donovan, and R. Mauricio. 2010. Plasticity, not adaptation to salt level, explains variation along a salinity gradient in a salt marsh perennial. Estuaries and Coasts 33: 840–852.
Rijstenbil, J.W., and J.A. Wijnholds. 1996. HPLC analysis of nonprotein thiols in planktonic diatoms: pool size, redox state and response to copper and cadmium exposure. Marine Biology 127: 45–54.
Tang, D., C. Hung, K.W. Warnken, and P. Santschi. 2000. The distribution of biogenic thiols in surface waters of Galveston Bay. Limnology and Oceanography 45: 1289–1297.
Telesh, I.V., and V.V. Khlebovich. 2010. Principal processes within the estuarine salinity gradient: a review. Marine Pollution Bulletin 61: 149–155.
Uncles, R.J., and J.A. Stephens. 1993. The freshwater–saltwater interface and its relationship to the turbidity maximum in the Tamar Estuary, United Kingdom. Estuaries 16: 126–141.
Van den Berg, C.M.G. 1991. Monitoring of labile copper and zinc in estuarine waters using cathodic stripping chronopotentiometry. Marine Chemistry 34: 211–223.
Wei, L.P., J.R. Donat, G. Fones, and B.A. Ahner. 2003. Interactions between Cd, Cu and Zn influence particulate phytochelatin concentrations in marine phytoplankton: laboratory results and preliminary field data. Environmental Science and Technology 37: 3609–3618.
Whitworth, D.J. 1999. Monitoring of trace metal behavior in natural waters. Ph.D. thesis, University of Plymouth.
Acknowledgements
Financial support was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq-Brazil (200252/00-3) and European Union IMTEC Project (EVK3-CT-2000-00036). We thank the reviewers for the constructive comments to improve the manuscript.
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Kawakami, S.K., Achterberg, E.P. Particulate Thiol Peptides Along a Salinity Gradient of a Metal-Contaminated Estuary. Estuaries and Coasts 35, 658–664 (2012). https://doi.org/10.1007/s12237-011-9451-1
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DOI: https://doi.org/10.1007/s12237-011-9451-1