Toxicity ranking of estuarine sediments on the basis of Sparus aurata biomarkers

Sparus aurata biomarkers were used to rank sediments from the Sado River estuary (Portugal) according to their toxicity. Initially, the activities of liver ethoxyresorufin‐O‐deethylase, liver and gill glutathione S‐transferases, muscle lactate dehydrogenase, and brain acetylcholinesterase were tested in a laboratory bioassay with the reference compound benzo[a]pyrene. Enzymatic activities were determined in different tissues of fish exposed for 48, 96, or 240 h to three concentrations of benzo[a]pyrene (25, 50, and 100 μg/L). Induction of liver ethoxyresorufin‐O‐deethylase was observed at all the exposure periods and concentrations, suggesting a continuous response of this system to toxicant exposure. Induction of liver glutathione S‐transferases activity was only observed after 240 h of exposure, whereas gill glutathione S‐transferases activity was significantly inhibited at all the exposure periods, suggesting a direct or indirect effect of the toxicant on these enzymes. Inhibition of lactate dehydrogenases activity was only observed after 96 h of exposure to 25 μg/L of benzo[a]pyrene. No significant effects were observed on acetylcholinesterase activity, suggesting that cholinergic function of S. aurata is not affected by benzo[a]pyrene. In a second phase, fish were exposed for 240 h to sediments collected at five sites of the Sado River estuary, and the same biomarkers were analyzed. For all the enzymes assayed, significant differences among sites were found. In this study, the battery of biomarkers used allowed to discrimination among sites with different types of contamination, levels of contamination, or both, after multivariate data analysis. Discrimination of sites was similar to the ranking provided by a more complex and parallel study (including chemical analysis of sediments, macrobenthic community analysis, amphipod mortality toxicity tests, and sea urchin abnormality embryo assays), suggesting its suitability to evaluate the toxicity of estuarine sediments.

[1]  S. Fukushima,et al.  Low dose DDT inhibition of hepatocarcinogenesis initiated by diethylnitrosamine in male rats: possible mechanisms. , 2005, Toxicology and applied pharmacology.

[2]  M. Costa,et al.  Acute marine sediment toxicity: a potential new test with the amphipod Gammarus locusta. , 1998, Ecotoxicology and environmental safety.

[3]  S. Moreira,et al.  The ‘Coral Bulker’ Fuel Oil Spill on the North Coast of Portugal: Spatial and Temporal Biomarker Responses in Mytilus galloprovincialis , 2004, Ecotoxicology.

[4]  Jonathan A Roling,et al.  Alterations in hepatic gene expression by trivalent chromium in Fundulus heteroclitus. , 2006, Marine environmental research.

[5]  A. Soares,et al.  In vivo evaluation of three biomarkers in the mosquitofish (Gambusia yucatana) exposed to pesticides. , 2005, Chemosphere.

[6]  S. Shukla,et al.  Impact of endosulfan on lactate dehydrogenase from the freshwater catfish Clarias batrachus , 1997 .

[7]  J. Girard,et al.  The nitroxide stable radical tempo prevents metal-induced inhibition of CYP1A1 expression and induction. , 2000, Toxicology letters.

[8]  J. Zelikoff,et al.  Benzo[a]pyrene-induced immunotoxicity in Japanese medaka (Oryzias latipes): relationship between lymphoid CYP1A activity and humoral immune suppression. , 2004, Toxicology and applied pharmacology.

[9]  J. Pedrajas,et al.  Oxidative stress in fish exposed to model xenobiotics. Oxidatively modified forms of Cu,Zn-superoxide dismutase as potential biomarkers. , 1995, Chemico-biological interactions.

[10]  W B Jakoby,et al.  Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. , 1974, The Journal of biological chemistry.

[11]  Rui Ribeiro,et al.  In situ bioassay chambers and procedures for assessment of sediment toxicity with Chironomus riparius. , 2003, Environmental pollution.

[12]  B. Ketterer,et al.  The organization of the human GSTP1-1 gene promoter and its response to retinoic acid and cellular redox status. , 1996, The Biochemical journal.

[13]  D. Nugegoda,et al.  Metabolic responses of fish following exposure to two different oil spill remediation techniques. , 2001, Ecotoxicology and environmental safety.

[14]  P. Verma,et al.  Pathway-specific response to cortisol in the metabolism of catfish. , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[15]  M. Pacheco,et al.  Sparus aurata L. liver EROD and GST activities, plasma cortisol, lactate, glucose and erythrocytic nuclear anomalies following short-term exposure either to 17beta-estradiol (E2) or E2 combined with 4-nonylphenol. , 2005, The Science of the total environment.

[16]  S. Caeiro.  Environmental data management in the Sado Estuary , 2004 .

[17]  A. Carvalho,et al.  Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia magna. , 1996, Chemosphere.

[18]  Xiuxian Song,et al.  Response of integrated biomarkers of fish (Lateolabrax japonicus) exposed to benzo[a]pyrene and sodium dodecylbenzene sulfonate. , 2006, Ecotoxicology and environmental safety.

[19]  P. Geraldine,et al.  Alterations in concentrations of protein, carbohydrate, glycogen, free sugar, and lipid in the prawn Macrobrachium malcolmsonii on exposure to sublethal concentrations of endosulfan , 1997 .

[20]  A. Nogueira,et al.  In vitro and in vivo inhibition of Daphnia magna acetylcholinesterase by surfactant agents: possible implications for contamination biomonitoring. , 2000, The Science of the total environment.

[21]  L. Guilhermino,et al.  Characterization of cholinesterase from guppy (Poecilia reticulata) muscle and its in vitro inhibition by environmental contaminants , 2000, Biomarkers : biochemical indicators of exposure, response, and susceptibility to chemicals.

[22]  M. Chatterjee,et al.  Cadmium-induced alterations of hepatic lipid peroxidation, glutathione S-transferase activity and reduced glutathione level and their possible correlation with chromosomal aberration in mice: a time course study. , 1998, Mutation research.

[23]  A. Soares,et al.  Should the use of inhibition of cholinesterases as a specific biomarker for organophosphate and carbamate pesticides be questioned , 1998 .

[24]  D. Livingstone,et al.  Responses of hepatic cytochrome P450 1A and formation of DNA-adducts in juveniles of turbot (Scophthalmus maximus L.) exposed to water-borne benzo[a]pyrene , 1997 .

[25]  A. Barchowsky,et al.  Inhibition of NF-kappa B binding to DNA by chromium, cadmium, mercury, zinc, and arsenite in vitro: evidence of a thiol mechanism. , 1998, Archives of biochemistry and biophysics.

[26]  D. Phillips,et al.  Correlative changes in metabolism and DNA damage in turbot (Scophthalmus maximus) exposed to benzo[a]pyrene. , 2002, Marine environmental research.

[27]  F. Carvalho,et al.  Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity , 2005, Biomarkers : biochemical indicators of exposure, response, and susceptibility to chemicals.

[28]  D. Webb,et al.  Metabolic enzyme activities in black bream (Acanthopagrus butcheri) from the Swan-Canning Estuary, Western Australia. , 2005, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[29]  A. Salvetti,et al.  Effects of β-naphthoflavone on the cytochrome P450 system, and phase II enzymes in gilthead seabream (Sparus aurata) , 2001 .

[30]  O. Sugita,et al.  [Lactate dehydrogenase]. , 1984, Rinsho byori. The Japanese journal of clinical pathology.

[31]  L. Gladden.  Lactate metabolism: a new paradigm for the third millennium , 2004, The Journal of physiology.

[32]  R. Caricato,et al.  Integrated use of biomarkers (acetylcholinesterase and antioxidant enzymes activities) in Mytilus galloprovincialis and Mullus barbatus in an Italian coastal marine area. , 2003, Marine pollution bulletin.

[33]  P. Dehn,et al.  Organochlorine insecticides: impacts on human HepG2 cytochrome P4501A, 2B activities and glutathione levels. , 2005, Toxicology in vitro : an international journal published in association with BIBRA.

[34]  S. De Flora,et al.  Enhanced liver metabolism of mutagens and carcinogens in fish living in polluted seawater. , 1991, Mutation research.

[35]  R. S. Dwivedi.  Lead exposure alters the drug metabolic activity and the homeostasis of essential metal ions in the lenticular system of the rat. , 1996, Environmental pollution.

[36]  L. Guilhermino,et al.  Sea-urchin (Paracentrotus lividus) glutathione S-transferases and cholinesterase activities as biomarkers of environmental contamination. , 2005, Journal of environmental monitoring : JEM.

[37]  T. Diamantino,et al.  Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. , 2001, Chemosphere.

[38]  M J Leaver,et al.  Structure and expression of a cluster of glutathione S-transferase genes from a marine fish, the plaice (Pleuronectes platessa). , 1997, The Biochemical journal.

[39]  R. Darlington,et al.  Factor Analysis , 2008 .

[40]  V. Talesa,et al.  Different activity of glyoxalase system enzymes in specimens of Sparus auratus exposed to sublethal copper concentrations. , 2003, Chemico-biological interactions.

[41]  K. Courtney,et al.  A new and rapid colorimetric determination of acetylcholinesterase activity. , 1961, Biochemical pharmacology.

[42]  Donald D. MacDonald,et al.  Recommended Uses of Empirically Derived, Sediment Quality Guidelines for Marine and Estuarine Ecosystems , 1998 .

[43]  T. Diamantino,et al.  Characterization of Cholinesterases from Daphnia magna Straus and Their Inhibition by Zinc , 2003, Bulletin of environmental contamination and toxicology.

[44]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[45]  E. Giovannini,et al.  Increased acetylcholinesterase activities in specimens of Sparus auratus exposed to sublethal copper concentrations. , 2003, Chemico-biological interactions.