Volume 15, Issue 3 - September 2015


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Revista de Gestão Costeira Integrada
Volume 15, Número 3, Setembro 2015, Páginas 371-376

DOI: 10.5894/rgci594
* Submission: 13 MAR 2015; Peer review: 16 APR 2015; Revised: 29 APR 2015; Accepted: 5 MAY 2015; Available on-line: 6 MAY 2015

Biomarkers responses in different body regions of the polychaeta Hediste diversicolor (Nereidae, Polychaete) exposed to copper *  

Z. Bouraoui@,a; J. Ghediraa; H. Boussettaa

@ Corresponding author, to whom correspondence should be addressed: <[email protected]>
a University of Sousse, Laboratory of Biochemistry and Environmental Toxicology, I.S.A. Chott-Mariem, 4042, Tunisia. Phone: 00 216 73 327 544. Fax: 00 216 73 327 591   

This study aims to evaluate the effects of exposure to 1 μM of copper during a period of test of 48 h, on enzymatic and lipid peroxidation biomarkers in anterior (A), middle (M) and posterior (P) body regions of the polychaeta (Nereididae) Hediste diversicolor. The biomarkers selected in this work were the NADPH cytochrome c reductase (NADPH red) as phase I biotransformation enzyme, glutathione-S-transferase (GST) as phase II enzyme, and the oxidative stress markers using catalase activity (CAT) and malondialdehyde accumulation (MDA). The NADPH red activity was not significantly affected by copper exposure in the different body regions. Glutathione-S-transferase (GST) was significantly augmented (p< 0.05) only in the A region of Cu group compared to control group. The higher and significant CAT activity (p< 0.05) was noted in the P region of treated group paralleled by a lack of MDA production in the same region. A higher MDA content was observed in A region compared with the same body region of treated worm supporting the idea of a highest oxidant condition in this region. 

Keywords: Copper, NADPH cytochrome c reductase,  glutathione-S-transferase, catalase, Hediste diversicolor.

Resposta de Biomarcadores em Hediste diversicolor (Nereidae, Polychaete): Efeitos da exposição ao Cobre

Com este trabalho pretende-se estudar a exposição ao cobre (1 μM) em testes de 48 h, com biomarcadores enzimáticos e de peroxidação lipídica nas regiões corporais anterior (A), mediana (M) e posterior (P) no poliqueta (Nereididae) Hediste diversicolor. Os biomarcadores selecionados para este estudo foram NADPH cytochrome c reductase (NADPH red) como enzimas biotransformadoras nas reações de fase I, glutathione-S-transferase (GST) como enzima da fase II, e os marcadores do stress oxidativo usando a atividade da enzima antioxidante catalase (CAT) e a acumulação de malondialdehyde (MDA). A atividade do NADPH não foi significativamente afetada pela exposição ao cobre nas diferentes regiões do corpo do poliqueta. Glutathione- S-transferase (GST) aumentou significativamente (p< 0.05) na região A comparativamente com o grupo controle. A maior e significativa atividade de CAT (p< 0.05) foi registada na região P paralelamente à ausência de produção de MDA nessa mesma região. Maiores concentrações de MDA foram registadas na região A evidenciando uma maior condição de stress oxidativo nessa região.   

Palavras-chave: Cobre, NADPH cytochrome c reductase, glutathione-S-transferase, catalase, Hediste diversicolor


Ait Alla, A.; Mouneyrac, C.; Durou, C.; Moukrim, A.; Pellerin, J. (2006) - Tolerance and biomarkers as useful tools for assessing environmental quality in the Oued Souss estuary (Bay of Agadir, Morocco). Comparative Biochemistry and Physiology C: Toxicology & Pharmacology, 143(1):23-29. DOI: 10.1016/j.cbpc.2005.11.015

Alexandrova, M.L.; Bochev, P.G. (2005) - Oxidative stress during the chronic phase after stroke. Free Radical Biology & Medicine, 39(3):297–316. DOI: 10.1179/135100003225001548

Arun, S.; Subramanian, P. (2003) - Cytochrome P450 and other
biotransformation activity in aquatic organisms: potential biomarkers
to environmental pollution. In: Tripathi, G., Kumar, A. (eds.), Potentials of Living Resources, pp.459–488, Discovery Publishers, New Delhi, India. ISBN: 978-8171417186.

Banni, M.; Jebal,, J.; Daubeze, M.; Clerendeau, C.; Guerbej, H.; Narbonne, J.F.; Boussetta, H. (2005) - Monitoring Pollution in Tunisian coasts: Application of a classification scale based on biochemical markers. Biomarkers, 10(2-3):105-116.
DOI: 10.1080/13547500500107497

Banni, M.; Dondero, F.; Jebali, J.; Guerbej, H.; Boussetta, H.; Viarengo,
A. (2007) - Assessment of heavy metal contamination using real time PCR analysis of mussel metallothionein mt10 and mt20 expression: avalidation along the Tunisian coasts. Biomarkers, 12(4):369–383.
DOI: 10.1080/13547500701217061

Banni, M.; Bouraoui, Z.; Clerandeau, C.; Narbonne, J.F.; Boussetta, H. (2009) - Mixture toxicity assessment of cadmium and benzo[a]pyrene in the sea worm Hediste diversicolor. Chemosphere, 77(7):902–906.
DOI: 10.1016/j.chemosphere.2009.08.041

Ben-Khedher, S.; Jebali, J.; Houas, Z.; Nawéli, H.; Jrad, A.; Banni, M.; Boussetta, H. (2014) - Metals bioaccumulation and histopathological
biomarkers in Carcinus maenas crab from Bizerta lagoon, Tunisia. Environmental Science and Pollution Research, 21(6):4343-4357.
DOI: 10.1007/s11356-013-2399-x

Bouraoui, Z.; Banni, M.; Ghedira, J.; Clerandeau, C.; Narbonne, JF.;
Boussetta, H. (2009) - Evaluation of enzymatic biomarkers and
lipoperoxidation level in Hediste diversicolor exposed to copper and benzo[a]pyrene. Ecotoxicology and Environmental Safety, 72(7):1893-1898. DOI: 10.1016/j.ecoenv.2009.05.011

Bouraoui, Z.; Banni, M.; Chouba, L.; Ghedira, J.; Clerandeau, C.; Jebali, J.; Narbonne, J.F.; Boussetta, H. (2010) - Monitoring pollution in Tunisian coasts using a scale of classification based on biochemical markers in worm Nereis (Hediste) diversicolor. Environmental Monitoring and Assessment, 164(1-4):691-700. DOI: 10.1007/s10661-009-0921-x

Bouraoui, Z.; Ghedira, J.; Capri, F.; Chouba, L.; Boussetta, H. (2014) - Cytochemical responses of Hediste diversicolor (Nereidae, Polychaete) sampled from polluted sites along the Tunisian coast. Revista de Gestão Costeira / Journal of Integrated Coastal Zone Management, 14(1):119-127. DOI: 10.5894/rgci480

Bradford, M. (1976). A rapid and sensitive method for the quantification
of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry. 72(1-2):248-254.
DOI: 10.1016/0003-2697(76)90527-3

Buege, J.A.; Aust, S.D. (1978) - Microsomal lipid peroxidation. In: Packer, L. (Ed.), Methods in Enzymology, 52:302–310.
DOI: 10.1016/S0076-6879(78)52032-6

Buffet, P.E.; Poirier, L.; Zalouk-Vergnoux, A.; Lopes, C.; Amiard, J.C.; Gaudin, P.; Risso-de Faverney, C.; Guibbolini, M.; Gilliland, D.; Perrein-Ettajani, H.; Valsami-Jones, E.; Mouneyrac, C. (2014) - Biochemical and behavioural responses of the marine polychaete Hediste diversicolor to cadmium sulfide quantum dots (CdS QDs): Waterborne and dietary exposure. Chemosphere, 100:63–70.
DOI: 10.1016/j.chemosphere.2013.12.069

Caldwell, G.S.; Lewis, C.; Pickavance, G.; Taylor, R.L.; Bentley, M.G. (2011) - Exposure to copper and cytotoxic polyunsaturated aldehyde induces reproductive failure in the marine polychaete Nereis virens (Sars). Aquatic Toxicology, 104(1-2):126–134.
DOI: 10.1016/j.aquatox.2011.03.018

Catalano, B.; Moltedo, G.; Martuccio, G.; Gastaldi, L.; Virno-Lambert, C.; Lauria, L.; Ausili A. (2012) - Can Hediste diversicolor (Nereidae, Polychaete) be considered a good candidate in evaluating PAH contamination? A multimarker approach. Chemosphere, 86(9):875-882. DOI: 10.1016/j.chemosphere.2011.10.040

Carvalho, A.N.; Lino Vaz, A.S.; Boto Sérgio, T.I.; Talhadas dos Santos, P.J. (2013) - Sustainability of bait fishing harvesting in estuarine ecosystems - Case study in the Local Natural Reserve of Douro Estuary, Portugal. Revista de Gestão Costeira Integrada / Journal of Integrated Coastal Zone Management, 13(2):157-168. DOI: 10.5894/rgci393

Christensen, M.; Andersen, O.; Banta, G. (2002) - Metabolism of pyrene by the polychaetes Nereis diversicolor and Arenicola marina. Aquatic Toxicology. 58(1-2):15-25. DOI: 10.1016/S0166-445X(01)00217-X

Claiborne, A. (1985) - Catalase activity. In: Robert A. Greenwald (ed.), CRC Handbook of Methods in Oxygen Radical Research, pp.283–294, CRC Press, Florida, U.S.A. ISBN: 978-0849329364

Durou, C.; Poirier, L.; Amiard, J.C.; Budzinski, H.; Gnassia-Barelli, M.; Lemenach, K.; Peluhet, L.; Mouneyrac, C.; Romeo, M.; Amiard-Triquet, C. (2007) - Biomonitoring in a clean and a multi-contaminated estuary based on biomarkers and chemical analyses in the endobenthic worm Nereis diversicolor. Environmental Pollution, 148(2):445-458.
DOI: 10.1016/j.envpol.2006.12.022

Eriksen, K.D.H.; Daae H.L.; Andersen, R.A. (1988) - Evidence of presence of heavy metal-binding proteins in polychaete species. Comparative Biochemistry and Physiology, Part C: Comparative Pharmacology, 91(2):377–384. DOI: 10.1016/0742-8413(88)90045-X

Ferreira-Cravo, M.; Ventura-Lima, J.; Sandrini, J.Z.; Amado, L.L.; Geracitano, L.A.; Rebelo, M.; Bianchini, A.; Monserrat, J.M. (2009) - Antioxidant responses in different body regions of the polychaeta Laeonereis acuta (Nereididae) exposed to copper. Ecotoxicology and Environmental Safety, 72(2):388–393.
DOI: 10.1016/j.ecoenv.2008.07.003

Guidia, P.; Frenzilli, G.; Benedettib, M.; Bernardeschia, M.; Falleni, A.; Fattorini, D.; Regoli, F.; Scarcelli, V.; Nigro, M. (2010) - Antioxidant, genotoxic and lysosomal biomarkers in the freshwater bivalve (Unio pictorum) transplanted in a metal polluted river basin. Aquatic Toxicology, 100(1):75-83. DOI: 10.1016/j.aquatox.2010.07.009

Gastaldi, L.; Ranzato, E.; Capri, F.; Hankard, P.;, Peres, G.; Canesi, L.; Viarengo, A.; Pons, G. (2007) - Application of a biomarker battery for the evaluation of the sublethal effects of pollutants in the earthworm Eisenia andrei. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 146(3):398-405.
DOI: 10.1016/j.cbpc.2007.04.014

Ghedira, J.; Jebali, J.; Banni M.; Chouba, L, Boussetta, H.; López-Barea, J.; Alhama, J. (2011) - Use of oxidative stress biomarker sin Carcinus maenas to assess littoral zone contamination in Tunisia. Aquatic Biology, 14(1):87–98. DOI: 10.3354/ab00377

Hankard, P.K.; Svendsen, C.; Wright, J.; Wienberg, C.; Fishwick, S.K.; Spurgeon, D.J. (2004) - Biological assessment of contaminated land using earthworm biomarkers in support of chemical analysis. Science of The Total Environment, 330(1-3):9-20.
DOI: 10.1016/j.scitotenv.2003.08.023

Habig, W.H.; Pabst, M.J.; Jakoby, W.B. (1974) - Glutathione  Stransferases, the first step in mercapturic acid formation. Journal
of Biological Chemistry, 249(22):7130-7139, American Society of Biological Chemists (ISSN: 0021-9258), Rockville, MD, U.S.A. Available on-line at

Hayes, AW. (1982) - Principles and Methods of Toxicology. 750p., Raven Press, New York, U.S.A. ISBN: 978-0890044704

Hermes-Lima, M. (2004) - Oxygen in biology and biochemistry: role of free radicals. In: Kenneth B. Storey (ed.), Functional Metabolism: Regulation and Adaptation, pp.319–368, Wiley, New York, NY, U.S.A. ISBN: 978-0471410904 DOI: 10.1002/047167558X.ch12

Jebali, J.; Banni, M.; Alves de Almeida, E.; Boussetta, H. (2007) -
Oxidative DNA damage levels in the clams Ruditapes decussatus
as pollution biomarkers of Tunisian marine environment.
Environmental Monitoring and Assessment, 124(1-3):195-200.
DOI: 10.1007/s10661-006- 9217-6.

Jebali, J.; Ben Khedher, S.; Sabbagh, M.; Kamel, N.; Banni, M.; Boussetta, H. (2013) - Cholinesterase activity as biomarker of
neurotoxicity: utility in the assessment of aquatic environment
contamination. Revista de Gestão Costeira Integrada / Journal
of Integrated Coastal Zone Management, 13(4):525-537.
DOI: 10.5894/rgci430.

Jebali, J.; Chicano-Gálvez, E.; Fernández-Cisnal, R.; Banni, M.; Chouba, L.; Boussetta H.; Barea, H.L.; Alhama, J. (2014) - Proteomic analysis in caged Mediterranean crab (Carcinus maenas) and chemical contaminant exposure in Téboulba Harbour. Tunisia. Ecotoxicology and Environmental Safety, 100:15–26. DOI: 10.1016/j.ecoenv.2013.11.025

Lucan-Bouché, M.L.; Biagianti-Risbourg, S.; Arsac, F.; Vernet, G.; (1999) - An original decontamination process developed by aquatic oligochaete Tubifex tubifex exposed to copper and lead. Aquatic Toxicology, 45(1):9-17. DOI: 10.1016/S0166-445X(98)00091-5

Marcano, L.; Nusetti, O.; Rodrıguez-Grau, J.; Vilas, J. (1996) - Uptake and depuration of copper and zinc in relation to metalbinding protein in the polychaete Eurythoe complanata. Comparative Biochemistry and Physiology, Part C: Pharmacology, Toxicology and Endocrinology, 114(3):179-184. DOI: 10.1016/0742-8413(96)00016-3

Moreira, S.M.; Moreira-Santos, M.; Guilhermino, L.; Ribeiro, R. (2005)- A short-term sublethal in situ toxicity assay with Hediste diversicolor (Polychaeta) for estuarine sediments based on postexposure feeding. Environmental Toxicology and Chemistry, 24(8): 2010-2018.
DOI: 10.1897/04-473R1.1

Moschino, V.; Nestoa, N.; Barisonb, S.; Agresti, F.; Colla, L.; Fedele, L.; Da Ros, L. (2014) - A preliminary investigation on nanohorn toxicity in marine mussels and polychaetes. Science of the Total Environment, 468-469:111-119. DOI: 10.1016/j.scitotenv.2013.08.020.

Rainbow, P.S.; Smith, B.D. (2013) - Accumulation and detoxification of copper and zinc by the decapods crustacean Palaemonetes varians from diets of field-contaminated polychaetes Nereis diversicolor. Journal of Experimental Marine Biology and Ecology, 449:312-320.
DOI: 10.1016/j.jembe.2013.09.022

Rosa, C.E.; Iurman, M.G.; Abreu, P.C.; Geracitano, L.A.; Monserrat, J.M..(2005) - Antioxidant mechanisms of the nereidid Laeonereis acuta (Annelida: Polychaeta) to cope with environmental hydrogen peroxide. Physiological and Biochemical Zoology, 78(4):641–649.
DOI: 10.1086/430229


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