Assessment of trace element accumulation on the Tunisian coasts using biochemical biomarkers in Perinereis cultrifera

Marwa  Bouhedi; Mouna  Antit; Marwa  Chaibi; Hanane  Perrein-Ettajani; Patrick  Gillet; Atf  Azzouna

doi:10.3989/scimar.05099.009

Authors

Marwa Bouhedi Laboratory of Ecology, Biology and Physiology of Aquatic Organisms, Department of Biology, Faculty of Sciences of Tunis, University of Tunis https://orcid.org/0000-0002-2705-7483
Mouna Antit Laboratory of Ecology, Biology and Physiology of Aquatic Organisms, Department of Biology, Faculty of Sciences of Tunis, University of Tunis https://orcid.org/0000-0002-0420-7119
Marwa Chaibi Laboratory of Ecology, Biology and Physiology of Aquatic Organisms, Department of Biology, Faculty of Sciences of Tunis, University of Tunis https://orcid.org/0000-0001-5958-4213
Hanane Perrein-Ettajani Mer Molécules Santé, Department of Biology Environment, Faculty of Sciences, UCO Angers https://orcid.org/0000-0002-4195-3137
Patrick Gillet Mer Molécules Santé, Department of Biology Environment, Faculty of Sciences, UCO Angers https://orcid.org/0000-0002-7183-9685
Atf Azzouna Laboratory of Ecology, Biology and Physiology of Aquatic Organisms, Department of Biology, Faculty of Sciences of Tunis, University of Tunis https://orcid.org/0000-0002-5606-5239

DOI:

https://doi.org/10.3989/scimar.05099.009

Keywords:

polychaete, coastal pollution, Gulf of Tunis, oxidative stress, environmental conditions, metallic pollution

Abstract

Our study aimed to evaluate the effect of trace element pollution in the polychaete Perinereis cultrifera (Grube, 1840) from two Tunisian coasts (the port of Rades, S1; and the Punic port of Carthage, S2). To this end, we used an approach based on proximate composition, biomarker responses and trace element bioaccumulation. Our results showed a decreasing order of metals concentrations (Zn>Cu>Cd>Pb) in P. cultrifera from S1 and S2. The accumulation of Cd, Cu and Zn was significantly higher in S1 than in S2, especially in summer. Lipid, protein and glycogen content also changed significantly between S1 and S2 in relation to trace metal accumulation and environmental conditions. The results revealed a higher level of thiobarbituric acid in P. cultrifera from S1 than from S2. In addition, the enzymatic and non-enzymatic antioxidant defence system (catalase, glutathione-S-transferase, superoxide dismutase, glutathione and metallothionein) was enhanced and acetylcholinesterase activities decreased in P. cultrifera in S1 in comparison with S2. A principal component analysis showed that P. cultrifera from S1 exhibited a clear disruption of oxidative stress responses and trace element bioaccumulation among seasons. Overall, these findings revealed the sensitivity of those organisms to environmental conditions.

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References

Aebi H. 1984. Catalase in Vitro. Method. Enzymol. 105: 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3

Aissaoui A., Dhib A., Reguera B., et al. 2014. First evidence of cell deformation occurrence during a Dinophysis bloom along the shores of the Gulf of Tunis (SW Mediterranean Sea). Harmful Algae 39: 191-201. https://doi.org/10.1016/j.hal.2014.07.017

Ait Alla A., Mouneyrac C., Durou C., et al. 2006. Tolerance and biomarkers as useful tools for assessing environmental quality in the Oued Souss estuary (Bay of Agadir, Morocco). Comp. Biochem. Phys. C. 143: 23-29. https://doi.org/10.1016/j.cbpc.2005.11.015 PMid:16413830

Aminot A., Chaussepied C. 1983. Manuel des analyses chimiques en milieu marin. Centre National d'Exploitation des Oc.ans, Brest, 395 pp.

Antit M. 2012. Caract.risation des communaut.s des Mollusques dans des milieux littoraux de la baie de Tunis, Th.se de Doctorat, Facult. des Sciences de Tunis, 396 pp.

Bat L., Şahin F., .ztekin A. 2019. Assessment of heavy metals pollution in water and sediments and Polychaetes in Sinop shores of the Black Sea. KS. Tarım ve Doğa Derg. 22: 806-816. https://doi.org/10.18016/ksutarimdoga.v22i45606.535882

Beauchamp C., Fridovich I. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44: 276-277. https://doi.org/10.1016/0003-2697(71)90370-8

Bejaoui S., Boussoufa D., Tir M., et al. 2017. DNA damage and oxidative stress in digestive gland of Venerupis decussata collected from two contrasting habitats in the southern Tunisian coast: biochemical and histopathological studies. Cah. Biol. Mar. 58: 123-135.

Bejaoui S., Fouzai C., Trabelsi W., et al. 2019. Evaluation of lead chloride toxicity on lipid profile in Venus verrucosa gills. Int. J. E. Res. 13: 793-800. https://doi.org/10.1007/s41742-019-00218-4

Bejaoui S., Michan C., Telahigue K., et al. 2020. Metal body burden and tissue oxidative status in the bivalve Venerupis decussata from Tunisian coastal lagoons. Mar. Environ. Res. 159: 105000. https://doi.org/10.1016/j.marenvres.2020.105000 PMid:32662434

Bodin N., N'Gom K. R., Le Loc'h F., et al. 2011. Are exploited mangrove molluscs exposed to Persistent Organic Pollutant contamination in Senegal, West Africa? Chemosphere. 84: 318-327. https://doi.org/10.1016/j.chemosphere.2011.04.012 PMid:21550627

Bouki E., Dimitriadis V.K., Kaloyianni M., et al. 2013. Antioxidant and pro-oxidant challenge of tannic acid in mussel hemocytes exposed to cadmium. Mar. Environ. Res. 85: 591-604. https://doi.org/10.1016/j.marenvres.2012.12.005 PMid:23375356

Bradford M. 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Campillo J.A., Albentosa M.N., Valdes J., et al. 2013. Impact assessment of agricultural inputs into a Mediterranean coastal lagoon (Mar Menor, SE Spain) on transplanted clams (Ruditapes decussatus) by biochemical and physiological responses. Aquat. Toxicol. 142-143: 365-379. https://doi.org/10.1016/j.aquatox.2013.09.012 PMid:24095956

Carr R.S., Neff J.M. 1984. Quantitative semi-automated enzymatic assay for tissue glycogen. Comp. Biochem. Phys. B. 77: 447-449. https://doi.org/10.1016/0305-0491(84)90258-X

Carregosa V., Velez C., Soares A.M.V.M., et al. 2014. Physiological and biochemical responses of three Veneridae clams exposed to salinity changes. Comp. Biochem. Phys. B. 177-178: 1-9. https://doi.org/10.1016/j.cbpb.2014.08.001 PMid:25132624

Cataldo J., Hidalgo M.E., Neaman A., et al. 2011. Use of molecular biomarkers in Eisenia foetida to assess copper toxicity in agricultural soils affected by mining activities. J. Soil. Sci. Plant. Nut.11: 57-70.

Chance B., Sies H., Boveris A. 1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59: 527-605. https://doi.org/10.1152/physrev.1979.59.3.527 PMid:37532

Chetoui I., Bejaoui S., Trabelsi W., et al. 2019. Exposure of Mactra corallina to acute doses of lead: effects on redox status, fatty acid composition and histomorphological aspect. Drug Chem. Toxicol. https://doi.org/10.1080/01480545.2019.1693590 PMid:31752645

Chouikh N., Gillet P., Langston W.J., et al. 2019. First investigation of the composition and spatial distribution of polychaete feeding guilds from Essaouira protected coastal area. Appl. Ecol. Env. Res. 17: 3231-3249. https://doi.org/10.15666/aeer/1702_32313249

Cravo A., Pereira C., Gomes T., et al. 2012. A multibiomarker approach in the clam Ruditapes decussatus to assess the impact of pollution in the Ria Formosa lagoon, South Coast of Portugal. Mar. Environ. Res. 75: 23-34. https://doi.org/10.1016/j.marenvres.2011.09.012 PMid:22001190

Das D., Moniruzzaman M., Sarbajna A., et al. 2017. Effect of heavy metals on tissue-specific antioxidant response in Indian major carps. Environ. Sci. Pollu. Res. 24: 18010-18024. https://doi.org/10.1007/s11356-017-9415-5 PMid:28624940

Di Salvatore P., Calcagno J.A., Ort.z N., et al. 2013. Effect of seasonality on oxidative stress responses and metal accumulation in soft tissues of Aulacomya atra, a mussel from the South Atlantic Patagonian coast. Mar. Environ. Res. 92: 244-252. https://doi.org/10.1016/j.marenvres.2013.10.004 PMid:24157268

Douhri H., Sayah F. 2009. The use of enzymatic biomarkers in two marine invertebrates Nereis diversicolor and Patella vulgata for the biomonitoring of Tangier's bay (Morocco). Ecotox. Environ. Safe. 72: 394-399. https://doi.org/10.1016/j.ecoenv.2008.07.016 PMid:18786724

Durchon M. 1957. Probl.mes pos.s par le comportement des n.r.idiens au moment de leur reproduction. Ann. Biol. 33: 31-42.

Durou C., Smith B.D., Romeo M., et al. 2007. From biomarkers to population responses in Nereis diversicolor: Assessment of stress in estuarine ecosystems. Ecotox. Environ. Safe. 66: 402-411. https://doi.org/10.1016/j.ecoenv.2006.02.016 PMid:16620980

Ellman G.L. 1959. Tissue sulhydryl groups. Arch. Biochem. Biophys. 82: 70-77. https://doi.org/10.1016/0003-9861(59)90090-6

Ellman G.L., Courtney K.D., Andres V., et al. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol.7: 88-95. https://doi.org/10.1016/0006-2952(61)90145-9

Freitas R., Ramos Pinto L., Sampaio M., et al. 2012. Effects of depuration on the element concentration in bivalves: Comparison between sympatric Ruditapes decussates and Ruditapes philippinarum. Estuar. Coast. Shelf Sci. 110: 43-53. https://doi.org/10.1016/j.ecss.2012.01.011

Freitas R., Pires A., Velez C., et al. 2015. The effects of salinity changes on the Polychaete Diopatra neapolitana: impacts on regenerative capacity and biochemical markers. Aquat. Toxicol.163: 167-176. https://doi.org/10.1016/j.aquatox.2015.04.006 PMid:25911382

Frings C.S., Fendley T.W., Dunn R.T., et al. 1972. Improved determination of total serum lipids by the sulfo-phospho- vanillin reaction. Clin. Chem. 18: 673-674. https://doi.org/10.1093/clinchem/18.7.673 PMid:5037917

Gaete H., .lvarez M., Lobos G., et al. 2017. Assessment of oxidative stress and bioaccumulation of the metals Cu, Fe, Zn, Pb, Cd in the polychaete Perinereis gualpensis from estuaries of central Chile. Ecotox. Environ. Safe.145: 653-658. https://doi.org/10.1016/j.ecoenv.2017.07.073 PMid:28822345

Ghirardini V.A., Cavallini L., Delaney E., et al. 1999. H. diversicolor, N. succinea and P. cultrifera (Polychaeta: Nereididae) as bioaccumulators of cadmium and zinc from sediments: Preliminary results in the Venetian lagoon (Italy). Toxicol. Environ. Chem. 71: 457-474. https://doi.org/10.1080/02772249909358815

Gomes T., Gonzalez-Rey M., Rodriguez-Romero A., et al. 2013. Biomarkers in Nereis diversicolor (Polychaeta: Nereididae) as management tools for environmental assessment on the southwest Iberian coast. Sci. Mar. 77S1: 69-78. https://doi.org/10.3989/scimar.03731.27F

Grube E. 1840. Actinien, Echinodermen und Würmer des Adriatischen und Mittlemeers. K.nisberg, 1840, 92 pp.

Guemouda M., Meghlaoui Z., Daas T., et al. 2014. Monitoring pollution in East Algerian coasts using biochemical markers in the polychaete annelid Perinereis cultrifera. Ann. Biol. Res. 5: 31-40.

Habig W.H., Pabst M.J., Jakoby W.B. 1974. Glutathione S-transferases, the first enzymatic stepin mercapturic acid formation. J. Biol. Chem. 249: 7130-7139. https://doi.org/10.1016/S0021-9258(19)42083-8

Halliwell B. 2007. Biochemistry of oxidative stress. Biochem. Soc. T. 35: 1147-1150. https://doi.org/10.1042/BST0351147 PMid:17956298

Han Q., Jiang X., Wang X. 2016. The polychaete feeding guild composition in the Sishili Bay, the northern Yellow Sea, China. J. Mar. Biol. Assoc. UK. 96: 1083-1092. https://doi.org/10.1017/S0025315415001873

Jebali J., Banni M., Alves de Almeida E., et al. 2007. Oxidative DNA damage levels clam Ruditapes decussatus as pollution biomarkers of Tunisian marine environment. Environ. Monit. Assess. 124: 195-200. https://doi.org/10.1007/s10661-006-9217-6 PMid:16897518

Jollow D.J., Mitchell J.R., Zampaglione N., et al. 1974. Bromobenzene- induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11: 151-169. https://doi.org/10.1159/000136485 PMid:4831804

King C.K., Dowse M.C., Simpson S.L., et al. 2004. An assessment of five Australian polychaetes and bivalves for use in whole-sediment toxicity tests: toxicity and accumulation of copper and zinc from water and sediment. Arch. Environ. Con. Toxicol. 47: 314-323. https://doi.org/10.1007/s00244-004-3122-1 PMid:15386125

Knight J.A., Pieper R.K., McClellan L. 1988. Specificity of the thiobarbituric acid reaction: its use in studies of lipid peroxidation. Clin. Chem. 34: 2433-2438. https://doi.org/10.1093/clinchem/34.12.2433 PMid:3197281

Li L., Liu X., You L., et al. 2012. Uptake pathways and subcellular fractionation of Cd in the polychaete Nereis diversicolor. Ecotoxicology 21:104. https://doi.org/10.1007/s10646-011-0770-6 PMid:21858512

Lodish H., Berk A., Zipursky S.L., et al. 2000. Molecular Cell Biology. 4th edition. New York: W. H. freeman.

Lv L., Dong X., Lv F., et al. 2016.Antioxidant enzymes responses of polychaete Perinereis aibuhitensis following chronic exposure to 17β-estradiol. Ital. J. Anim. Sci. 15: 552-557. https://doi.org/10.1080/1828051X.2016.1194172

Ma X., Deng D., Chen W. 2017. Inhibitors and Activators of SOD, GSH-Px, and CAT. In: Sentürk M. (ed.), Enzyme Inhibitors and Activators, Intech. Open. https://doi.org/10.5772/65936

Meghlaoui Z., Guemouda M., Snani M., et al. 2015. Effect of oil pollution on polychaete annelids in the Algerian East coast. J. Entomol. Zool. Stud. 3: 339-343.

Michel X., Narbonne J.F., Mora P., et al. 1998. Utilisation de biomarqueurs pour la surveillance de la qualit. de l'environnement. In: Lagadic L., Caquet T., Amiard J.C., et al. (eds), Lavoisier Tec & Doc, Paris, New York, Londres, pp. 9-30.

Moulton W.N., Howard T., Pruett M. 1996. Business Failure Pathways: Environmental Stress and Organizational Response. J. Manage. 22: 571-595. https://doi.org/10.1016/S0149-2063(96)90025-2

Mouneyrac C., Geffard A., Amiard J.C., et al. 2000. Metallothioneinlike proteins in Macoma balthica: effects of metal exposure and natural factors. Can. J. Fish. Aquat. Sci. 57: 34-42. https://doi.org/10.1139/f99-183

Paraskevopoulou V., Zeri C., Kaberi H., et al. 2014. Trace metal variability, background levels and pollution status assessment in line with the water framework and marine strategy framework EU Directives in the waters of a heavily impacted Mediterranean Gulf. Mar. Pollut. Bull. 87: 323-337. https://doi.org/10.1016/j.marpolbul.2014.07.054 PMid:25113102

Petrovic S., Ozretic B., Krajnovic-Ozretic M., et al. 2001. Lysosomal membrane stability and metallothioneins in digestive gland of mussels (Mytilus galloprovincialis Lam.) as biomarkers in afield study. Mar. Pollut. Bull. 42: 1373-1378. https://doi.org/10.1016/S0025-326X(01)00167-9

Rouabah A., Scaps P. 2003. Life cycle and population dynamics of the polychaete Perinereis cultrifera from the Algerian Mediterranean Coast. P.S.Z.N.: Mar. Ecol. 24: 85-99. https://doi.org/10.1046/j.1439-0485.2003.03796.x

Rouhi A., Sif J., Ferssiwi A., et al. 2007. Bioaccumulation de quelques .l.ments m.talliques par deux esp.ces d'Ann.lides Polych.tes du littoral de Jorf Lasfar (r.gion d'El Jadida, Maroc). Bull. Inst. Sci. Rabat. 29: 81-87.

Salinas A.E., Wong M.G. 1999.Glutathione S-transferases-a review. Curr. Med. Chem. 6: 279 309.

Scaps P., Borot O. 2000. Acetylcholinesterase activity of the polychaete Nereis diversicolor: effects of temperature and salinity. Comp. Biochem. Physiol. C. 125: 377-383. https://doi.org/10.1016/S0742-8413(00)00087-6

Scaps P., Reti.re C., Desrosiers G., et al. 1992. Dynamique d'une population de Perinereis cultrifera (Grube) de la c.te nord Bretagne. Cah. Biol. Mar. 33: 477-194.

Snani M., Meghlaoui Z., Maamcha O., et al. 2015. Laying period and biomarkers of the polychaete Perinereis cultrifera from the eastern coast of Algeria subjected to marine pollution. J. Entomol. Zool. Stud. 3: 249-254.

Souissi S., Daly Yahia-K.fi O., Daly Yahia M.N. 2000. Spatial characterization of nutrient dynamics in the Bay of Tunis (south western Mediterranean) using multivariate analyses: consequences for phyto- and zooplankton distribution. J. Plankton Res. 22: 2039-2059. https://doi.org/10.1093/plankt/22.11.2039

Sun F., Zhou Q. 2008. Oxidative stress biomarkers of the polychaete Nereis diversicolor exposed to cadmium and petroleum hydrocarbons. Ecotox. Environ. Safe.70: 106-114. https://doi.org/10.1016/j.ecoenv.2007.04.014 PMid:17673290

Sureda A., Box A., Tejada S., et al. 2011. Biochemical responses of Mytilus galloprovincialis as biomarkers of acute environmental pollution caused by the Don Pedro oil spill (Eivissa Island, Spain). Aquat. Toxicol. 101: 540-549. https://doi.org/10.1016/j.aquatox.2010.12.011 PMid:21276480

Suriya J., Bharathiraja S., Sekar V., et al. 2012. Metallothionein induction and antioxidative responses in the estuarine polychaeta Capitella capitata (Capitellidae). Asian Pac. J. Trop. Biomed. 2: 1052-1059. https://doi.org/10.1016/S2221-1691(12)60360-8

Tlili S., Minguez L., Giamberini L., et al. 2013. Assessment of the health status of Donax trunculus from the Gulf of Tunis using integrative biomarker indices. Ecol. Indic. 32: 285-293. https://doi.org/10.1016/j.ecolind.2013.04.003

Usero J., Morillo J., Gracia I. 2005. Heavy metal concentrations in molluscs from the Atlantic coast of southern Spain. Chemosphere. 59: 1175-1181. https://doi.org/10.1016/j.chemosphere.2004.11.089 PMid:15833492

Viarengo A., Ponzano E., Dondero F., et al. 1997. A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antartic molluscs. Mar. Environ. Res. 44: 69-84. https://doi.org/10.1016/S0141-1136(96)00103-1

Viarengo A., Burlando B., Cavaletto M., et al. 1999. Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am. J. Physiol. 277: 1612-1619. https://doi.org/10.1152/ajpregu.1999.277.6.R1612 PMid:10600906

Wang k., Jiang J., Lei Y., et al. 2019. Targeting Metabolic-Redox Circuits for Cancer Therapy. Trends Biochem. Sci. 44: 5. https://doi.org/10.1016/j.tibs.2019.01.001 PMid:30679131

Won E.J., Raisuddin S., Shin K.H. 2008. Evaluation of induction of metallothionein-like proteins (MTLPs) in the polychaetes for biomonitoring of heavy metal pollution in marine sediments. Mar. Pollut. Bull. 57: 544-551. https://doi.org/10.1016/j.marpolbul.2008.02.025 PMid:18395758

Wu B., Sun R., Yang D. 1985. The Nereidae (Polychaetous annelids) of the Chinese coast. China Ocean Press. Beijing, 234 pp.

Yi Yu-jun., Wang Z., Zhang K., et al. 2008. Sediment pollution and its effect on fish through 531 food chain in the Yangtze River. Int. J. Sediment Res. 23: 338-347. https://doi.org/10.1016/S1001-6279(09)60005-6

Zhao S., Feng C., Wang D., et al. 2013. Salinity increases the mobility of Cd, Cu, Mn, and Pb in the sediments of Yangtze Estuary: relative role of sediments' properties and metal speciation. Chemosphere 91: 977-984. https://doi.org/10.1016/j.chemosphere.2013.02.001 PMid:23478125

Zghal F., Ben Amor Z. 1989. Sur la presence en Mediterrane de la race Perinereis cultrifera (Polych.te). Archives de l'institut Pasteur de Tunis 66: 293-301.