Abstract
This study aims to verify the relevance of Brachidontes pharaonis to assess the ecotoxicological status of polluted sites. For this, the levels of some heavy metals (i.e. Zn, Cu, Pb, and Cd) and a battery of biomarkers including metallothionein (MT), malondialdehyde (MDA), reduced glutathione (GSH), glutathione peroxidase (GPx), superoxide dismutase (SOD), and catalase (CAT) were assessed in mussels collected from the harbor of Rades (North), and the harbor of Zarzis (South). Moreover, abiotic parameters including temperature, salinity, pH, and dissolved oxygen were assessed. Results from the ICP-OES showed that the southern population exhibited a higher metal pollution index with significantly higher Zn, Cu, and Pb concentrations. Moreover, the specimens from Zarzis displayed significantly higher levels of MDA, MT, GSH, GPx, SOD, and CAT reflecting higher levels of oxidative and chemical stress. These results emphasize the potential utility of B. pharaonis for the monitoring of heavily impacted sites.
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References
Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202. https://doi.org/10.1016/j.aquatox.2005.08.015
Annabi-Trabelsi N, Guermazi W, Karam Q, Ali M, Uddin S, Leignel V, Ayadi H (2021) Concentrations of trace metals in phytoplankton and zooplankton in the Gulf of Gabès, Tunisia. Mar Pollut Bull 168:112392. https://doi.org/10.1016/j.marpolbul.2021.112392
Antit M, Amor N, Urra J, Alagaili AN, Farjallah S (2018) Genetic variability of the Lessepsian migrant mussel Brachidontes pharaonis (Bivalvia: Mytilidae) in Tunisia. Afr J Mar Sci 40:211–217. https://doi.org/10.2989/1814232X.2018.1476265
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Benaltabet T, Gutner-Hoch D, Torfstein A (2021) Heavy metal, rare earth element and Pb isotope dynamics in mussels during a depuration experiment in the gulf of Aqaba, Northern Red Sea. Front Mar Sci 8:669329. https://doi.org/10.3389/fmars.2021.669329
Chen L, Ma L, Bai Q et al (2014) Heavy metal-induced metallothionein expression is regulated by specific protein phosphatase 2A complexes. J Biol Chem 289:22413–22426. https://doi.org/10.1074/jbc.M114.548677
Çinar ME, Bilecenoğlu M, Yokeş MB et al (2021) Current status (as of end of 2020) of marine alien species in Turkey. PLoS ONE 16:e0251086. https://doi.org/10.1371/journal.pone.0251086
Core Team R (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
de Lorenzo V, Sekowska A, Danchin A (2015) Chemical reactivity drives spatiotemporal organisation of bacterial metabolism. FEMS Microbiol Rev 39:96–119. https://doi.org/10.1111/1574-6976.12089
Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Meth Enzymol 186:421–431. https://doi.org/10.1016/0076-6879(90)86135-I
Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77. https://doi.org/10.1016/0003-9861(59)90090-6
Flohé L, Günzler WA (1984) Assays of glutathione peroxidase. Meth Enzymol 105:114–121. https://doi.org/10.1016/S0076-6879(84)05015-1
Freitas R, Coppola F, Costa S et al (2019) Does salinity modulates the response of Mytilus galloprovincialis exposed to triclosan and diclofenac? Environ Pollut 251:756–765. https://doi.org/10.1016/j.envpol.2019.04.115
Géret F, Serafim A, Barreira L, Bebianno MJ (2002) Response of antioxidant systems to copper in the gills of the clam Ruditapes decussatus. Mar Environ Res 54:413–417
Gokkus K, Berber S (2019) Heavy metal pollution in Inebolu and Bartin Ports, Black Sea, Turkey. Indian J Geol-Mar Sci 48:1600
Hamed ESAE, Khaled A, Ahdy H, Ahmed HO, Abdel Razek FA (2020) Health risk assessment of heavy metals in three invertebrate species collected along Alexandria Coast, Egypt, Egypt. J Aquat Res 46:389–395. https://doi.org/10.1016/j.ejar.2020.11.001
Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (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
Karayakar F, Erdem C, Cicik B (2007) Seasonal variation in copper, zinc, chromium, lead and cadmium levels in hepatopancreas, gill and muscle tissues of the mussel Brachidontes pharaonis Fischer, collected along the Mersin coast, Turkey. Bull Environ Contam Toxicol 79(3):350–355. https://doi.org/10.1007/s00128-007-9246-z
Keller RP, Drake JM, Drew MB, Lodge DM (2010) Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network. Divers Distrib 17:93–102
Krishnakumar PK, Qurban MA, Geetha Sasikumar G (2018) Biomonitoring of trace metals in the coastal waters using bivalve molluscs. In: Saleh HEM, El-Adham E (eds) Trace elements—human health and environment. IntechOpen, London. https://doi.org/10.5772/intechopen.76938
Lavradas RT, Rafael RCC, Bordon ICAC et al (2016) Differential metallothionein, reduced glutathione and metal levels in Perna perna mussels in two environmentally impacted tropical bays in southeastern Brazil. Ecotoxicol Environ Saf 129:75–84. https://doi.org/10.1016/j.ecoenv.2016.03.011
LCAs (2021) Logistics capacity assessments. Available at https://dlca.logcluster.org/display/public/DLCA/LCA+Homepage. Accessed on 06 Jan 2022
Le Saux A, David E, Betoulle S et al (2020) New insights into cellular impacts of metals in aquatic animals. Environments 7:46. https://doi.org/10.3390/environments7060046
Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666. https://doi.org/10.1016/s0025-326x(01)00060-1
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Mansouri B, Gzam M, Souid F, Telahigue F, Chahlaoui A, Ouarrak K, Kharroubi A (2020) Assessment of heavy metal contamination in Gulf of Gabès coastland (southeastern Tunisia): impact of chemical industries and drift currents. Arab J Geosci 13:11–05. https://doi.org/10.1007/s12517-020-06163-3
Petrović S, Ozretić B, Krajnović-Ozretić M, Bobinac D (2001) Lysosomal membrane stability and metallothioneins in digestive gland of mussels (Mytilus galloprovincialis Lam.) as biomarkers in a field study. Mar Pollut Bull 42:1373–1378. https://doi.org/10.1016/S0025-326X(01)00167-9
Quéméneur M, Bel Hassen M, Armougom F, Khammeri Y, Lajnef R, Bellaaj-Zouari A (2020) Prokaryotic diversity and distribution along physical and nutrient gradients in the Tunisian coastal waters (South Mediterranean Sea). Front Microbiol 11:593540. https://doi.org/10.3389/fmicb.2020.593540
Rouane-Hacene O, Boutiba Z, Belhaouari B, GuibboliniSabatier ME, Francour P, Risso-De Faverney C (2015) Seasonal assessment of biological indices, bioaccumulation and bioavailability of heavy metals in mussels Mytilus galloprovincialis from Algerian west coast, applied to environmental monitoring. Oceanologia 57(4):362–374. https://doi.org/10.1016/j.oceano.2015.07.004
Saebi M, Xu J, Curasi SR, Grey EK, Chawla NV, Lodge DM (2020) Network analysis of ballast-mediated species transfer reveals important introduction and dispersal patterns in the Arctic. Sci Rep 10(1):1–15
Sarà G, Porporato EM, Mangano MC, Mieszkowska N (2018) Multiple stressors facilitate the spread of a non-indigenous bivalve in the Mediterranean Sea. J Biogeogr 45:1090–1103. https://doi.org/10.1111/jbi.13184
Schettino T, Caricato R, Calisi A, Giordano ME, Lionetto MG (2012) Biomarker approach in marine monitoring and assessment: new insights and perspectives. Open Environ Sci 6:20–27. https://doi.org/10.2174/1876325101206010020
Tang H, Ke Z, Yan M et al (2018) Concentrations, distribution, and ecological risk assessment of heavy metals in Daya Bay, China. Water 10:780. https://doi.org/10.3390/w10060780
Telahigue K, Rabeh I, Chouba L et al (2022) Assessment of the heavy metal levels and biomarker responses in the smooth scallop Flexopecten glaber from a heavily urbanized Mediterranean lagoon (Bizerte lagoon). Environ Monit Assess 194(6):397. https://doi.org/10.1007/s10661-022-10071-2
Tsangaris C, Moschino V, Strogyloudi E et al (2016) Biochemical biomarker responses to pollution in selected sentinel organisms across the Eastern Mediterranean and the Black Sea. Environ Sci Pollut Res 23:1789–1804. https://doi.org/10.1007/s11356-015-5410-x
Usero J, Rega–lado EG, Gracia I (1997) Trace metals in bivalve molluscs Ruditapes decussatus and Ruditapes philippinarum from the Atlantic coast of southern Spain. Environ Int 23:291–298. https://doi.org/10.1016/S0160-4120(97)00030-5
Valko M, Jomova K, Rhodes CJ, Kuča K, Musílek K (2016) Redox- and non-redox-metal-induced formation of free radicals and their role in human disease. Arch Toxicol 90(1):1–37. https://doi.org/10.1007/s00204-015-1579-5
Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar Environ Res 44:69–84. https://doi.org/10.1016/S0141-1136(96)00103-1
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Telahigue, K., Antit, M., Rabeh, I. et al. Heavy Metal Bioaccumulation and Oxidative Stress Profile in Brachidontes pharaonis (Bivalvia: Mytilidae) from the Tunisian Coast: Insight into Its Relevance as Bioindicator of Marine Pollution. Bull Environ Contam Toxicol 109, 831–838 (2022). https://doi.org/10.1007/s00128-022-03593-5
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DOI: https://doi.org/10.1007/s00128-022-03593-5