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Multiple Biomarker Responses in Corbicula fluminea Exposed to Copper in Laboratory Toxicity Tests

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Abstract

This study evaluated the alteration of the enzymatic system of the freshwater Asian clam exposed to different copper concentrations. Individuals of Corbicula fluminea were exposed to different concentrations of dissolved Cu (0.5, 1, and 2 mg L−1) for 7 days, then, biomarkers of oxidative stress (GST, GPx, GR), exposure (MTs), effect (AChE), and damage (LPO, DNA strand breaks) were quantified. Results showed positive correlations between dissolved metal concentrations and GPx, MTs, and DNA damage, and negative correlation with GST and AChE. In contrast, no clear trend was found for GR and LPO. In general, the established mechanisms of protection might have a beneficial effect on the decreasing ROS attack on membrane and the activation of the metallothioneins. Integrated biomarker analysis revealed that the measured alterations are well correlated with the levels of increasing dissolved copper concentrations in water, demonstrating the effectiveness of this organism for biomonitoring approach purposes.

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References

  • Abessa DMS, Gonçalves L, Fernando C, Davanso MB, Guimarães V et al (2014) Sediment geochemistry and climatic influences in a river influenced by former mining activities: the case of Ribeira de Iguape River, SP-PR, Brazil. Open J Water Pollut Treat 1:43–54

    Article  Google Scholar 

  • Bagchi D, Bagchi M, Hassoun EA, Stohs SJ (1995) In vitro and in vivo generation of reactive oxygen species, DNA damage and lactate dehydrogenase leakage by selected pesticides. Toxicology 104:129–140

    Article  CAS  Google Scholar 

  • Barka S, Pavillon JF, Amiard JC (2001) Influence of different essential and non- essential metals on MTLP levels in the copepod Tigriopus brevicornis. Comp Biochem Physiol C 128:479–493

    Article  CAS  Google Scholar 

  • Bayne BL, Brown DA, Burns K, Dixon DP, Ivanovici A, Livingstone DR, Lowe DM et al (1985) The effects of stress and pollution on marine animals. Praeger Scientific, New York

    Google Scholar 

  • Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21(6):1316–1322

    Article  CAS  Google Scholar 

  • Bocquené G, Galgani F, Truquet P (1990) Characterization and assay conditions for use of AChE activity from several marine species in pollution monitoring. Mar Environ Res 30:75–89

    Article  Google Scholar 

  • Bonnail E, Sarmiento AM, DelValls TA, Nieto JM, Riba I (2016) Assessment of metal contamination, bioavailability, toxicity and bioaccumulation in extreme metallic environments (Iberian Pyrite Belt) using Corbicula fluminea. Sci Total Environ 544:1031–1044

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 2:248–254

    Article  Google Scholar 

  • Capdevila M, Bofill R, Palacio O, Atrian S (2012) State-of-the-art of metallothioneins at the beginning of the 21st centuruy. Coord Chem Rev 256:46–62

    Article  CAS  Google Scholar 

  • CONAMA 357/2005. Resoluçao N257, de 17 de Março de 2005. http://www.mma.gov.br/port/conama/res/res05/res35705.pdf

  • Depledge MH (1994) The rational basis for use of biomarkers as ecotoxicological tools. In: Fossi MC, Leonzio C (eds) Nondestructive biomarkers in vertebrates. Lewis Publishers, Boca Raton, pp 271–295

    Google Scholar 

  • Directive 2000/60/EC of the European Parliament and of the Council establishing a framework for the Community action in the field of water policy. http://ec.europa.eu/environment/water/water-framework/index_en.html

  • Doyotte A, Cossu C, Jacquin MC, Babut M, Vasseur P (1997) Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquat Toxicol 39(2):93–110

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney D, Andres JV, Feathersthone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–96

    Article  CAS  Google Scholar 

  • Franco R, Sánchez-Olea R, Reyes-Reyes EM, Panayiotidis MI (2009) Environmental toxicity, oxidative stress and apoptosis: ménage à trois. Mutat Res 674:3–22

    Article  CAS  Google Scholar 

  • Frasco MF, Fournier D, Carvalho F, Guilhermino L (2005) Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity. Biomarkers 10(5):360–375

    Article  CAS  Google Scholar 

  • Frausto da Silva JJR, Williams JP (2001) Copper: extracytoplasmic oxidases and matrix formation. In: Silva JJR, Williams JP (eds) The biological chemistry of the element, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Gaetke LM, Chow K (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163

    Article  CAS  Google Scholar 

  • Graney RL, Donald JS, Cairns CJ Jr (1983) Heavy metal indicator potential of the Asiatic clam (Corbicula fluminea) in artificial stream systems. Hydrobiologia 102:81–88

    Article  CAS  Google Scholar 

  • Huggett JR, Kimerle RA, Mehrle PM, Bergman HL (1992) Biomarkers, biochemical, physiological, and histological markers and anthropogenic stress. Lewis, Boca Raton, p 347

    Google Scholar 

  • Key PB, Fulton MH (2002) Characterization of cholinesterase activity in tissues of the grass shrimp (Palaemonetes pugio). Pestic Biochem Physiol 72:186–192

    Article  CAS  Google Scholar 

  • Kopecka-Pilarczyk J (2010) The effect of pesticides and metals on acetylcholinesterase (AChE) in various tissues of blue mussel (Mytilus trossulus L.) in short-term in vivo exposures at different temperatures. J Environ Sci Health B 45:336–346

    Article  CAS  Google Scholar 

  • Luza SC, Speisky HC (1996) Liver copper storage and transport during development: implications for cytotoxicity. Am J Clin Nutr 63:812S–820S

    CAS  Google Scholar 

  • Marie V, Baudrimont M, Boudou A (2006) Cadmium and zinc bioaccumulation and metallothionein response in two freshwater bivalves (Corbicula fluminea and Dreissena polymorpha) transplanted along a polymetallic gradient. Chemosphere 65:609–617

    Article  CAS  Google Scholar 

  • Martín-Díaz ML, Blasco J, Sales D, DelValls TA (2009) The use of a kinetic biomarker approach for in situ monitoring of littoral sediments using the crab Carcinus maenas. Mar Environ Res 68(2):82–88

    Article  Google Scholar 

  • Mason AZ, Jenkins KD (1995) Metal detoxification in aquatic organisms. In: Tessier A, Turner DR (eds) Metal speciation and bioavailability in aquatic systems. Wiley, Chichester, p 679

    Google Scholar 

  • McFarland VA, Inouye SL, Lutz CH, Jarvis AS, Clarke JU, McCant DD (1999) Biomarkers of oxidative stress and genotoxicity in livers of field collected brown bullhead, Ameiurus nebulosus. Arch Environ Contam Toxicol 37:236–241

    Article  CAS  Google Scholar 

  • Meagher EA, Fitzgerald GA (2000) Indices of lipid peroxidation in vivo: strengths and limitations. Free Radic Biol Med 28:1745–1750

    Article  CAS  Google Scholar 

  • Mora P, Fournier D, Narbonne JF (1999) Cholinesterases from the marine mussels Mytilus galloprovincialis Lmk. and Mytillus edulis from the freshwater bivalve Corbicula fluminea Müller. Comp Biochem Physiol C 122:353–361

    CAS  Google Scholar 

  • Morais LG, Perina FC, Davanso MB, Buruaem LM, Rodrigues VGS, Sígolo JB, Abessa DMS (2013) Water and sediment ecotoxicological assessment in a river affected by former mining activities. Pan-Am J Aquat Sci 8(4):327–338

    Google Scholar 

  • Olive PL (1988) DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environ Mol Mutagen 11:487–495

    Article  CAS  Google Scholar 

  • Oliveira LF, Silva SMCP, Martinez CBR (2014) Assessment of domestic landfill leachate toxicity to the Asian clam Corbicula fluminea via biomarkers. Ecotoxiol Environ Safe 103:17–23

    Article  CAS  Google Scholar 

  • Paekeall DB, Shugart RL (1993) Research and application in the assessment of environmental health. In: Paekall DB, Shugart RL (eds) Biomarkers: research and application in the assessment of environmental health. NATO ASI Series—Series H: Cell Biology 68. NATO, Texel

  • Ringwood AH, Conners DE (2000) The effects of glutathione depletion on reproductive success in oysters, Crassostrea virginica. Mar Environ Res 50:207–211

    Article  CAS  Google Scholar 

  • Roesijadi G, Robinson WE (1994) Metal regulation in aquatic animals: mechanisms of uptake, accumulation and release. In: Malins DC, Ostrander GK (eds) Aquatic toxicology; molecular biochemical and cellular perspectives. CRC Press, Boca Raton

    Google Scholar 

  • Sánchez W, Burgeot T, Porcher JM (2013) A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ Sci Pollut R 20(5):2721–2725

    Article  Google Scholar 

  • Stagg RM (1998) The development of an international programme for monitoring the biological effects of contaminants in the OSPAR convention area. Mar Environ Res 46:307–313

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal-ions. Free Radic Biol Med 18:321–336

    Article  CAS  Google Scholar 

  • Tsarpali V, Dailianis S (2012) Investigation of landfill leachate toxic potency: an integrated approach with the use of stress indices in tissue of mussels. Aquat Toxicol 124–125:58–65

    Article  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Safe 64:178–189

    Article  CAS  Google Scholar 

  • van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Viarengo A, Nott JA (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Biochem Phys C 104:355–372

    Article  Google Scholar 

  • Viarengo A, Canesi L, Pertica M, Poli G, Moore MN, Orunesu M (1990) Heavy metal effects on lipid peroxidation in the tissues of Mytilus galloprovincialis Lam. Comp Biochem Physiol 97C:37–42

    CAS  Google Scholar 

  • Viarengo A, Ponzano E, Dondero F, Fabbri E (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antartic mollusks. Mar Environ Res 44:69–84

    Article  CAS  Google Scholar 

  • Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A (2007) The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Phys Part C 146:281–300

    CAS  Google Scholar 

  • Wills ED (1987) Evaluation of lipid peroxidation in lipids and biological membranes. In: Mullock B, Snell K (ed) Biochemical toxicology a practical approach. IRL Press, Oxford, pp 127–150

    Google Scholar 

Download references

Acknowledgments

The first author thanks the International Grant from Bank Santander/UNESCO Chair UNITWIN/WiCop and the Erasmus Mundus Programme for the MACOMA Doctoral funding contract (SGA 2012-1701/001-001-EMJD). We thank the Brazilian National Council for Scientific and Technological Development (CNPq; Grant #479899/2013-4), the São Paulo Research Foundation (FAPESP, Grant #2009/52762-6), and the Brazilian Aquatic Research Foundation (FUNDESPA) for the financial support. Dr. Lucas Buruaem thanks FAPESP (Grant #2013/15482-0, São Paulo Research Foundation) and Dr. Abessa thanks CNPq (Grants 308649/2011-7 and 311609/2014-7). The authors thank Dr. Van Den Brink and the reviewers for their expert guidance that has contributed to the improvement of the manuscript and R. Ojeda for the English language review.

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Authors and Affiliations

  1. UNESCO UNITWIN/WiCop, Department of Physical-Chemistry, Faculty of Marine and Environmental Sciences, University of Cádiz, Campus Río San Pedro, 11510, Puerto Real, Cádiz, Spain

    Estefanía Bonnail & T. Ángel DelValls

  2. Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus Experimental do Litoral Paulista, Núcleo de Estudos sobre Poluição e Ecotoxicologia Aquática, Praça Infante Dom Henrique s/n, 11330-900, São Vicente, SP, Brazil

    Lucas M. Buruaem, Giuliana S. Araujo & Denis M. S. Abessa

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  1. Estefanía Bonnail
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  2. Lucas M. Buruaem
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  3. Giuliana S. Araujo
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  4. Denis M. S. Abessa
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  5. T. Ángel DelValls
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Correspondence to Estefanía Bonnail.

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Bonnail, E., Buruaem, L.M., Araujo, G.S. et al. Multiple Biomarker Responses in Corbicula fluminea Exposed to Copper in Laboratory Toxicity Tests. Arch Environ Contam Toxicol 71, 278–285 (2016). https://doi.org/10.1007/s00244-016-0281-9

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