Skip to main content
Log in

Consequences of oxidative damage on the fatty acid profile in muscle of Cichlasoma amazonarum acutely exposed to copper

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Rapid industrialization results in the production of large quantities of waste that are commonly discharged into water bodies, leading to the damage of the aquatic ecosystem and freshwater organisms. Copper (Cu) can induce oxidative damage in fish muscle, the main fish portion that is consumed by humans. However, the responses of the Amazon fish Cichlasoma amazonarum and its capacity to withstand acute Cu concentrations found in Amazon water around mines remain unknown. Thus, the aim of this study was to evaluate whether exposure to Cu causes muscle oxidative stress and/or oxidative damage and impairs the fillet fatty acid profile of C. amazonarum acutely exposed to Cu found in Amazon waters around mines. Muscle reactive oxygen species and protein carbonylation levels were significantly higher in fish exposed to 1500 μg/L Cu compared with the control group, while muscle lipid peroxidation levels were significantly higher in fish exposed to 500, 750, and 1500 μg/L Cu compared with control group. Muscle antioxidant capacity against peroxyl radical’s levels and glutathione peroxidase activity were significantly lower in fish exposed to 1500 μg/L Cu compared with the control group, while muscle superoxide dismutase activity was significantly lower in fish exposed to 750 and 1500 μg/L Cu compared with control group. The total content of saturated fatty acids was significantly higher in fish exposed to 1500 μg/L Cu compared with the control group, while the total content of monounsaturated fatty acids and sum of n3 fatty acids were significantly lower in fish exposed to 1500 μg/L Cu compared with control group. No significant difference was observed regarding muscle catalase, glutathione S-transferase, and glutathione reductase activities. Based on these lines of evidence, the results of this comprehensive study agree with the initial hypothesis that the exposure to Cu found in Amazon water around mines induces oxidative damage and inhibits enzymatic and non-enzymatic antioxidant response in the muscle of C. amazonarum exposed to high Cu levels. Moreover, the impairment of the fillet fatty acid profile appears to be mediated by oxidative damage, representing a negative impact on fish health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abou Anni IS, Zebral YD, Afonso SB, Moreno Abril SI, Lauer MM, Bianchini A (2019) Life-time exposure to waterborne copper III: effects on the energy metabolism of the killifish Poecilia vivipara. Chemosphere 227:580–588

    CAS  PubMed  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  PubMed  Google Scholar 

  • Afridi AJ, Zuberi A, Yousafzai AM, Kamran M, Ullah S (2019) Hemp (marijuana) reverted copper-induced toxic effects on the essential fatty acid profile of Labeo rohita and Cirrhinus mrigala. Mol Biol Rep 46:391–401

    CAS  PubMed  Google Scholar 

  • Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JLR, Yunes JS, Montserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123

    CAS  PubMed  Google Scholar 

  • Baldissera MD, Souza CF, Barroso DC, Pereira RS, Alessio KO, Bizzi C, Baldisserotto B, Val AL (2020) Acute exposure to environmentally relevant concentrations of copper affects branchial and hepatic phosphoryl transfer network of Cichlasoma amazonarum: Impacts on bioenergetics homeostasis. Comp Biochem Physiol C Toxicol Pharmacol 238:108846

    CAS  PubMed  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Boareto AC, Giareta EP, Guiloski IC, Rodrigues MS, Freire CA, Silva-de-Assis HC (2018) Effects of short-term exposure to copper on biochemical biomarkers in juvenile freshwater fish. Pan-American J Aquatic Scie 13:135–147

    Google Scholar 

  • Calder PC, Yaqoob P (2009) Omega-3 polyunsaturated fatty acids and human health outcomes. Biofactors 35:266–272

    CAS  PubMed  Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzymol 113:484–490

    CAS  PubMed  Google Scholar 

  • Crémazy A, Wood CM, Smith DS, Ferreira MS, Johannsson OE, Giacomin M, Val AL (2016) Investigating copper toxicity in the tropical fish cardinal tetra (Paracheirodon axelrodi) in natural Amazonian waters: measurements, modeling, and reality. Aquatic Toxicol 180:353–363

    Google Scholar 

  • Das D, Das P, Moniruzzaman M, Sarkar MP, Mukherjee J, Chakraborty SB (2018) Consequences of oxidative damage and mitochondrial dysfunction on the fatty acid profile of muscle of Indian major carps considering metal toxicity. Chemosphere 207:385–396

    CAS  PubMed  Google Scholar 

  • Delgado-Lista J, Perez-Martinez P, Lopez-Miranda J, Perez-Jimenez F (2012) Long chain omega-3 fatty acids and cardiovascular disease: a systematic review. Br J Nutr 107:S201–S213

    CAS  PubMed  Google Scholar 

  • Díaz-Alba M, Raya AC, Granado-Costa MD, Ramírez MO, El Mai B, García FC, Troyano-Montoro M, Espada-Bellido E, Santiago RT, Galindo-Riaño MD (2017) Biomarker responses of Cu-induced toxicity in European seabass Dicentrarchus labrax: assessing oxidative stress and histopathological alterations. Mar Poll Bul 124:336–348

    Google Scholar 

  • DiNicolantonio JJ (2017) Good fats versus bad fats: a comparison of fatty acids in the promotion of insulin resistance, inflammation, and obesity. Miss Med 114:303–307

    Google Scholar 

  • Feng M, He Q, Meng L, Zhang X, Sun P, Wang Z (2015) Evaluation of single and joint toxicity of perfluorooctane sulfonate, perfluorooctanoic acid, and copper to Carassius auratus using oxidative stress biomarkers. Aquatic Toxicol 161:108–116

    CAS  Google Scholar 

  • Fry KL, Wheeler CA, Gillings MM, Flegal AR, Taylor MP (2020) Anthropogenic contamination of residential environments from smelter As, Cu and Pb emissions: implications for human health. Environm Poll 262:114235

    CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Hader DP, Banaszak AT, Villafane VE, Narvarte MA, González RA, Helbing EW (2020) Anthropogenic pollution of aquatic ecosystems: emerging problems with global implications. Sci Total Environm 713:136586

    Google Scholar 

  • Hartman L, Lago RC (1973) Rapid preparation of fatty acid methyl esters from lipids. Lab Pract 22:475–477

    CAS  PubMed  Google Scholar 

  • He Z, Li F, Dominech S, Wen X, Yang S (2019) Heavy metals of surface sediments in the Changjiang (Yangtze River) estuary: distribution, speciation and environmental risks. J Geochem Expl 198:18–28

    CAS  Google Scholar 

  • Hrbek T, Farias IP, Crossa M, Sampaio I, Porto JIR, Meyer A (2005) Population genetic analysis of Arapaima gigas, one of the largest freshwater fishes of the Amazon basin: implications for its conservation. Anim Conserv 8:297–308

    Google Scholar 

  • Jafari AJ, Kermani M, Kalantary RR, Arfaeinia H (2018) The effect of traffic on levels, distribution and chemical partitioning of harmful metals in the street dust and surface soil from urban areas of Tehran. Iran Environ Earth Sci 77:38

    Google Scholar 

  • Javed M, Usmani N (2019) An overview of the adverse effects of heavy metal contamination on fish health. Proc Natl Acad Sci 89:389–403

    CAS  Google Scholar 

  • Jiang WD, Liu Y, Jiang J, Wu P, Feng L, Zhou XQ (2015) Copper exposure induces toxicity to the antioxidant system via the destruction of Nrf2/ARE signaling and caspase-3-regulated DNA damage in fish muscle: amelioration by myo-inositol. Aquatic Toxicol 159:245–255

    CAS  Google Scholar 

  • Kim WK, Park JW, Lim ES, Lee SK, Kim J, Lee SW, Choi K, Jung J (2014) Tissue-specific antioxidant responses in pale chub (Zacco platypus) exposed to copper and benzo[a]pyrene. Bull Environ Contam Toxicol 92:540–545

    CAS  PubMed  Google Scholar 

  • Kotwal S, Jun M, Sullivan D, Perkovic V, Neal B (2012) Omega 3 fatty acids and cardiovascular outcomes: systematic review and meta-analysis. Circ Cardiovasc Qual Outcomes 5:808–818

    PubMed  Google Scholar 

  • LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231

    CAS  PubMed  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    CAS  PubMed  Google Scholar 

  • Mensink R (2016) Effects of saturated fatty acids on serum lipids and lipoproteins: a systematic review and regression analysis. World Health Organization, Geneva

    Google Scholar 

  • Michielsen CCJR, Hangelbroek RWJ, Feskens EJM, Afman LA (2019) Disentangling the effects of monounsaturated fatty acids from other components of a mediterranean diet on serum metabolite profiles: a randomized fully controlled dietary intervention in healthy subjects at risk of the metabolic syndrome. Mol Nutr Food Res 63:e1801095

    PubMed  Google Scholar 

  • Mohanty BP, Mahanty A, Ganguly S, Mitra T, Karunakaran D, Anandan R (2019) Nutritional composition of food fishes and their importance in providing food and nutritional security. Food Chem 293:561–570

    CAS  PubMed  Google Scholar 

  • Monserrat JM, Geracitano LA, Pinho GLL, Vinagre TM, Faleiros M, Alciati JC, Bianchini A (2003) Determination of lipid peroxides in invertebrates using the Fe (III) xylenol orange complex formation. Arch Environ Contam Toxicol 45:177–183

    CAS  PubMed  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocytes glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  PubMed  Google Scholar 

  • Ransberry VE, Blewett TA, McClelland GB (2016) The oxidative stress response in freshwater-acclimated killifish (Fundulus heteroclitus) to acute copper and hypoxia exposure. Comp Biochem Physiol C 179:11–18

    CAS  Google Scholar 

  • Read SM, Northcote DH (1981) Minimization of variation in the response to different proteins of the Coomassie blue G dye-binding assay for protein. Anal Biochem 116:53–64

    CAS  PubMed  Google Scholar 

  • Reznick AZ, Packer L (1994) Oxidative damage of proteins: spectrophotometer for carbonyl assay. Methods Enzymol 233:357–363

    CAS  PubMed  Google Scholar 

  • Santana GP, Barroncas DSRP (2007) Estudo de metais pesados (Co, Cu, Fe, Cr, Ni, Mn, Pb e Zn) na Bacia do Tarumã-Açu Manaus (AM). Acta Amaz 37(1):11–118

    Google Scholar 

  • Shekh K, Alcaraz AJ, Niyogi S, Hecker M (2020) Comparative analyses of oxidative stress response and metallothione in induction in white sturgeon and rainbow trout during acute waterborne copper exposure. Comp Biochem Physiol C 231:108723

    CAS  Google Scholar 

  • Sies H, Berndt C, Jones DP (2017) Oxidative stress. Ann Review Biochem 86:715–748

    CAS  Google Scholar 

  • Siqueira-Gay J, Sonter LJ, Sánchez LE (2020) Exploring potential impacts of mining on forest loss and fragmentation within a biodiverse region of Brazil’s northeastern Amazon. Res Pol 67:101662

    Google Scholar 

  • Sissener NH, Araujo P, Saele O, Roselund G, Stubhaug I, Sanden M (2020) Dietary 18:2n-6 affects EPA (20:5n-3) and ARA (20:4n-6) content in cell membranes and eicosanoid production in Atlantic salmon (Salmo salar L.). Aquaculture 522:735098

    CAS  Google Scholar 

  • Tesser ME, de Paula AL, Risso WE, Monteiro RA, Pereira AES, Fraceto LF, Martinez CBR (2020) Sublethal effects of waterborne copper and copper nanoparticles on the freshwater Neotropical teleost Prochilodus lineatus: a comparative approach. Sci Total Environ 704:135332

    CAS  PubMed  Google Scholar 

  • Viña J, Borras C, Gomez-Cabrera MC (2018) A free radical theory of frailty. Free Rad Biol Med 124:358–363

    PubMed  Google Scholar 

  • Xiang QQ, Wang D, Zhang JL, Ding CZ, Luo X, Tao J, Ling J, Shea D, Chen LQ (2020) Effect of silver nanoparticles on gill membranes of common carp: modification of fatty acid profile, lipid peroxidation and membrane fluidity. Environm Poll 256:113504

    CAS  Google Scholar 

  • Yuan SS, Ming Z, Zhu AY, Zheng JL, Wu CW (2017) Negative effect of chronic cadmium exposure on growth, histology, ultrastructure, antioxidant and innate immune responses in the liver of zebrafish: preventive role of blue light emitting diodes. Ecotoxicol Environ Saf 139:18–26

    CAS  PubMed  Google Scholar 

  • Zebral YD, Roza M, Fonseca JS, Costa PG, de Oliveira CS, Zocke TG, Dal Pizzol JL, Robaldo RB, Bianchini A (2019) Waterborne copper is more toxic to the killifish Poecilia vivipara in elevated temperatures: linking oxidative stress in the liver with reduced organismal thermal performance. Aquatic Toxicol 209:142–149

    Google Scholar 

  • Zhang Z, Lu Y, Li H, Tu Y, Liu B, Yang Z (2018) Assessment of heavy metal contamination, distribution and source identification in the sediments from the Zijiang River, China. Scie Total Environ 645:235–243

    CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank to the technician Reginaldo Oliveira for all logistical support. Thanks are due to Maria de Nazaré Paula da Silva for laboratory support.

Credit author statement

Matheus Baldissera: conceptualization, sample collection, data curation, and writing-reviewing; Danilo Barroso, Rogério Pereira, Cezar A. Bizzi, and Keiti Alessio: Cu analysis; Carine Souza: oxidative stress analysis; Fernanda C. de Oliveira and Roger Wagner: fatty acid analysis; Bernardo Baldisserotto and Adalberto Val: conceptualization and review.

Funding

This research was funded by a joint grant from the Brazilian National Research Council (CNPq, 465540/2014-7), the Amazonas State Research Foundation (FAPEAM, 062.01187/2017), and Coordination for the Improvement of Higher Education Personnel (CAPES, finance code 001) to ALV (INCT ADAPTA). ALV is the recipient of a research fellowship from the CNPq. CFS was the recipient of a fellowship from FAPEAM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matheus D. Baldissera.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baldissera, M.D., Souza, C.F., Barroso, D.C. et al. Consequences of oxidative damage on the fatty acid profile in muscle of Cichlasoma amazonarum acutely exposed to copper. Fish Physiol Biochem 46, 2377–2387 (2020). https://doi.org/10.1007/s10695-020-00884-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00884-8

Keywords

Navigation