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Cytosolic and Metallothionein-Bound Hepatic Metals and Detoxification in a Sentinel Teleost, Dules auriga, from Southern Rio de Janeiro, Brazil

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Abstract

Dules auriga, a native Brazilian teleost, was applied as a sentinel species regarding metal contamination at Ilha Grande Bay, previously considered a reference site in Southeastern Brazil. Cytosolic (S50) and metallothionein-bound (HTS50) hepatic iron (Fe), zinc (Zn), copper (Cu), manganese (Mn), cadmium (Cd), and silver (Ag) were determined by inductively coupled plasma optical emission spectrometry (ICP-OES), while metallothionein (MT) concentrations were determined by polarography. Ag concentrations in both cytosolic fractions were below the limit of detection. All other HTS50 metal contents were significantly lower than S50 contents. No significant associations were found for MT. Fe and Mn S50 were positively and moderately correlated to total length, as well as HTS50 Mn, while total weight was correlated to both Mn fractions, suggesting that environmental Mn and Fe concentrations may influence fish growth. A moderate correlation between the condition factor and the S50 Cu fraction was observed, also indicating that Cu may affect fish growth. Inter-element correlations were observed, including between Cd, a toxic element, and Mn and Zn, both essential elements. Calculated molar ratios indicate that both Mn and Zn are in molar excesses compared with Cd, corroborating literature assessments regarding protective Mn and Zn effects against Cd. Lack of MT correlations suggests that metal concentrations may not be high enough to reach an MT induction threshold and that MT variability is probably linked to environmental metal concentrations. Therefore, the increased environmental contaminant levels observed in the study area indicate the need for biomonitoring efforts aiming at the application of efficient mitigation measures.

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References

  1. Nathan AJ, Scobell A (2012) Summary for Policymakers. In: How China sees America. CRC Press, Boca Raton. https://doi.org/10.1017/CBO9781107415324.004

    Chapter  Google Scholar 

  2. Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25:272–280. https://doi.org/10.1897/05-257R.1

    Article  CAS  PubMed  Google Scholar 

  3. Lavradas RT, Rocha RCC, Saint’Pierre TD, Godoy JM, Hauser-Davis RA (2016) Investigation of thermostable metalloproteins in Perna perna mussels from differentially contaminated areas in Southeastern Brazil by bioanalytical techniques. J Trace Elem Med Biol 34:70–78. https://doi.org/10.1016/j.jtemb.2016.01.003

    Article  CAS  PubMed  Google Scholar 

  4. Lavradas RT, Rocha RCC, Bordon ICAC, Saint’Pierre TD, Godoy JM, Hauser-Davis RA (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

    Article  CAS  PubMed  Google Scholar 

  5. Cardoso AGA, Boaventura GR, Silva Filho EV, Brod JA (2001) Metal distribution in sediments from the Ribeira Bay, Rio de Janeiro, Brazil. J Braz Chem Soc 12:767–774. https://doi.org/10.1590/S0103-50532001000600013

    Article  CAS  Google Scholar 

  6. Pāulo S (1982) Níveis naturais de metais pesados em sedimentos marinhos da Baía da Ribeira, Angra dos Reis. Cienc Cult 34:921–924

    Google Scholar 

  7. CEPERJ, do Estado do Rio de Janeiro, 2004. http://www.ceperj.rj.gov.br/ceep/info_territorios/div_poli/Estado_RJ_2010_Jubileu.jpg

  8. Kehrig HA, Malm O, Moreira I (1998) Mercury in a widely consumed fish Micropogonias furnieri (Demarest, 1823) from four main Brazilian estuaries. Sci Total Environ 213:263–271. https://doi.org/10.1016/S0048-9697(98)00099-0

    Article  CAS  PubMed  Google Scholar 

  9. De Souza Lima RG, Araújo FG, Maia MF, Seda Da Silveira A (2002) Evaluation of heavy metals in fish of the Sepetiba and Ilha Grande Bays, Rio de Janeiro, Brazil. Environ Res 89:171–179. https://doi.org/10.1006/enrs.2002.4341

    Article  CAS  PubMed  Google Scholar 

  10. Barros de Oliveira SM, Ruiz Pessenda LC, Teixeira Favaro DI, Babinski M (2012) A 2400-year record of trace metal loading in lake sediments of Lagoa Vermelha, southeastern Brazil. J S Am Earth Sci 33:1–7. https://doi.org/10.1016/j.jsames.2011.07.007

    Article  CAS  Google Scholar 

  11. Silva Junior DR, Carvalho DMT, Vianna M (2013) The catfish Genidens genidens (Cuvier, 1829) as a potential sentinel species in Brazilian estuarine waters. J Appl Ichthyol 29:1297–1303. https://doi.org/10.1111/jai.12280

    Article  Google Scholar 

  12. Hauser-Davis RA, Silva-Junior DR, Linde-Arias AR, Vianna M (2019) Hepatic metal and metallothionein levels in a potential sentinel teleost, Dules auriga, from a southeastern Brazilian estuary. Bull Environ Contam Toxicol 103:538–543. https://doi.org/10.1007/s00128-019-02654-6

    Article  CAS  PubMed  Google Scholar 

  13. Cussac VE, Molero AM (1987) Contribución al conocimiento de la biología de Dules auriga Cuvier (Pisces, Serranidae). Rev Bras Biol 47:375–384

    Google Scholar 

  14. C.E.L. Ferreira, Peixes recifais. Biodiversidade Marinha da Baía da Ilha Grande, Ministério Do Meio Ambient. (2007)

  15. VAZZOLER AEAM (1996) Biologia da reprodução de peixes teleósteos: teoria e prática. SBI/EDUEM, São Paulo http://www.academia.edu/3334063/Biologia_da_reprodução_de_peixes_teleósteos_teoria_e_prática

    Google Scholar 

  16. Erk M, Ivanković D, Raspor B, Pavičič J (2002) Evaluation of different purification procedures for the electrochemical quantification of mussel metallothioneins. Talanta. 57:1211–1218. https://doi.org/10.1016/S0039-9140(02)00239-4

    Article  CAS  PubMed  Google Scholar 

  17. Dabrio M, Rodríguez AR, Bordin G, Bebianno MJ, De Ley M, Šestáková I, Vašák M, Nordberg M (2002) Recent developments in quantification methods for metallothionein. J Inorg Biochem:123–134. https://doi.org/10.1016/S0162-0134(01)00374-9

  18. Ishak I, Rosli FD, Mohamed J, Mohd Ismail MF (2015) Comparison of digestion methods for the determination of trace elements and heavy metals in human hair and nails. Malaysian J Med Sci 22:11–20

    Google Scholar 

  19. Eurachem, The Fitness for Purpose of Analytical Methods, 1998. 978-91-87461-59-0

  20. Starkings S (2012) Quantitative data analysis with IBM SPSS 17, 18 & 19: a guide for social scientists by Alan Bryman and Duncan Cramer. Int Stat Rev 80:334–335. https://doi.org/10.1111/j.1751-5823.2012.00187_14.x

    Article  Google Scholar 

  21. da Silva DR, Paranhos R, Vianna M (2016) Spatial patterns of distribution and the influence of seasonal and abiotic factors on demersal ichthyofauna in an estuarine tropical bay. J Fish Biol 89:821–846. https://doi.org/10.1111/jfb.13033

    Article  PubMed  Google Scholar 

  22. Langston WJ, Chesman BS, Burt GR, Pope ND, McEvoy J (2002) Metallothionein in liver of eels Anguilla anguilla from the Thames Estuary: an indicator of environmental quality? Mar Environ Res 53:263–293. https://doi.org/10.1016/S0141-1136(01)00113-1

    Article  CAS  PubMed  Google Scholar 

  23. Marijić VF, Raspor B (2006) Age- and tissue-dependent metallothionein and cytosolic metal distribution in a native Mediterranean fish, Mullus barbatus, from the Eastern Adriatic Sea. Comp Biochem Physiol - C Toxicol Pharmacol 143:382–387. https://doi.org/10.1016/j.cbpc.2005.05.019

    Article  CAS  PubMed  Google Scholar 

  24. Ploetz DM, Fitts BE, Rice TM (2007) Differential accumulation of heavy metals in muscle and liver of a marine fish, (king mackerel, Scomberomorus cavalla Cuvier) from the Northern Gulf of Mexico, USA. Bull Environ Contam Toxicol 78:124–127. https://doi.org/10.1007/s00128-007-9028-7

    Article  CAS  Google Scholar 

  25. Carvalho CEV, Faria VV, Cavalcante MPO, Gomes MP, Rezende CE (2000) Distribuição de Metais Pesados em Peixes Costeiros Bentônicos da Região de Macaé, RJ, Brasil. Ecotoxicol Environ Restor 3:64–68

    Google Scholar 

  26. Decataldo A, Di Leo A, Giandomenico S, Cardellicchio N (2004) Association of metals (mercury, cadmium and zinc) with metallothionein-like proteins in storage organs of stranded dolphins from the Mediterranean sea (Southern Italy). J Environ Monit 6:361–367. https://doi.org/10.1039/b315685k

    Article  CAS  PubMed  Google Scholar 

  27. Lopes CA, Araujo NLF, Rocha L, Monteiro F, Rocha RCC, Saint’Pierre TD, Lutfi DS, Vianna M, Hauser-Davis RA (2019) Toxic and essential metals in Narcine brasiliensis (Elasmobranchii: Narcinidae): a baseline ecotoxicological study in the Southeast Atlantic and preliminary maternal transfer implications. Mar Pollut Bull 149:110606. https://doi.org/10.1016/j.marpolbul.2019.110606

    Article  CAS  Google Scholar 

  28. Baer KN (1996) Fundamentals of aquatic toxicology: effects, environmental fate, and risk assessment. J Am Coll Toxicol 15:453–454. https://doi.org/10.1177/109158189601500514

    Article  Google Scholar 

  29. Mouneyrac C, Amiard JC, Amiard-Triquet C (1998) Effects of natural factors (salinity and body weight) on cadmium, copper, zinc and metallothionein-like protein levels in resident populations of oysters Crassostrea gigas from a polluted estuary. Mar Ecol Prog Ser 162:125–135. https://doi.org/10.3354/meps162125

    Article  CAS  Google Scholar 

  30. Monteiro F, Lemos LS, de Moura JF, Rocha RCC, Moreira I, Di Beneditto AP, Kehrig HA, Bordon ICAC, Siciliano S, Saint’Pierre TD, Hauser-Davis RA (2019) Subcellular metal distributions and metallothionein associations in rough-toothed dolphins (Steno bredanensis) from Southeastern Brazil. Mar Pollut Bull 146:263–273. https://doi.org/10.1016/j.marpolbul.2019.06.038

    Article  CAS  PubMed  Google Scholar 

  31. M’Kandawire E, Mierek-Adamska A, Stürzenbaum SR, Choongo K, Yabe J, Mwase M, Saasa N, Blindauer CA (2017) Metallothionein from wild populations of the African catfish Clarias gariepinus: From sequence, protein expression and metal binding properties to transcriptional biomarker of metal pollution. Int J Mol Sci 18. https://doi.org/10.3390/ijms18071548

  32. Giguère A, Couillard Y, Campbell PGC, Perceval O, Hare L, Pinel-Alloul B, Pellerin J (2003) Steady-state distribution of metals among metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquat Toxicol 64:185–200. https://doi.org/10.1016/S0166-445X(03)00052-3

    Article  CAS  PubMed  Google Scholar 

  33. Rodríguez-Cea A, Linde Arias AR, Fernández de la Campa MR, Costa Moreira J, Sanz-Medel A (2006) Metal speciation of metallothionein in white sea catfish, Netuma barba, and pearl cichlid, Geophagus brasiliensis, by orthogonal liquid chromatography coupled to ICP-MS detection. Talanta 69:963–969. https://doi.org/10.1016/j.talanta.2005.11.045

    Article  CAS  PubMed  Google Scholar 

  34. Sutherland DEK, Stillman MJ (2011) The “magic numbers” of metallothionein. Metallomics. 3:444–463. https://doi.org/10.1039/c0mt00102c

    Article  CAS  PubMed  Google Scholar 

  35. Galbraith ED, Le Mézo P, Hernandez GS, Bianchi D, Kroodsma D (2019) Growth limitation of marine fish by low iron availability in the open ocean. Front Mar Sci 6:509. https://doi.org/10.3389/fmars.2019.00509

    Article  Google Scholar 

  36. Watanabe T, Kiron V, Satoh S (1997) Trace minerals in fish nutrition. Aquaculture. 151:185–207. https://doi.org/10.1016/S0044-8486(96)01503-7

    Article  CAS  Google Scholar 

  37. Kasozi N, Tandlich R, Fick M, Kaiser H, Wilhelmi B (2019) Iron supplementation and management in aquaponic systems: a review. Aquac Reports 15:100221. https://doi.org/10.1016/j.aqrep.2019.100221

    Article  Google Scholar 

  38. Roeder M, Roeder RH (1966) Effect of iron on the growth rate of fishes. J Nutr 90:86–90. https://doi.org/10.1093/jn/90.1.86

    Article  CAS  PubMed  Google Scholar 

  39. Gatlin DM, Wilson RP (1986) Characterization of iron deficiency and the dietary iron requirement of fingerling channel catfish. Aquaculture. 52:191–198. https://doi.org/10.1016/0044-8486(86)90143-2

    Article  CAS  Google Scholar 

  40. Hauser-Davis RA, Lavandier RC, Bastos FF, Oliveira TF, Oliveira Ribeiro CA, Ziolli RL, De Campos RC (2012) Alterations in morphometric and organosomatic indices and histopathological analyses indicative of environmental contamination in mullet, Mugil liza, from southeastern Brazil. Bull Environ Contam Toxicol 89:1154–1160. https://doi.org/10.1007/s00128-012-0846-x

    Article  CAS  PubMed  Google Scholar 

  41. Eastwood S, Couture P (2002) Seasonal variations in condition and liver metal concentrations of yellow perch (Perca flavescens) from a metal-contaminated environment. Aquat Toxicol 58:43–56. https://doi.org/10.1016/S0166-445X(01)00218-1

    Article  CAS  PubMed  Google Scholar 

  42. Laflamme JS, Couillard Y, Campbell PGC, Hontela A (2000) Interrenal metallothionein and cortisol secretion in relation to Cd, Cu, and Zn exposure in yellow perch, Perca flavescens, from Abitibi lakes. Can J Fish Aquat Sci 57:1692–1700. https://doi.org/10.1139/f00-118

    Article  CAS  Google Scholar 

  43. Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23. https://doi.org/10.1242/jeb.00068

    Article  CAS  PubMed  Google Scholar 

  44. Vulpe CD (1995) Cellular copper transport. Annu Rev Nutr 15:293–322. https://doi.org/10.1146/annurev.nutr.15.1.293

    Article  CAS  PubMed  Google Scholar 

  45. Jerez S, Motas M, Benzal J, Diaz J, Barbosa A (2013) Monitoring trace elements in Antarctic penguin chicks from South Shetland Islands, Antarctica. Mar Pollut Bull 69:67–75. https://doi.org/10.1016/j.marpolbul.2013.01.004

    Article  CAS  PubMed  Google Scholar 

  46. Ribeiro AR, Eira C, Torres J, Mendes P, Miquel J, Soares AMVM, Vingada J (2009) Toxic element concentrations in the razorbill alca torda (charadriiformes, alcidae) in Portugal. Arch Environ Contam Toxicol 56:588–595. https://doi.org/10.1007/s00244-008-9215-5

    Article  CAS  PubMed  Google Scholar 

  47. Glynn AW, Haux C, Hogstrand C (1992) Chronic toxicity and metabolism of Cd and Zn in juvenile minnows (Phoxinus phoxinus) exposed to a Cd and Zn mixture. Can J Fish Aquat Sci 49:2070–2079. https://doi.org/10.1139/f92-230

    Article  CAS  Google Scholar 

  48. Volpe AR, Cesare P, Aimola P, Boscolo M, Valle G, Carmignani M (2011) Zinc opposes genotoxicity of cadmium and vanadium but not of lead. J Biol Regul Homeost Agents 25:589–601

    CAS  PubMed  Google Scholar 

  49. Ralston NVC, Blackwell JL, Raymond LJ (2007) Importance of molar ratios in selenium-dependent protection against methylmercury toxicity. Biol Trace Elem Res 119:255–268. https://doi.org/10.1007/s12011-007-8005-7

    Article  CAS  PubMed  Google Scholar 

  50. Banni M, Chouchene L, Said K, Kerkeni A, Messaoudi I (2011) Mechanisms underlying the protective effect of zinc and selenium against cadmium-induced oxidative stress in zebrafish Danio rerio. Bio Metals 24:981–992. https://doi.org/10.1007/s10534-011-9456-z

    Article  CAS  Google Scholar 

  51. Jihen EH, Imed M, Fatima H, Abdelhamid K (2009) Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver of the rat: effects on the oxidative stress. Ecotoxicol Environ Saf 72:1559–1564. https://doi.org/10.1016/j.ecoenv.2008.12.006

    Article  CAS  Google Scholar 

  52. Zhang D, Liu J, Gao J, Shahzad M, Han Z, Wang Z, Li J, Sjölinder H (2014) Zinc supplementation protects against cadmium accumulation and cytotoxicity in madin-darby bovine kidney cells. PLoS One 9. https://doi.org/10.1371/journal.pone.0103427

  53. Chouchene L, Banni M, Kerkeni A, Saïd K, Messaoudi I (2011) Cadmium-induced ovarian pathophysiology is mediated by change in gene expression pattern of zinc transporters in zebrafish (Danio rerio). Chem Biol Interact 193:172–179. https://doi.org/10.1016/j.cbi.2011.06.010

    Article  CAS  PubMed  Google Scholar 

  54. &NA;, the Hepatocyte Review, Springer Science & Business Media, 2001. https://doi.org/10.1097/00024382-200116030-00013

  55. Graham N (1999) Guidelines for drinking-water quality, 2nd edition, Addendum to Volume 1 – Recommendations, World Health Organisation, Geneva, 1998, 36 pages. Urban Water 1:183. https://doi.org/10.1016/s1462-0758(00)00006-6

    Article  Google Scholar 

  56. Eybl V, Kotyzová D (2010) Protective effect of manganese in cadmium-induced hepatic oxidative damage, changes in cadmium distribution and trace elements level in mice. Interdiscip Toxicol 3:68–72. https://doi.org/10.2478/v10102-010-0013-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Chaudhary S, Iram S, Raisuddin S, Parvez S (2015) Manganese pre-treatment attenuates cadmium induced hepatotoxicity in Swiss albino mice. J Trace Elem Med Biol 29:284–288. https://doi.org/10.1016/j.jtemb.2014.06.013

    Article  CAS  PubMed  Google Scholar 

  58. Flachowsky G (1997) Basic animal nutrition and feeding. Wiley, Hoboken. https://doi.org/10.1016/s0377-8401(97)84958-9

    Book  Google Scholar 

  59. Dutta TK, Kaviraj A (2001) Acute toxicity of cadmium to fish Labeo rohita and copepod Diaptomus forbesi pre-exposed to CaO and KMnO4. Chemosphere. 42:955–958. https://doi.org/10.1016/S0045-6535(00)00166-1

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to the Laboratório de Biologia e Tecnologia Pesqueira group for the help in Dules auriga samplings, measurements, and dissections.

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Data will be made available upon request.

Funding

MV was funded by Brazilian National Council for Scientific and Technological Development (CNPq) grants.

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Authors and Affiliations

  1. Laboratório de Avaliação Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil, 4.365, Manguinhos, Rio de Janeiro, 21040-360, Brazil

    R. A. Hauser-Davis

  2. Laboratório de Biologia e Tecnologia Pesqueira, Departamento de Biologia Marinha, Instituto de Biologia, UFRJ, Av. Carlos Chagas Filho, 373, CCS, Bl. A., Rio de Janeiro, Rio de Janeiro, 21941-541, Brazil

    D. R. Silva-Junior & M. Vianna

  3. Laboratório de Toxicologia, Centro de Estudos da Saúde do Trabalhador e Ecologia Humana, Escola Nacional de Saúde Pública Sérgio Arouca, Fundação Oswaldo Cruz, Leopoldo Bulhões, Rio de Janeiro, 1480, Brazil

    A. R. Linde-Arias

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  1. R. A. Hauser-Davis
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The animals used in this study were processed in conformity with the ethical principles of animal experimentation, elaborated by the Brazilian College for Animal Experimentation (COBEA). Fish sampling was authorized under Permit No. 13012-1, April 10, 2007.

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Hauser-Davis, R.A., Silva-Junior, D.R., Linde-Arias, A.R. et al. Cytosolic and Metallothionein-Bound Hepatic Metals and Detoxification in a Sentinel Teleost, Dules auriga, from Southern Rio de Janeiro, Brazil. Biol Trace Elem Res 199, 744–752 (2021). https://doi.org/10.1007/s12011-020-02195-8

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