• Environmental and human health issues related to long term contamination by chlordecone in the French West Indies
  • Published:

Multi-scale impact of chronic exposure to environmental concentrations of chlordecone in freshwater cnidarian, Hydra circumcincta

Abstract

Chlordecone (CLD) is an organochlorine pesticide widely used in the past to control pest insects in banana plantations in the French West Indies. Due to its persistence in the environment, CLD has contaminated the soils where it has been spread, as well as the waters, and is still present in them. The objective of our study was to evaluate the effects of chronic exposure to environmentally relevant CLD concentrations in an animal model, the freshwater hydra (Hydra circumcincta). In a multi-marker approach, we have studied the expression of some target stress genes, the morphology, and the asexual reproduction rates. Our data showed that exposure to low concentrations of chlordecone leads to (i) a modulation of the expression of target genes involved in oxidative stress, detoxification, and neurobiological processes, and (ii) morphological damages and asexual reproduction impairment. We have observed non-monotonic dose-response curves, which agree with endocrine-disrupting chemical effects. Thus, “U-shaped” dose-response curves were observed for SOD, GRed, Hym355, and potentially GST gene expressions; inverted “U-shaped” curves for GPx and CYP1A gene expressions and reproductive rates; and a biphasic dose-response curve for morphological damages. Therefore, in the range of environmental concentrations tested, very low concentrations of CLD can produce equally or more important deleterious effects than higher ones. Finally, to our knowledge, this study is the first one to fill the lack of knowledge concerning the effects of CLD in Hydra circumcincta and confirms that this diploblastic organism is a pertinent freshwater model in the risk assessment.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Adler V, Yin Z, Tew KD, Ronai Z (1999) Role of redox potential and reactive oxygen species in stress signaling. Oncogene 18:6104–6111

    CAS  Article  Google Scholar 

  2. Arkhipchuk VV, Blaise C, Malinovskaya MV (2006) Use of hydra for chronic toxicity assessment of waters intended for human consumption. Environ Pollut 142:200–211. https://doi.org/10.1016/j.envpol.2005.10.012

    CAS  Article  Google Scholar 

  3. Arnaud L, Baran N, Gourcy L (2013) Etude du transfert de la chlordécone vers les eaux souterraines en Martinique. Rapport BRGM/RP-61767-FR. 73p, 49 ill.

  4. Bonello S, Zähringer C, BelAiba RS, Djordjevic T, Hess J, Michiels C, Kietzmann T, Görlach A (2007) Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 27(4):755–761

    CAS  Article  Google Scholar 

  5. Boucher O, Simard M-N, Muckle G, Rouget F, Kadhel P, Bataille H, Chajès V, Dallaire R, Monfort C, Thomé JP, Multigner L, Cordier S (2013) Exposure to an organochlorine pesticide (chlordecone) and development of 18-month-old infants. Neurotoxicology 35:162–168. https://doi.org/10.1016/j.neuro.2013.01.007

    CAS  Article  Google Scholar 

  6. Cabidoche Y-M, Achard R, Cattan P, Clermont-Dauphin C, Massat F, Sansoulet J (2009) Long-term pollution by chlordecone of tropical volcanic soils in the French West Indies: a simple leaching model accounts for current residue. Environ Pollut 157:1697–1705. https://doi.org/10.1016/j.envpol.2008.12.015

    CAS  Article  Google Scholar 

  7. Coat S, Monti D, Legendre P, Bouchon C, Massat F, Lepoint G (2011) Organochlorine pollution in tropical rivers (Guadeloupe): role of ecological factors in food web bioaccumulation. Environ Pollut 159:1692–1701. https://doi.org/10.1016/j.envpol.2011.02.036

    CAS  Article  Google Scholar 

  8. Conolly RB, Lutz WK (2004) Nonmonotonic dose-response relationships: mechanistic basis, kinetic modeling, and implications for risk assessment. Toxicol Sci Off J Soc Toxicol 77:151–157

    CAS  Article  Google Scholar 

  9. Dallaire R, Muckle G, Rouget F, Kadhel P, Bataille H, Guldner L, Seurin S, Chajès V, Monfort C, Boucher O, Thomé JP, Jacobson SW, Multigner L, Cordier S (2012) Cognitive, visual, and motor development of 7-month-old Guadeloupean infants exposed to chlordecone. Environ Res 118:79–85. https://doi.org/10.1016/j.envres.2012.07.006

    CAS  Article  Google Scholar 

  10. de Jong L, Pech N, de Aragão UG, Moreau X (2016) Multi-scale biomarker evaluation of the toxicity of a commercial azo dye (Disperse Red 1) in an animal model, the freshwater cnidarian Hydra attenuata. Water Res 96:62–73. https://doi.org/10.1016/j.watres.2016.03.043

    CAS  Article  Google Scholar 

  11. Dubuisson C, Héraud F, Leblanc J-C, Gallotti S, Flamand C, Blateau A, Quenel P, Volatier JL (2007) Impact of subsistence production on the management options to reduce the food exposure of the Martinican population to chlordecone. Regul Toxicol Pharmacol 49:5–16

    CAS  Article  Google Scholar 

  12. Eggen RIL, Behra R, Burkhardt-Holm P, Escher BI, Schweigert N (2004) Challenges in ecotoxicology. Environ Sci Technol 38(3):58A–64A. https://doi.org/10.1021/es040349c

    CAS  Article  Google Scholar 

  13. Galliot B (2012) Hydra, a fruitful model system for 270 years. Int J Dev Biol 56:411–423. https://doi.org/10.1387/ijdb.120086bg

    CAS  Article  Google Scholar 

  14. Galliot B (2013) Regeneration in Hydra. In: eLS. Wiley, Chichester. http://www.els.net. https://doi.org/10.1002/9780470015902.a0001096.pub3

    Google Scholar 

  15. Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A, Prins GS, Toppari J, Zoeller RT (2015) EDC-2: the Endocrine Society’s second scientific statement on endocrine-disrupting chemicals. Endocr Rev 36(6):E1–E150. https://doi.org/10.1210/er.2015-1010

    CAS  Article  Google Scholar 

  16. Gourcy LN, Vittecoq B (2009) Improving the knowledge of pesticide and nitrate transfer processes using age-dating tools (CFC, SF6, 3H) in a volcanic island (Martinique, French West Indies). J Contam Hydrol 108(3–4):107–117. https://doi.org/10.1016/j.jconhyd.2009.06.004

    CAS  Article  Google Scholar 

  17. Guldner L, Multigner L, Héraud F, Monfort C, Thomé J-P, Giusti A, Kadhel P, Cordier S (2010) Pesticide exposure of pregnant women in Guadeloupe: ability of a food frequency questionnaire to estimate blood concentration of chlordecone. Environ Res 110:146–151. https://doi.org/10.1016/j.envres.2009.10.015

    CAS  Article  Google Scholar 

  18. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    CAS  Article  Google Scholar 

  19. Hou L, Zhang X, Wang D, Baccarelli A (2012) Environmental chemical exposures and human epigenetics. Int J Epidemiol 41(1):79–105. https://doi.org/10.1093/ije/dyr154

    Article  Google Scholar 

  20. Jablonski PE, Pheasant DJ, Ferry JG (1996) Conversion of kepone by Methanosarcina thermophila. FEMS Microbiol Lett 139:169–173. https://doi.org/10.1016/0378-1097(96)00137-1

    CAS  Article  Google Scholar 

  21. Kashian DR (2004) Toxaphene detoxification and acclimation in Daphnia magna: do cytochrome P-450 enzymes play a role? Comp Biochem Physiol Toxicol Pharmacol CBP 137:53–63

    Article  Google Scholar 

  22. Knerr S, Schaefer J, Both S, Mally A, Dekant W, Schrenk D (2006) 2,3,7,8-Tetrachlorodibenzo-p-dioxin induced cytochrome P450s alter the formation of reactive oxygen species in liver cells. Mol Nutr Food Res 50:378–384. https://doi.org/10.1002/mnfr.200500183

    CAS  Article  Google Scholar 

  23. Ma Q, Lu AYH (2007) CYP1A induction and human risk assessment: an evolving tale of in vitro and in vivo studies. Drug Metab Dispos Biol Fate Chem 35:1009–1016. https://doi.org/10.1124/dmd.107.015826

    CAS  Article  Google Scholar 

  24. Martínez DE, Bridge D (2012) Hydra, the everlasting embryo, confronts aging. Int J Dev Biol 56(6-8):479–487

    Article  Google Scholar 

  25. Mottes C, Lesueur Jannoyer M, Le Bail M, Guéné M, Carles C, Malézieux E (2017) Relationships between past and present pesticide applications and pollution at a watershed outlet: the case of a horticultural catchment in Martinique, French West Indies. Chemosphere. 184:762–773. https://doi.org/10.1016/j.chemosphere.2017.06.061

    CAS  Article  Google Scholar 

  26. Multigner L, Ndong JR, Giusti A, Romana M, Delacroix-Maillard H, Cordier S, Jégou B, Thome JP, Blanchet P (2010) Chlordecone exposure and risk of prostate cancer. J Clin Oncol 28:3457–3462. https://doi.org/10.1200/JCO.2009.27.2153

    CAS  Article  Google Scholar 

  27. Nelson DR, Koymans L, Kamataki T, Stegeman JJ, Feyereisen R, Waxman DJ, Waterman MR, Gotoh O, Coon MJ, Estabrook RW, Gunsalus IC, Nebert DW (1996) P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics. 6(1):1–42

    CAS  Article  Google Scholar 

  28. Nóbrega-Pereira S, Fernandez-Marcos PJ, Brioche T, Gomez-Cabrera MC, Salvador-Pascual A, Flores JM, Viña J, Serrano M (2016) G6PD protects from oxidative damage and improves healthspan in mice. Nat Commun 7:10894. https://doi.org/10.1038/ncomms10894

    CAS  Article  Google Scholar 

  29. Nordberg J, Arnér ES (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287–1312

    CAS  Article  Google Scholar 

  30. Pachura-Bouchet S, Blaise C, Vasseur P (2006) Toxicity of nonylphenol on the cnidarian Hydra attenuata and environmental risk assessment. Environ Toxicol 21(4):388–394. https://doi.org/10.1002/tox.20201

    CAS  Article  Google Scholar 

  31. Quinn B, Gagné F, Blaise C (2012) Hydra, a model system for environmental studies. Int J Dev Biol 56:613–625. https://doi.org/10.1387/ijdb.113469bq

    CAS  Article  Google Scholar 

  32. Reed L, Arlt VM, Phillips DH (2018) The role of cytochrome P450 enzymes in carcinogen activation and detoxication: an in vivo-in vitro paradox. Carcinogenesis. 39(7):851–859. https://doi.org/10.1093/carcin/bgy058

    CAS  Article  Google Scholar 

  33. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108

    CAS  Article  Google Scholar 

  34. Simon HU, Haj-Yehia A, Levi-Schaffer F (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5(5):415–418

    CAS  Article  Google Scholar 

  35. Song Y, Wu WS, Gao M, Song P, Lou J, Tan Y, Liu K (2014) Transgenerational impaired male fertility with an Igf2 epigenetic defect in the rat are induced by the endocrine disruptor p,p’-DDE. Hum Reprod 29(11):2512–2521. https://doi.org/10.1093/humrep/deu208

    CAS  Article  Google Scholar 

  36. Takahashi T, Koizumi O, Ariura Y, Romanovitch A, Bosch TC, Kobayakawa Y, Mohri S, Bode HR, Yum S, Hatta M, Fujisawa T (2000) A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. Development. 127(5):997–1005

    CAS  Google Scholar 

  37. Trottier S, Blaise C, Kusui T, Johnson EM (1997) Acute toxicity assessment of aqueous samples using a microplate-based Hydra attenuata assay. Environ Toxicol Water Qual 12:265–271. https://doi.org/10.1002/(SICI)1098-2256(1997)12:3<265::AID-TOX10>3.0.CO;2-9

    CAS  Article  Google Scholar 

  38. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 33(3):378–455. https://doi.org/10.1210/er.2011-1050

    CAS  Article  Google Scholar 

  39. Veal EA, Toone WM, Jones N, Morgan BA (2002) Distinct roles for glutathione S-transferases in the oxidative stress response in Schizosaccharomyces pombe. J Biol Chem 277(38):35523–35531. https://doi.org/10.1074/jbc.M111548200

    CAS  Article  Google Scholar 

  40. Villard PH, Seree EM, Re JL, De Meo M, Barra Y, Attolini L, Dumenil G, Catalin J, Durand A, Lacarelle B (1998) Effects of tobacco smoke on the gene expression of the Cyp1a, Cyp2b, Cyp2e, and Cyp3a subfamilies in mouse liver and lung: relation to single strand breaks of DNA. Toxicol Appl Pharmacol 148(2):195–204. https://doi.org/10.1006/taap.1997.8332

    CAS  Article  Google Scholar 

  41. Woo S, Yum S, Kim DW, Park HS (2009) Transcripts level responses in a marine medaka (Oryzias javanicus) exposed to organophosphorus pesticide. Comp Biochem Physiol C Toxicol Pharmacol 149(3):427–432. https://doi.org/10.1016/j.cbpc.2008.10.100

    CAS  Article  Google Scholar 

  42. Woo S, Lee A, Won H, Ryu JC, Yum S (2012) Toxaphene affects the levels of mRNA transcripts that encode antioxidant enzymes in Hydra. Comp Biochem Physiol C Toxicol Pharmacol 156(1):37–41. https://doi.org/10.1016/j.cbpc.2012.03.005

    CAS  Article  Google Scholar 

  43. Yu HY, Guo Y, Zeng EY (2010) Dietary intake of persistent organic pollutants and potential health risks via consumption of global aquatic products. Environ Toxicol Chem 29(10):2135–2142. https://doi.org/10.1002/etc.315

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Pierre-Henri Villard.

Additional information

Publisher’s note

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

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Colpaert, R., Villard, PH., de Jong, L. et al. Multi-scale impact of chronic exposure to environmental concentrations of chlordecone in freshwater cnidarian, Hydra circumcincta. Environ Sci Pollut Res 27, 41052–41062 (2020). https://doi.org/10.1007/s11356-019-06859-4

Download citation

Keywords

  • Hydra circumcincta
  • Chlordecone
  • Endocrine-disrupting chemicals
  • Non-monotonic dose-response curves
  • Freshwater risk assessment
  • Pesticides
  • Environmental toxicology
  • Persistent organic pollutant