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 by 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 expression; inverted "U-shaped" curves for GPx and CYP1A gene expression, and reproductive rates; as well as 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.

Effects of mixtures containing chlordecone and a dechlorinated by-product on hydra regeneration capacity: use of experimental design to evaluate the toxicity risk associated with remediation programs in long-lasting polluted areas

“…Previous authors have pointed out that EDs could have higher or similar effects at low concentrations than at higher concentrations(Gore et al 2015;Vandenberg et al 2012). In accordance with previous studies using adult hydra polyps(Colpaert et al 2020), our results show the need to investigate biological effects after exposure to low CLD concentrations. Using the same hydra clone as in present work,Colpaert et al (2020) have shown asexual reproduction impairments, morphological damages, and modulations of the expression of target genes involved in oxidative stress, detoxi cation, and neurobiological processes after exposure to low concentrations of CLD (0.1 µg.L -1 ).…”

“…In accordance with previous studies using adult hydra polyps(Colpaert et al 2020), our results show the need to investigate biological effects after exposure to low CLD concentrations. Using the same hydra clone as in present work,Colpaert et al (2020) have shown asexual reproduction impairments, morphological damages, and modulations of the expression of target genes involved in oxidative stress, detoxi cation, and neurobiological processes after exposure to low concentrations of CLD (0.1 µg.L -1 ). In the same way, using the giant freshwater prawn Macrobrachium rosenbergii, a crustacean living in FWI,Gaume et al (2015) have also pointed out the necessity to investigate biological effects of low environmental concentrations of CLD.…”

“…Thus, whereas the teratogenic effect could be explained by the presence of CLD in the mixtures, it was not dependent on an increase in CLD concentrations. Such stochastic phenomenon has been also recently described concerning several biological endpoints in hydra entire polyps under exposure to CLD: reproductive rates, morphological changes, and expression of target stress genes (Colpaert et al 2020). Therefore, our results con rm the previous observations of Colpaert et al…”

“…The CLD concentrations were in the range of those measured in FWI surface freshwaters (Lesueur-Jannoyer et al 2016, Mottes et al 2020). Hydra was chosen as a freshwater animal model for the study because it has been already used in a recent work to assess the effect of long-term exposure of CLD on several biological markers such as stress gene expression, oxidative stress endpoints and reproduction rate (Colpaert et al 2020). The pertinence of this choice has been reinforced recently by the nding that Hydra species are ubiquitous in FWI surface waters (Macarie and Martínez, unpublished results).…”

“…1.4 µg.L −1 of CLD) and variable increasing CLD-3Cl concentrations (experiments 16, 17 and 18); three mixtures containing 2.88 10 −3 µM of CLD-3Cl and variable increasing CLD concentrations (experiments 14, 15 and 18). The choice of the 2.88 10 −3 µM concentration of CLD was supported by the study ofColpaert et al (2020), that have demonstrated stochastic "endocrine disruptor effect" at a concentration of 1 µg.L −1 of CLD for several biological endpoints after 14-day exposure of entire polyps of the same Hydra species.…”