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Multi-Scale Impact of Chronic Exposure to Environmental Concentrations Of Multi-scale impact of chronic exposure to environmental concentrations of chlordecone in freshwater cnidarian, Hydra circumcincta Romain Colpaert, Pierre-Henri Villard, Laetitia de Jong, Marina Mambert, Karim Benbrahim, Joelle Abraldes, Claire Cerini, Valérie Pique, Maxime Robin, Xavier Moreau To cite this version: Romain Colpaert, Pierre-Henri Villard, Laetitia de Jong, Marina Mambert, Karim Benbrahim, et al.. Multi-scale impact of chronic exposure to environmental concentrations of chlordecone in freshwater cnidarian, Hydra circumcincta. Environmental Science and Pollution Research, Springer Verlag, 2020, 27 (33), pp.41052-41062. 10.1007/s11356-019-06859-4. hal-02451113 HAL Id: hal-02451113 https://hal-amu.archives-ouvertes.fr/hal-02451113 Submitted on 23 Jan 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Multi-scale impact of chronic exposure to environmental concentrations of chlordecone in freshwater cnidarian, Hydra circumcincta. Romain COLPAERT1, Pierre-Henri VILLARD1, Laetitia DE JONG1, Marina MAMBERT1, Karim BENBRAHIM1, Joelle ABRALDES1, Claire CERINI2, Valérie PIQUE1, Maxime ROBIN1, Xavier MOREAU1 1 : Aix Marseille Univ, Avignon Univ, CNRS, IRD, IMBE, Marseille, France 2 : Aix Marseille Univ, Inserm U1263, C2VN, Marseille, France Corresponding author: email : [email protected] phone : +33-(0)4-91-83-56-38 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. Keywords : Hydra circumcincta, Chlordecone, endocrine disrupting chemicals, non-monotonic dose-response curves, freshwater risk assessment, pesticides, environmental toxicology, persistent organic pollutant Introduction Chlordecone (CLD) belongs to the well-known organochlorine pesticides, which are potent Persistent Organic Pollutants (POPs). POPs are chemicals of global concern, due to (1) one or several toxic impacts on human health, (2) the long-range transport, (3) the persistence in the environment and (4) the ability to bio-magnify in food webs, leading to high bioaccumulation in apex predators, even though environmental water concentrations are low and ranged from ng/L to µg/L (Yu et al. 2010). In the French West Indies, soils, freshwaters and coastal areas have been polluted by extensive use over a twenty-year period (1972-1993) of this pesticide, especially in banana plantations to limit black weevil populations (Cosmopolites sordidus). In soils, CLD can binds strongly with organic matter and resists to biodegradation and degradation under environmental conditions (Jablonski et al. 1996; Cabidoche et al. 2009). Thus, soil contaminations lead to subsequent contamination of water, plants and animals (Dubuisson et al. 2007; Coat et al. 2011). Major impregnation of human populations occurs through daily diet of contaminated crops and animals such as fish and other aquatic food (Guldner et al. 2010). In the French West Indies, contamination of foodstuffs by CLD was associated to an increase of the prevalence of prostate cancer (Multigner et al. 2010), and to an impaired cognitive and motor development of children exposed during pregnancy and/or through breast feeding (Dallaire et al. 2012; Boucher et al. 2013). Therefore, monitoring the CLD and its effects in contaminated human environments is of a great concern. In Martinican waterways, the highest concentrations of CLD measured are around 6 µg/L and could arise 20 µg/L after major cyclonic events such as typhoons (Gourcy et al. 2009; Arnaud et al. 2013). In a recent study in the Martinique island (Mottes et al. 2017), the CLD detection frequency at the catchment outlet was 100%, and concentration varied from 0.05 to 0.77 µg/L. Furthermore, numerous organochlorine pesticides are referred as Endocrine Disrupting Chemicals (EDCs) (Gore et al. 2015). EDCs are well known compounds able to alter physiological functions of the endocrine system. Consequently, EDC exposures lead to severe adverse health effects in adults, but also on their progeny and therefore impact reproduction and fitness of wild populations. It has been reported that EDCs could exert deleterious effects in both human and fauna at low environmental concentrations, and that the effects do not follow classical dose-response curves (Gore et al., 2015). In this context, it would be of interest to use water sentinel organisms able to respond to environmental low concentrations of pollutants. Among candidates, the freshwater Hydra sp. is a suitable animal model for ecotoxicological investigations (Galliot, 2012; Quinn et al., 2012; de Jong et al. 2016), as it allows to study multi-scale biological endpoints from genes to population, which makes this cnidarian a sensitive environmental indicator. Numerous advantages of this model include the asexual reproduction, leading to clone populations with a negligible genetic interindividual variations, and the simple body plan organization of the diploblastic polyp, leading to direct contact between all body cells and the exposure media. Finally, the evaluation by qRT-PCR analyses of the expression of some stress genes can be easily performed and is inexpensive (Woo et al. 2012). The objective of our study was to evaluate in the freshwater hydra (Hydra circumcincta), the effects of chronic exposure to low concentrations of CLD, compatible with environmental exposure, on the expression of some target stress genes, the morphology, and the asexual reproduction rates. According to Eggen et al. (2004), low concentrations of pollutants and long exposure time (i.e. chronic effects) as well as multiple effects by single pollutants are two great challenges in ecotoxicological studies. Materials and Methods Chemicals and reagents Pure CLD was provided as a powder from Azur Isotopes (Marseille, France), with a purity greater than 97 %, and was diluted in pure water at a concentration of 1 mg/L. All the solutions were stored in the dark at 4°C. The stock solutions of CLD for expositions were freshly prepared in TES buffer (Sigma-Aldrich, Saint Quentin-Fallavier, France), the hydra breeding media. Isopropanol was purchased from Sigma (L'Isle d'Abeau, France). Chloroform (99%), and ethanol (75%) were from Carlo Erba® Reagents (Val-de-Reuil, France). Moloney Murine Leukemia Virus Reverse Transcriptase was from In Vitrogen/Thermo-Fischer (Cergy- Pontoise, France). PCR Water Nuclease Free, 5x HOT Pol Evagreen® qPCR Mix Plus, and Tri-Reagent™ were from Euromedex (Souffelweyersheim, France). Biological material and culture conditions Before expositions, the population of Hydra circumcincta polyps was raised at a constant temperature of 20°C ± 0.1°C, with a 12/12h light-dark cycle in TES buffer (0.1 mM; pH 7), as previously described by de Jong et al. (2016). Culture maintenance procedure was adapted from that developed by Trottier et al. (1997). The polyps were fed every three days with 24h hatched Artemia sp. nauplii. All specimens used in this experiment arise from a single polyp and thus belong to the same clone. Chlordecone chronic toxicity assay Exposure protocol is based on that of de Jong et al. (2016). All solutions were prepared in TES buffer, and the CLD concentrations ranged from 0.1 µg/L to 20 µg/L. Experiments were carried in sterile 6-well polystyrene microplates. Using a stereo-microscope, non-budding H. circumcincta polyps of similar size were randomly collected among a dense healthy population (Trottier et al. 1997). The multi-well microplates were placed into a thermo-regulated incubator at 20 0.1°C
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