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Hydra bioassay for the evaluation of chlordecone toxicity at environmental concentrations, alone or in complex mixtures with dechlorinated byproducts: experimental observations and modeling by experimental design

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Abstract

In chlordecone (CLD)-contaminated soils of the French West Indies, if microbial remediation or a physicochemical remediation process, e.g., in situ chemical reduction, is implemented, concentrations of degradation byproducts, such as hydrochlordecones, are expected to increase in the ecosystems. To study their impact in mixtures with CLD, bioassays were carried out. They consisted in evaluating the regenerative capacity of hydra polyps, from a clone whose phylogenetic analysis confirmed that it belonged to the species Hydra vulgaris Pallas, 1766. Hydra gastric sections were exposed to CLD alone or CLD plus dechlorinated byproducts (CLD-BP) for 96 h to assess regeneration. Based on chromatographic analysis, the CLD-BP mix was composed of the 5-monohydrochlordecone isomer (CAS nomenclature), four dihydrochlordecone isomers, and one trihydrochlordecone isomer representing 50%, 47%, and 3% of the total chromatographic area, respectively. A total of 18 mixtures of CLD and CLD-BP were tested. Six environmental concentrations of CLD (2.10−4 μM to 4.10−2 μM) and a similar range of CLD-BP were used. Results from exposures to CLD alone showed the following: (i) a significant decrease in the regenerative capacity of hydra, except at the lowest concentration (2.10−4 μM); (ii) a concentration-independent deleterious effect. The regeneration scores obtained after the exposure to the addition of CLD-BP were not significantly different from those obtained after exposure to CLD alone. Using an experimental design, a modeling of the regeneration scores of hydra exposed to mixtures is proposed. Interpreted carefully, since they are limited to only one type of bioassay, the present results suggest that the situation in the aquatic environments should not become worse in terms of toxicity, if soil remediation programs resulting in the formation of hydrochlordecones are put in place.

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Notes

  1. Ability to promote vascularization and tumor growth.

  2. GC-EI-MS: Gas Chromatography – Electronic Impact – Mass Spectrometry.

  3. LC-MS: Liquid Chromatography – Mass Spectrometry.

  4. A coaffective teratogen is a substance that is not primarily targeted at development but can disrupt it.

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Acknowledgements

We thank Professor Christian Blaise (Environment Canada), Dr Sophie Pachura (Agestra, France) and Professor Paule Vasseur (Université de Lorraine, France) for their help in reconstructing the laboratory history of the Hydra IMBE1 strain. Special thanks to Dr Stéphane Greff (Chemical Ecology and Metabolomics facility at IMBE) and Dr Pierre Vanloot who led the analysis of CLD-BP by UHPLC-ESI-qToF and GC-EI-MS, respectively. Thanks to our students, Margot Cardenas-Saavedra, Estelle Levert, Nicolas Martin, Elisa Viande, and Gaëlle Zanzana, who performed some of the exposure experiments during their laboratory internship. The authors are grateful to the two anonymous reviewers whose constructive and insightful comments substantially improved the manuscript.

Funding

This work was financed in part by the European Regional Development Fund (FEDER) through the RIVAGE project (MQ0003772-CIRAD) and by an internal grant from the IMBE research unit to stimulate cooperation between several of its teams. Jean-Pascal Andraud received a PhD grant from the doctoral school ED251 Environmental Sciences of Aix Marseille University.

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Laetitia De Jong and Xavier Moreau contributed to the overall conception and design of the study and carried out most of the exposure experiments with the help of Jean-Pascal Andraud. Magalie Claeys-Bruno and Michelle Sergent contributed to the design of the experimental matrix and the development of the mathematical model. Daniel E Martínez performed the phylogenetic analysis of the hydra clone IMBE1. Hervé Macarie contributed to the selection of (1) the dechlorinated byproducts (CLD-BP) to be used in the study and (2) the range of CLD and CLD-BP concentrations that are representative of the French West Indies environments. He also contributed to the literature search, reconstruction of the laboratory history of the IMBE1 hydra clone, and analysis of mass spectra of CLD-BPs to identify possible isomers. Maxime Robin synthesized the CLD standard used in the study. All authors contributed to the analysis of the results. The first version of the manuscript was written by Laetitia de Jong and Xavier Moreau, and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Laetitia De Jong.

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The manuscript is an original study and has not been submitted elsewhere in any form or language, but some of the results were presented, in French, at the congress of the “Groupement Français de Recherche sur les Pesticides,” GFP (May 20, 2021; http://www.gfpesticides.org/congres/579/593-20-mai-2021.html) in the form of a commented slideshow.

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All authors approved the content and gave their explicit consent to submit the manuscript. They obtained consent from their research laboratory and the university where the work was performed.

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The authors declare no competing interests.

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Moreau, X., Claeys-Bruno, M., Andraud, JP. et al. Hydra bioassay for the evaluation of chlordecone toxicity at environmental concentrations, alone or in complex mixtures with dechlorinated byproducts: experimental observations and modeling by experimental design. Environ Sci Pollut Res 29, 91017–91035 (2022). https://doi.org/10.1007/s11356-022-22050-8

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  • DOI: https://doi.org/10.1007/s11356-022-22050-8

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