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Lymnaea Stagnalis by Maël Dugué © The compact disc on the opposite page contains: • PDF version of the Thesis • Figures presented in the Thesis • Tables presented in the Thesis • Supplementary material of the Part 4: chapter 6 Cover page photography: Lymnaea stagnalis by Maël Dugué © Résumé Des molécules connues pour leur capacité d’interférer avec le système endocrinien des vertébrés peuvent engendrer, à de faibles concentrations, des effets néfastes sur la reproduction des invertébrés. Ces produits, appelés perturbateurs endocriniens, peuvent à terme avoir des conséquences préjudiciables sur la croissance et la survie des populations exposées. Parmi les espèces d’invertébrés touchées par les perturbateurs endocriniens, les mollusques voient leur reproduction affectée par de nombreuses molécules à des concentrations inférieures que celles atteignant d’autres phyla. Les mollusques ont donc été proposés comme espèce-modèle pour l’évaluation de la reprotoxicité des produits chimiques, dont font partie les perturbateurs endocriniens, dans les guidelines développées par l’OCDE. Lymnaea stagnalis, une espèce de gastéropode dulçaquicole hermaphrodite, a été proposée comme espèce de référence pour le développement de ce type de test. Le premier objectif de cette thèse consiste à définir les impacts de différentes molécules, choisies sur base de leurs interactions avec le système endocrinien des vertébrés, sur la reproduction de L. stagnalis. Son deuxième objectif vise à apporter une meilleure compréhension des mécanismes d’action de ces perturbateurs endocriniens. Dans ce travail, nous avons testé plusieurs produits choisis sur base de leurs interactions avec le système endocrinien des vertébrés. La testostérone est le ligand naturel du récepteur aux androgènes. Trois autres molécules sont des antagonistes avérés de ce récepteur : l’acétate de cyprotérone qui est un stéroïde synthétique, la vinclozoline qui est un fongicide dicarbamide, et le fénitrothion qui est un insecticide organophosphoré. La chlordécone, un pesticide organochloré, peut se lier au récepteur aux oestrogènes. Enfin, les deux organoétains, triphenyltin (TPT) and tributyltin (TBT), peuvent induire une masculinisation des femelles, consistant en la formation additionnelle de caractères masculins (l’imposexe) chez les gastéropodes prosobranches. Les résultats de ce travail sont divisés en deux volets. Le premier regroupe les résultats obtenus sur les impacts de ces substances sur la reproduction de L. stagnalis. Le nombre total d’œufs (fécondité) et de pontes (oviposition) produits par individu sur toute la période d’exposition à ces molécules nous a permis d’évaluer l’impact des différentes substances. De plus, l’analyse de la qualité des œufs produits a montré que toutes les molécules testées, excepté le TPT, peuvent augmenter la fréquence des œufs malformés produits par les individus exposés. Les œufs polyembryonés (contenant plusieurs embryons par œuf) sont les plus fréquemment produits parmi tous les œufs malformés. Etant donné que ces effets sur la qualité des œufs sont observés à des concentrations plus faibles que celles affectant l’oviposition et la fécondité, l’inclusion de ce paramètre lors de l’analyse des impacts de reprotoxicité sur L. stagnalis pourrait améliorer la sensibilité des tests, particulièrement pour l’étude des perturbateurs endocriniens. Le second volet des résultats, présentés dans les chapitres 3 et 4, nous a permis de mieux comprendre les mécanismes d’action des molécules induisant des effets sur la reproduction de L. stagnalis suite à des interactions probables avec le système endocrinien de cette espèce. Dans le chapitre 5, nous avons analysé les impacts de la testostérone, de l’acétate de cyprotérone, de la chlordécone et du tributylétain sur les concentrations en testostérone sous forme libre et estérifiée présentes dans les tissus d’individus exposés pendant 21 jours. La testostérone est une hormone stéroïdienne de « type vertébré » qui a été isolée dans les tissus de nombreuses espèces de mollusques. Nos résultats ont confirmé que les lymnées peuvent incorporer ce stéroïde depuis le milieu environnant. De plus, chez cette espèce comme chez d’autres espèces de mollusques, une régulation homéostatique des concentrations en testostérone permet de stocker, dans les tissus adipeux, les excès de testostérone en forme libre sous une forme estérifiée. Cependant, dans le premier volet des résultats, les impacts de ces molécules sur la reproduction n’ont pu être mis en relation avec les modifications des concentrations en testostérone. Dès lors, le rôle joué par cette hormone stéroïde dans la reproduction de la lymnée n’a pu être élucidé. Dans le chapitre 6, des analyses protéomiques (2D-DIGE, western blot) ont été réalisées afin d’identifier les impacts de la testostérone, de l’acétate de cyprotérone, de la chlordécone et du tributylétain sur l’expression de protéines extraites des tissus reproducteurs des individus exposés pendant 21 jours. Ces techniques d’analyse nous ont permis d’identifier des protéines qui jouent un rôle dans la reproduction de cette espèce (yolk ferritin, ovipostatin et PIWI). Les altérations d’expression de ces protéines pourraient expliquer les effets de ces molécules sur la reproduction de L. stagnalis observés dans les chapitres précédents. En intégrant les résultats obtenus au cours de cette thèse, il apparaît que les produits testés peuvent induire des impacts néfastes sur la reproduction en interagissant avec le système endocrinien de Lymnaea stagnalis. De plus, l’étude de la qualité des œufs, ainsi que l’analyse de protéines impliquées dans la reproduction, constituent indéniablement des outils utiles pour évaluer la reprotoxicité de ces molécules chez Lymnaea stagnalis. Summary Adverse impacts exerted by molecules called endocrine disruptors on reproduction have been extensively described in vertebrates. However, endocrine-disrupting chemicals might alter reproduction of invertebrate species, at lower concentrations or through different modes of action, with consequences on population growth and stability. Among invertebrates, molluscs have been shown to be very sensitive to endocrine disruptors and were therefore proposed as model species for the development of OECD guideline for the testing and the assessment of reprotoxic effect of chemicals, including EDCs. The hermaphrodite gastropod species Lymnaea stagnalis is a candidate species for the development of such guidelines. In this context, the aim of this thesis is to provide a better understanding of the impacts and the mechanisms of action of endocrine disrupting chemicals on the reproduction of L. stagnalis. The chemicals tested in the present work were chosen based on their interactions with the endocrine system of vertebrates. Testosterone is the natural ligand of the androgen receptor in vertebrates. Three different molecules were selected for their antagonism of the androgen receptor in vertebrates: the synthetic steroid cyproterone acetate, the dicarbamide fungicide vinclozolin and the organophosphate insecticide fenitrothion. Chlordecone is an organochlorinated pesticide, which binds oestrogen receptors in vertebrates. Finally, two organotin compounds, triphenyltin and tributyltin, are able to induce the development of imposex, imposition of male sex organs in females, in gonochoric gastropod molluscs. Results of the present work are divided into two main sections. Firstly, we investigated the impacts of the selected chemicals on the reproduction of L. stagnalis. Our results displayed that TBT, TPT, and chlordecone are able to induce adverse impacts on the reproduction of L. stagnalis through a reduction of the cumulative number of eggs and clutches produced per individual. The assessment of the quality of eggs produced showed that exposure to the chemicals, except TPT, increases the frequency of abnormal eggs laid. The impacts on egg quality were observed at lower concentrations than those affecting the classical reproductive endpoints assessed in reprotoxicity tests in this species. Our results highlight that the implementation of egg quality as an endpoint should increase the sensitivity of the reprotoxicity test with L. stagnalis. The second section of results aims at providing new insights on the mechanisms of action of putative endocrine disruptors in L. stagnalis. Results from chapter 3 and 4 allowed us to select chemical treatments (testosterone, tributyltin, cyproterone acetate, and chlordecone) that induced adverse effects, by interacting with the endocrine system, on the reproduction of L. stagnalis. In Chapter 5, we analysed endogenous concentrations of testosterone, in its free and esterified forms, in the reproductive organs of L. stagnalis. Exposure to waterborne testosterone has confirmed that molluscs can take up this steroid from environmental media and that a homeostatic regulation of endogenous concentrations occurs through the esterification of steroids to fatty acid esters. Moreover, our results support that testosterone is endogenously synthesised in L. stagnalis, as it has been suggested in other mollusc species. However, the impacts on the reproduction and the modifications of endogenous concentrations of testosterone reported in this thesis could not be associated. In chapter 6, proteomic experiments were used to identify proteins differently expressed in reproductive organs of L. stagnalis exposed to testosterone, tributyltin, cyproterone acetate, and chlordecone. Modifications in the expression of three proteins involved in L. stagnalis reproduction
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