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Genotoxic and epigenetic effects of diuron in the Pacific oyster: in vitro evidence of interaction between DNA damage and DNA methylation

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Abstract

Recently, research has contributed to better knowledge on the occurrence of pesticides in coastal water by identifying frequently detected substances, their concentration range and their acute and chronic toxicity for organisms. Pesticide pollution is of particular concern in France due to important agricultural activities and presence of several exoreic catchment areas that vehicle pesticides up to coastal waters, impacting non-target marine species. Several ecotoxicology questions remain to be addressed concerning the long-term effects of chronic pesticide exposure and the mechanisms involved in adaptation to chemical stress. In the present study, we brought new insights on the genetic and epigenetic effects of the herbicide diuron in oyster genitors. During gametogenesis, we exposed Crassostrea gigas to environmentally realistic herbicide concentrations (0.2–0.3 μg L−1 during two 7-day periods at half-course and end of gametogenesis). Diuron exposure was shown to decrease global DNA methylation and total methyltransferase activity in whole oyster tissue; this is consistent with the previous observation of a significant decrease in DNMT1 gene expression. Diuron effect seemed to be tissue-specific; hypermethylation was detected in the digestive gland, whereas diuron exposure had no effect on gill and gonad tissue. The genotoxicity of diuron was confirmed by the detection of one adduct in gonad DNA. By using in vitro approaches and human DNMT1 (DNMT1 has not been purified yet in bivalves), the presence of DNA lesions (adduct, 8-oxodGuo) was shown to interfere with DNMT1 activity, indicating a complex interaction between DNA damage and DNA methylation. Based on our results, we propose mechanisms to explain the effect of diuron exposure on DNA methylation, a widespread epigenetic mark.

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Data availability

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

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Funding

This work was supported by the French National Agency for Research (GIMEPEC project, ANRCESA-01601) and the French Research Institute for Sea Exploration (Ifremer).

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Authors and Affiliations

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Contributions

F. Akcha, A. Barranger and E. Bachère designed the experiment and participated to the experimentation and sampling operations. E. Bachère performed the gene expression analysis. F. Akcha measured global DNA methylation level and activity, and human DNMT1 activity using different substrates. A. Barranger measured 8-oxodGuo levels. Adduct analysis has been subcontracted to ADn’tox Society. F. Akcha wrote the manuscript which was read and approved by the two co-authors.

Corresponding author

Correspondence to Farida Akcha.

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Ethical approval

All procedures performed in the invertebrate Pacific oyster C. gigas were in accordance with the ethical standards.

Competing interests

The authors declare that they have no conflict of interest.

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Responsible Editor: Philippe Garrigues

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Akcha, F., Barranger, A. & Bachère, E. Genotoxic and epigenetic effects of diuron in the Pacific oyster: in vitro evidence of interaction between DNA damage and DNA methylation. Environ Sci Pollut Res 28, 8266–8280 (2021). https://doi.org/10.1007/s11356-020-11021-6

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  • DOI: https://doi.org/10.1007/s11356-020-11021-6

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