Integration of epigenetics into ecotoxicology: insights and fundamental research needs

Epigenetics refers to heritable changes in genome function that occur without direct alterations to the DNA sequence. A multitude of environmental contaminants can influence the epigenetic marks of a genome. Changes of epigenetic marks including DNA methylation, histone modifications, and non-coding RNAs can induce alterations at the gene transcription level, potentially leading to physiological long-term changes that can be inherited transgenerationally. (Eco)Toxicoepigenetics is thus an emerging field of research focusing on linking environmental exposure with epigenome alterations, with a high postulated relevance for improved ecological risk assessment at the regulatory level. Despite its huge potential, fundamental knowledge is scarce and scattered concerning epigenetic regulation in relevant ecotoxicological model species and mechanisms of interaction between environmental contaminants and the epigenome. This is a paramount challenge for the efficient implementation of (eco)toxicoepigenetics that is not often recognised in the literature. Herein, we provide updated knowledge regarding the main epigenetic modifications that occur on ecotoxicologically relevant models and summarize the differences in epigenetic patterns between vertebrate and invertebrate species that are routinely used as test organisms in ecotoxicology. We also systematically revise what is known on the mechanisms through which environmental contaminants can modulate the epigenome, using three legacy contaminants of the aquatic compartment for which appreciable information exists concerning ecotoxicologically relevant species. Future directions for (eco)toxicoepigenetics research are discussed in the context of the existing knowledge, with particular emphasis on the much-needed characterization of the epigenomes of ecotoxicological models and the need to understand better the mechanisms underlying the modulation of epigenetic marks and related machinery by environmental contaminants. This review will hopefully stimulate future research contributing to the continuous incorporation of epigenetic studies in ecotoxicology and the development and implementation of effective epigenetic-based ecotoxicological biomarkers for environmental stress assessment.