Environmental Epigenetics in Soil Ecosystems: Earthworms as Model Organisms

One of the major emerging concerns within ecotoxicology is the effect of environmental pollutants on epigenetic changes, including DNA methylation, histone modifications, and non-coding RNAs. Epigenetic mechanisms regulate gene expression, meaning that the alterations of epigenetic marks can induce long-term physiological effects that can even be inherited across generations. Many invertebrate species have been used as models in environmental epigenetics, with a special focus on DNA methylation changes caused by environmental perturbations (e.g., pollution). Among soil organisms, earthworms are considered the most relevant sentinel organisms for anthropogenic stress assessment and are widely used as standard models in ecotoxicological testing of soil toxicity. In the last decade, several research groups have focused on assessing the impact of environmental stress on earthworm epigenetic mechanisms and tried to link these mechanisms to the physiological effects. The aim of this review is to give an overview and to critically examine the available literature covering this topic. The high level of earthworm genome methylation for an invertebrate species, responsiveness of epigenome to environmental stimuli, availability of molecular resources, and the possibility to study epigenetic inheritance make earthworms adequate models in environmental epigenomics. However, there are still many knowledge gaps that need to be filled in, before we can fully explore earthworms as models in this field. These include detailed characterization of the methylome using next-generation sequencing tools, exploration of multigenerational and transgenerational effects of pollutants, and information about other epigenetic mechanisms apart from DNA methylation. Moreover, the connection between epigenetic effects and phenotype has to be further explored.