Transgenerational Inheritance of DNA Hypomethylation inDaphnia magnain Response to Salinity Stress

Abstract

Epigenetic mechanisms have been found to play important roles in environmental stress response and regulation. These can, theoretically, be transmitted to future unexposed generations, yet few studies have shown persisting stress-induced transgenerational effects, particularly in invertebrates. Here, we focus on the aquatic microcrustacean Daphnia, a parthenogenetic model species, and its response to salinity stress. Salinity is a serious threat to freshwater ecosystems and a relevant form of environmental perturbation affecting freshwater ecosystems. We exposed one generation of D. magna to high levels of salinity (F0) and found that the exposure provoked specific methylation patterns that were transferred to the three consequent nonexposed generations (F1, F2, and F3). This was the case for the hypomethylation of six protein-coding genes with important roles in the organisms' response to environmental change: DNA damage repair, cytoskeleton organization, and protein synthesis. This suggests that epigenetic changes in Daphnia are particularly targeted to genes involved in coping with general cellular stress responses. Our results highlight that epigenetic marks are affected by environmental stressors and can be transferred to subsequent unexposed generations. Epigenetic marks could therefore prove to be useful indicators of past or historic pollution in this parthenogenetic model system. Furthermore, no life history costs seem to be associated with the maintenance of hypomethylation across unexposed generations in Daphnia following a single stress exposure.

Prospects for incorporation of epigenetic biomarkers in human health and environmental risk assessment of chemicals

“…In Daphnia magna , a key species in regulatory ecotoxicological assessment, Jeremias et al . () and Trijau et al . () monitored methylation changes that occurred when organisms were exposed to high salinity levels and chronic γ irradiation, respectively.…”

“…Daphnia and Artemia are two suitable invertebrate candidates: in species of both genera, epigenetic marks that potentially serve as biological markers of exposure have already been identified for several natural stressors (Norouzitallab et al ., ; Trijau et al ., ; Jeremias et al ., ). Both have great potential as epigenetic model organisms since there is a very large ecological, ecotoxicological and evolutionary literature available for these species, and clonal populations can be easily established and maintained in the laboratory (Harris et al ., ; Granada et al ., ; Norouzitallab et al ., ).…”

“…Supporting this claim, the authors provided evidence that certain classes of chemicals can induce class‐specific alterations to normal DNAm patterns (Mirbahai & Chipman, ). Epigenetic biomarkers can reflect present and/or previous stress exposures throughout an organisms' lifetime, but also inform on parental germ cell exposures, depending on the nature of the exposure and the development stages affected (Manikkam et al ., ; Ly et al ., ; Trijau et al ., ; Jeremias et al ., ). Within this field, several major challenges remain.…”

“…In parallel to advances in medicine, the epigenetic machinery of model species in environmental studies is known to respond to several environmental stressors (Vandegehuchte & Janssen, ; Jeremias et al ., ; Norouzitallab et al ., ). Several experimental studies have now confirmed that epigenetic marks/patterns are inherited in numerous organisms (Jeremias et al ., ; Norouzitallab et al ., ). Thus, epigenetic biomarkers have great potential in environmental quality assessment.…”

“…Importantly, some of these environmentally induced epigenetic marks/patterns have been demonstrated to be reversible when the environmental inducer is no longer present, but some can be mitotically/meiotically inherited through a process known as epigenetic transgenerational inheritance (Bird, ; Ho & Burggren, ; Walker, Kublin & Zunt, ; Blake & Watson, ; Burggren, ). This phenomenon has been shown to occur in several organisms, including model species in diverse scientific fields (Rando, ; Kamstra et al ., ; Trijau et al ., ; Jeremias et al ., ). As epigenetic mechanisms regulate gene expression, the consequence of a given environmental stressor in this context can be a change in the phenotype of cells and organisms (environmentally induced epigenetic phenotypes).…”