Temperature influences histone methylation and mRNA expression of the Jmj-C histone-demethylase orthologues during the early development of the oyster Crassostrea gigas

In many groups, epigenetic mechanisms influence developmental gene regulation under environmental inputs. The Pacific oyster Crassostrea gigas belongs to lophotrochozoans and its larval development is highly dependent on temperature, but the role of epigenetic mechanisms in this context is unknown despite high levels of the recently characterized Jumonji histone demethylase (JHDM) orthologues (Cg_Jumonji) suggesting a physiological relevance of histone methylation in the oyster development. Because in other species alterations of the histone methylation pattern have deleterious outcomes, we investigated the influence of temperature during the oyster larval life on histone methylation and JHDM expression. To shed light on this point, oyster embryonic and early larval development experiments were carried out at different temperatures (18 °C, 25 °C and 32 °C). Histone methylation levels were investigated using fluorescent ELISA at 6 and 24 h post-fertilization. When compared to the 25 °C group, at 18 °C H3K4, H3K9 and H3K27 residues were hypomethylated at 6 h post fertilization (hpf) and hypermethylated at 24 hpf. In contrast, at 32 °C, 6 hpf animals present a dramatic hypermethylation (ca. 4-fold) of all examined residues, which is minored but sustained at 24 hpf. RT-qPCR investigations of the mRNA expression of the nine oyster JHDMs, showed gene- and stage-specific temperature sensitivities throughout the early life of oysters. This study provides evidence of the biological significance of histone methylation during development in a lophotrochozoan species. Our results also indicate that temperature influences histone methylation, possibly through the expression level of putative actors of its regulation, which might participate in developmental control. To our knowledge, this is the first report indicating a direct relationship between an epigenetic mark and an environmental parameter in marine molluscs. Such investigations could help better understand the molecular mechanisms of development and adaptation in lophotrochozoans.