The role of salinity on genome‐wide DNA methylation dynamics in European sea bass gills

Abstract

Epigenetic modifications, like DNA methylation, generate phenotypic diversity in fish and ultimately lead to adaptive evolutionary processes. Euryhaline marine species that migrate between salinity‐contrasted habitats have received little attention regarding the role of salinity on whole‐genome DNA methylation. Investigation of salinity‐induced DNA methylation in fish will help to better understand the potential role of this process in salinity acclimation. Using whole‐genome bisulfite sequencing, we compared DNA methylation patterns in European sea bass (Dicentrarchus labrax) juveniles in seawater and after freshwater transfer. We targeted the gill as a crucial organ involved in plastic responses to environmental changes. To investigate the function of DNA methylation in gills, we performed RNAseq and assessed DNA methylome‐transcriptome correlations. We showed a negative correlation between gene expression levels and DNA methylation levels in promoters, first introns and first exons. A significant effect of salinity on DNA methylation dynamics with an overall DNA hypomethylation in freshwater‐transferred fish compared to seawater controls was demonstrated. This suggests a role of DNA methylation changes in salinity acclimation. Genes involved in key functions as metabolism, ion transport and transepithelial permeability (junctional complexes) were differentially methylated and expressed between salinity conditions. Expression of genes involved in mitochondrial metabolism (tricarboxylic acid cycle) was increased, whereas the expression of DNA methyltransferases 3a was repressed. This study reveals novel links between DNA methylation, mainly in promoters and first exons/introns, and gene expression patterns following salinity change.

Unravelling the molecular mechanisms of fish salinity adaptation in the face of multiple stressors: A comparative multi-tissue transcriptomic study in the Llobregat River, Barcelona, Spain

“…Another set of relevant pathways are those related to neurogenesis and eye development have been related to the effect multiple chemical stressors in previous transcriptomic studies (Meade et al, 2023), and in our case can be related to the multiple stressors that act together with salt pollution in the Llobregat River. Interestingly, the "methylation" pathway was enriched in all tissues, and in the liver, "histone modification," as suggested by a recent study coupling methylation and transcriptomics in a euryhaline fish, indicates methylation changes and gene expression patterns under salinity stress (Blondeau Bidet et al, 2023). As we are investigating the transcriptomic response of three tissues in a field setting where multiple stressors act simultaneously, and the complexity of the enriched metabolic pathways and their interplay increases, a thorough discussion of all enriched pathways would be beyond the scope of this study.…”

“…KCNN3 is a potassiumactivated channel that has been proven to be differentially expressed in euryhaline fish exposed to osmotic stress (Bonzi et al, 2021). The potassium channels KCNT1 and KCNT2 are activated under high concentrations of chloride and be differentially expressed in euryhaline fish exposed to osmotic stress (Blondeau Bidet et al, 2023;Lüscher et al, 2020). RYR2 and RYR3 are known interaction partners in the formation of chloride channels that are key in several physiological processes, including osmoregulation (Zeng et al, 2018).…”