Third-Generation Sequencing Reveals the Adaptive Role of the Epigenome in Three Deep-Sea Polychaetes

Abstract The roles of DNA methylation in invertebrates are poorly characterized, and critical data are missing for the phylum Annelida. We fill this knowledge gap by conducting the first genome-wide survey of DNA methylation in the deep-sea polychaetes dominant in deep-sea vents and seeps: Paraescarpia echinospica, Ridgeia piscesae, and Paralvinella palmiformis. DNA methylation calls were inferred from Oxford Nanopore sequencing after assembling high-quality genomes of these animals. The genomes of these worms encode all the key enzymes of the DNA methylation metabolism and possess a mosaic methylome similar to that of other invertebrates. Transcriptomic data of these polychaetes support the hypotheses that gene body methylation strengthens the expression of housekeeping genes and that promoter methylation acts as a silencing mechanism but not the hypothesis that DNA methylation suppresses the activity of transposable elements. The conserved epigenetic profiles of genes responsible for maintaining homeostasis under extreme hydrostatic pressure suggest DNA methylation plays an important adaptive role in these worms.