DNA Methylation in the Demosponge Amphimedon queenslandica is Involved in Genome Evolution and Transcription

Abstract

DNA methylation is an epigenetic mechanism with roles that range from the fine tuning of transcription to genome wide dynamic acclimation to changing environments and regulation of developmental processes. While recent work has confirmed the presence and regulatory functions of DNA methylation in non-bilaterians, its role and distribution in Porifera has never been addressed. In this study, we performed whole genome bisulfite sequencing of the demosponge Amphimedon queenslandica and show that DNA methylation occurs mostly in CpG dinucleotides of coding regions. While high levels of gene-body methylation correlate positively with high expression and co-occur with the histone modification H3K36me3, they are not associated with amelioration of spurious transcription as found in other metazoans; nonetheless, per-exon methylation levels are predictive for exon retention suggesting a role in mRNA splicing. Additionally, analyses of Amphimedon and other sponges genomic data consistently revealed biased dinucleotide frequencies that suggest a long history of methylation-driven CpG conversion. Despite a genome wide loss of CpG dinucleotides, these are positively selected in exons and in methylated genes. These results indicate DNA methylation as a component of early metazoans regulome and challenge hypothesis on CpG methylation acting as a means for codon usage optimization.