Phylogenomics of the epigenetic toolkit reveals punctate retention of genes across eukaryotes

Abstract

Epigenetic processes in eukaryotes play important roles through regulation of gene expression, chromatin structure, and genome rearrangements. The roles of chromatin modification (e.g., DNA methylation and histone modification) and non-protein-coding RNAs have been well studied in animals and plants. With the exception of a few model organisms (e.g., Saccharomyces and Plasmodium), much less is known about epigenetic toolkits across the remainder of the eukaryotic tree of life. Even with limited data, previous work suggested the existence of an ancient epigenetic toolkit in the last eukaryotic common ancestor. We use PhyloToL, our taxon-rich phylogenomic pipeline, to detect homologs of epigenetic genes and evaluate their macroevolutionary patterns among eukaryotes. In addition to data from GenBank, we increase taxon sampling from understudied clades of SAR (Stramenopila, Alveolata, and Rhizaria) and Amoebozoa by adding new single-cell transcriptomes from ciliates, foraminifera, and testate amoebae. We focus on 118 gene families, 94 involved in chromatin modification and 24 involved in non-protein-coding RNA processes based on the epigenetics literature. Our results indicate 1) the presence of a large number of epigenetic gene families in the last eukaryotic common ancestor; 2) differential conservation among major eukaryotic clades, with a notable paucity of genes within Excavata; and 3) punctate distribution of epigenetic gene families between species consistent with rapid evolution leading to gene loss. Together these data demonstrate the power of taxon-rich phylogenomic studies for illuminating evolutionary patterns at scales of >1 billion years of evolution and suggest that macroevolutionary phenomena, such as genome conflict, have shaped the evolution of the eukaryotic epigenetic toolkit.