The evolution and developmental dynamics of histone-based chromatin regulation in Annelida

Eukaryotic histones protect and package nuclear DNA into nucleosomes. The dynamic addition and removal of posttranslational modifications on these proteins define regulatory regions that play a central role in genome and chromatin biology. However, our understanding of these regulatory mechanisms in animals is largely based on a few model systems, which prevents a general understanding of how histone-based regulation unfolds and promotes phenotypic variation during animal embryogenesis. Here, we apply a comprehensive multi-omics approach to dissect the histone-based regulatory complement in Annelida, one of the largest invertebrate phyla. Annelids exhibit a conserved histone repertoire organised in clusters of dynamically regulated, hyperaccessible chromatin. However, unlike other animals with reduced genomes, the worm Dimorphilus gyrociliatus shows a dramatically streamlined histone repertoire, revealing that genome compaction has lineage-specific effects on histone-based regulation. Notably, the annelid Owenia fusiformis has two H2A.X variants that co-occur in other animals, whose functional implications are unclear but represent a unique case of widespread parallel evolution of a histone variant in Eukarya. Histone-modifying enzyme complements are largely conserved amongst annelids. Yet, temporal differences in the expression of a reduced set of histone modifiers correlate with distinct ontogenetic traits and variation in the adult landscapes of histone modifications, as revealed by quantitative mass spectrometry in O. fusiformis and Capitella teleta . Collectively, our unparalleled analysis of histone-based epigenetics within a non-model phylum informs the evolution of histone-based regulation, presenting a framework to explore how this fundamental genome regulatory layer contributes to developmental and morphological diversification in annelids and animals generally.