Chromatin profiling identifies putative dual roles for H3K27me3 in regulating cell type-specific genes and transposable elements in choanoflagellates

Chromatin-based mechanisms contribute to the exquisite regulation of gene expression during animal development. But how those mechanisms evolved remains elusive. Here we investigate chromatin regulatory features in the closest relatives of animals, choanoflagellates. In a model choanoflagellate Salpingoeca rosetta, we compare chromatin accessibility and histone modifications to gene expression. Accessible genomic regions in S. rosetta primarily correspond to gene promoters, and we find no evidence of distal gene regulatory elements that resemble enhancers deployed to regulate developmental genes in animals. Remarkably, the histone modification H3K27me3 decorates genes with cell type-specific expression, revealing a functional similarity in S. rosetta and animals. Additionally, H3K27me3 marks LTR retrotransposons, retaining a potential ancestral role in regulating these elements. We further uncover a putative bivalent chromatin state at cell type-specific genes that consists of H3K27me3 and H3K4me1. Together, these data support the emergence of gene-associated histone modification states that underpin development before the evolution of animal multicellularity.