A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution

Abstract

Histones and associated chromatin proteins have essential functions in eukaryotic genome organization and regulation. Despite this fundamental role in eukaryotic cell biology, we lack a phylogenetically-comprehensive understanding of chromatin evolution. Here, we combine comparative proteomics and genomics analysis of chromatin in eukaryotes and archaea. Proteomics uncovers the existence of histone post-translational modifications in Archaea. However, archaeal histone modifications are scarce, in contrast with the highly conserved and abundant marks we identify across eukaryotes. Phylogenetic analysis reveals that chromatin-associated catalytic functions (e.g., methyltransferases) have pre-eukaryotic origins, whereas histone mark readers and chaperones are eukaryotic innovations. We show that further chromatin evolution is characterized by expansion of readers, including capture by transposable elements and viruses. Overall, our study infers detailed evolutionary history of eukaryotic chromatin: from its archaeal roots, through the emergence of nucleosome-based regulation in the eukaryotic ancestor, to the diversification of chromatin regulators and their hijacking by genomic parasites.

A developmental role for the chromatin-regulating CoREST complex in the cnidarian Nematostella vectensis

“…Using a literature and homology-based approach we searched for core components of the CoREST complex in the genomes of a representative group of eukaryotes (see materials and methods and Additional file 1 : Table S1). Lsd1 and HDAC1/2 are found across eukaryotes and are thought to have been present in the last common eukaryotic ancestor [ 10 , 52 – 55 ]. CoREST orthologs, on the other hand, have a more complex evolutionary history.…”

“…The presence/absence of orthologs of Lsd1 and HDAC1/2 in different groups was extracted from existing literature [ 10 , 52 – 55 ]. The presence of choanoflagellate Lsd1 orthologs was assessed by reciprocal blast searches in the genomes of Salpingoeca rosetta and Monosiga brevicollis.…”

“…Most chromatin regulators are ancient and predate the evolution of animal multicellularity [ 10 ]. One possible way to evolve new roles in developmental programs is the integration of chromatin regulators into multiprotein complexes that facilitate the coordination of different regulatory (e.g.…”

The ancestral chromatin landscape of land plants

“…Although some PTMs are restricted to specific lineages, many PTMs are conserved and are found in similar genomic contexts across eukaryotes (Grau-Bové et al, 2022;Sequeira-Mendes et al, 2014;.…”

“…Although a plethora of PTMs have been identified, the most conserved modifications are methylation, phosphorylation, and acetylation of H2A, H2B, and H3 (Allis and Jenuwein, 2016). Although some PTMs are restricted to specific lineages, many PTMs are conserved and are found in similar genomic contexts across eukaryotes (Grau-Bové et al, 2022; Sequeira-Mendes et al, 2014; Jamge et al, 2022).…”