The landscape of the histone-organized chromatin of Bdellovibrionota bacteria
Histone proteins have traditionally been thought to be restricted to eukaryotes and most archaea, with eukaryotic nucleosomal histones deriving from their archaeal ancestors. In contrast, bacteria lack histones as a rule. However, in recent years histone proteins have been identified in a few bacterial clades, in particular the phylum Bdellovibrionota, and these histones have been proposed to exhibit a range of divergent features compared to histones in archaea and eukaryotes. However, no experimental functional genomic studies of the properties of Bdellovibrionota chromatin have been carried out. In this work, we map the landscape of chromatin accessibility, active transcription and three-dimensional genome organization in a member of Bdellovibrionota (a Bacteriovorax strain). We find that Bacteriovorax chromatin is characterized by preferential accessibility around promoter regions, similar to what is observed in eukaryotes with compact genomes such as yeast, and also to some archaea. As in eukaryotes, chromatin accessibility positively correlates with gene expression. Mapping active transcription through single-strand DNA (ssDNA) profiling revealed that Bacteriovorax promoters exhibit very strong polymerase pausing, unlike in yeast, but similar to the state of mammalian and fly promoters. Finally, the Bacteriovorax genome exists in a three-dimensional (3D) conformation analogous to that of other bacteria without histones, organized by the parABS system and along the axis defined by replication origin and termination regions. These results provide a foundation for understanding the chromatin biology of the unique Bdellovibrionota bacteria and the deep evolution of chromatin organization across the tree of life. Overall design: ATAC-seq, KAS-seq and Hi-C in Bacterioforax sp. ICPB 3264