Histone-organized chromatin in bacteria

Abstract

Histones are the principal constituents of chromatin in eukaryotes and most archaea, while bacteria generally rely on an orthogonal set of proteins to organize their chromosomes. However, several bacterial genomes encode proteins with putative histone fold domains. Whether these proteins are structurally and functionally equivalent to archaeal and eukaryotic histones is unknown. Here, we demonstrate that histones are essential and are major components of chromatin in the bacteriaBdellovibrio bacteriovorusandLeptospira interrogans. Patterns of sequence evolution suggest important roles in several additional bacterial clades. Structural analysis of theB. bacteriovorushistone (Bd0055) dimer shows that histone fold topology is conserved between bacteria, archaea, and eukaryotes. Yet, unexpectedly, Bd0055 binds DNA end-on and forms a sheath of tightly packed histone dimers to encase straight DNA. This binding mode is in stark contrast to that employed by archaeal, eukaryotic, and viral histones, which invariably bend and wrap DNA around their outer surface. Our results demonstrate that histones are integral chromatin components across the tree of life and highlight organizational innovation in the domain Bacteria.

Bacterial histone HBb fromBdellovibrio bacteriovoruscompacts DNA by bending

“…Moreover, our findings also show that HBb is essential for maintaining bacterial viability. These results are consistent with a recent preprint published on bioRxiv, which reports the structure of the HBb-DNA complex and proposes a role for HBb in genome organization (Hocher et al, 2023).…”

“…To understand the functional significance of HBb, we attempted to construct a strain in which the hbb gene (BD_RS00255) was replaced by a kanamycin resistance cassette. However, we were unable to select for the loss of the gene, suggesting that HBb is essential for B. bacteriovorus during the growth phase, as also shown in a recent study (Hocher et al, 2023). These results provide compelling evidence for the critical role of HBb in the growth and survival of B. bacteriovorus.…”

“…However, unlike archaeal and eukaryotic histones, recent research has shown that HBb does not form nucleosome-like structures, but that HBb dimers form a sheath around straight DNA (Hocher et al, 2023). Futhermore, we found that HBb is indispensable for the survival of B. bacteriovorus, suggesting that bacterial histones, much like their counterparts in archaea and eukaryotes, are likely involved in critical cellular functions.…”

“…3c). This value is considerably lower than the nanomolar DNA-binding affinities determined for other histone homologs (Bailey et al, 2002, indicating that HBb likely binds to DNA non-specifically via a different type of interaction, as was shown recently (Hocher et al, 2023).…”

“…This suggests that HBb likely binds DNA, but possibly in a different manner than HMfB. Indeed, an HBb-DNA complex reported in a recent preprint suggests that HBb binds DNA differently than archaeal and eukaryotic histones (Hocher et al, 2023).…”