Chromatin is an ancient innovation conserved between Archaea and Eukarya

Abstract

The eukaryotic nucleosome is the fundamental unit of chromatin, comprising a protein octamer that wraps ∼147 bp of DNA and has essential roles in DNA compaction, replication and gene expression. Nucleosomes and chromatin have historically been considered to be unique to eukaryotes, yet studies of select archaea have identified homologs of histone proteins that assemble into tetrameric nucleosomes. Here we report the first archaeal genome-wide nucleosome occupancy map, as observed in the halophile Haloferax volcanii. Nucleosome occupancy was compared with gene expression by compiling a comprehensive transcriptome of Hfx. volcanii. We found that archaeal transcripts possess hallmarks of eukaryotic chromatin structure: nucleosome-depleted regions at transcriptional start sites and conserved −1 and +1 promoter nucleosomes. Our observations demonstrate that histones and chromatin architecture evolved before the divergence of Archaea and Eukarya, suggesting that the fundamental role of chromatin in the regulation of gene expression is ancient.DOI: http://dx.doi.org/10.7554/eLife.00078.001

Clipping of arginine-methylated histone tails by JMJD5 and JMJD7

“…Interestingly, it was well known that Archaea contain histone-like proteins and form nucleosomelike structures but without tails or chromatin remodeling complex (56)(57)(58). It seems that RNA polymerases alone in Archaea could overcome tailless nucleosomes during transcription since there is no known chromatin remodeling complex in Archaea (58).…”

Transcription Regulation in Archaea

“…The topology of naked DNA templates does influence the positions and efficiencies of intrinsic terminators, suggesting that chromatin templates may also influence termination patterns. Nucleosomes are depleted not only from promoter regions but also from predicted termination regions, suggesting a potential regulatory role for chromatin architecture on termination of transcription (164).…”

“…The best-described complexes are homo-or hetero-histone tetramers, homologous to the H3/H4 tetramer in eukaryotes, that associate with ϳ60 bp of double-stranded DNA. Archaeal histones share similar biases with eukaryotic nucleosomes for flexible DNA sequences and are, in general, absent from the core promoters of archaeal genes (164,165). Archaeal histone proteins share the same core fold as eukaryotic histones but lack the extensions from this fold (i.e., tails) that are highly modified and essential for proper nucleosome dynamics in eukaryotes (166).…”

“…Chromatin architecture at a promoter could influence or prevent transcription initiation by occluding transcription factor binding or inhibiting DNA melting (164,167,168,177). Crenarchaeonencoded nucleoid-associated proteins have been shown to influence transcription output through the acetylation/deaceytlation of Alba in vitro (76), although Alba has not yet been shown to influence transcription in vivo.…”

“…These studies contrast the view of histone proteins as general organizational factors with the global influence on gene expression and minimally suggest that the archaeal chromatin of some species is dependent on the activities of many nucleoid-associated proteins. When histone-encoding genes have been deleted, or have been attempted to be deleted from other species, more global disruption of gene expression has been noted (161,164,165,167,(171)(172)(173)(174)(175)(176). Some species are reliant on at least one histone protein, and it is unclear at this point whether the noted global changes in gene expression seen in deletion strains stem from reorganization or disorganization of the archaeal genomes or the primary, secondary, and tertiary effects of localized disruptions that lead to additional differences in regulation at remote sites.…”