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.
Highlights
Archaeal nucleosome core particles protect ∼ 60 bp of DNA, approximately half that of eukaryotic nucleosomes, as demonstrated by the landmark work of Pereira et al (1997)
We further show that the nucleosomal protected fragments and nucleosomedepleted region (NDR) are shorter in archaea than in eukaryotes
Archaeal histone tetramers likely resemble an ancestral state of chromatin, as it has been observed that functional (H3-H4)2 tetramers can be formed in vitro from eukaryotic histones, and these tetramers are functional; they facilitate more rapid transcription in vitro compared to native histone octamers (Puerta et al, 1993)
Summary
Archaeal nucleosome core particles protect ∼ 60 bp of DNA, approximately half that of eukaryotic nucleosomes, as demonstrated by the landmark work of Pereira et al (1997) Comparing both eukaryotic and archaeal nucleosomes, the former is an octamer composed of heterodimers of histones H2A, H2B, H3 and H4 whereas the latter histones assemble from homologs of H3 and H4 proteins (Pereira and Reeve, 1998; Talbert and Henikoff, 2010). The genome of Hfx. volcanii has an average GC content of 65% and a total genome length of 4 Mb (Hartman et al, 2010) composed of five circular genetic elements: a 2.8 Mb main chromosome, three smaller chromosomes pHV1, pHV3 and pHV4 and the plasmid pHV2 It is highly polyploid with ∼15 genome copies during exponential growth and ∼10 during stationary phase (Breuert et al, 2006). The histone protein of Hfx. volcanii, hstA (HVO_0520), has a domain architecture containing two distinct histone fold domains within the same peptide that heterodimerize similar to the Methanopyrus kandleri histone (HMk) (Geer et al, 2002; Talbert and Henikoff, 2010; Marchler-Bauer et al, 2011)
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