The origin of chromosomal histones in a 30S ribosomal protein

Gene. 2020 Feb 5:726:144155. doi: 10.1016/j.gene.2019.144155. Epub 2019 Oct 17.

Abstract

Histones are genes that regulate chromatin structure. They are present in both eukaryotes and archaea, and form nucleosomes with DNA, but their exact evolutionary origins have hitherto remained a mystery. A longstanding hypothesis is that they have precursors in ribosomal proteins with whom they share much in common in terms of size and chemistry. By examining the proteome of the Asgard archaeon, Lokiarchaeum, the most conserved of all the histones, H4, is found to plausibly be homologous with one of its 30S ribosomal proteins, RPS6. This is based on both sequence identity and statistical analysis. The N-terminal tail, containing key sites involved in post-translational modifications, is notably present in the precursor gene. Although other archaeal groups possess similar homologs, these are not as close to H4 as the one found in Lokiarchaeum. The other core histones, H2A, H2B and H3, appear to have also evolved from the same ribosomal protein. Parts of H4 are also similar to another ribosomal protein, namely RPS15, suggesting that the ancestral precursor could have resembled both. Eukaryotic histones, in addition, appear to have an independent origin to that of their archaeal counterparts that evolved from similar, but still different, 30S subunit proteins, some of which are much more like histones in terms of their physical structure. The nucleosome may, therefore, be not only of archaeal but also of ribosomal origin.

Keywords: Gene duplication; Histones; Lokiarchaea; Pre-adaptation; Ribosomal proteins.

MeSH terms

  • Archaea / genetics
  • Chromatin / genetics*
  • DNA / genetics
  • Eukaryota / genetics
  • Evolution, Molecular
  • Histones / genetics*
  • Nucleosomes / genetics
  • Protein Processing, Post-Translational / genetics
  • Ribosomal Proteins / genetics*

Substances

  • Chromatin
  • Histones
  • Nucleosomes
  • Ribosomal Proteins
  • ribosomal protein S30
  • DNA