Solution Dynamics in Histone-Based Archaeal Chromatin

Abstract

Over the last two decades, histone-fold containing proteins have been identified in most known Archaea, and their similarities in sequence and structure strongly suggest that they share a common evolutionary ancestor to the eukaryotic histones that form the nucleosome core particle. Recently, crystal structures of archaeal histones in complex with DNA have shown that they are capable of forming oligomers that bind DNA in superhelical turns that are identical to the nucleosome; however, archaeal chromatin can stack as an extended superhelix, in contrast to the defined particulate character of nucleosomes. Here, we have conducted molecular dynamics simulations on archaeal histone chromatin oligomers of varying sizes, and we compare these systems with one another and with nucleosomes in order to elucidate the structure-dynamics-function relationship of this superhelical stacking. Our models provide further proof that the interaction between L1 loops in neighboring archaeal histone dimers is paramount to chromatin stack formation, as its absence results in a highly dynamic complex. Furthermore, we find that eukaryotic histones are tighter binders of DNA, even when reduced to the hexasome complex and in the absence of the highly-charged histone tails. Together, these data provide further insight into the structural origin of chromatin, and display an energetic rationale for the evolution of the nucleosome complex.