Histone-DNA Interactions in the Archaeon Methanocaldococcus Jannaschii

Abstract

The requirement for DNA compaction is universal across all domains of life. Although the histone proteins of Archaea and Eukaryotes have low sequence homology, the core histone fold is well-conserved and structures are virtually identical. However, small structural differences mean that Archaeal nucleosomes might assemble into a continuous solenoid-like fiber: the ‘hypernucleosome’. Given that M. jannaschii thrives at 80oC and its genomic DNA is positively supercoiled (the opposite to mesophiles like us), the mechanism of DNA packaging may show interesting adaptations and diversity that will inform us about the biophysics of chromatin in general. Here, we have used magnetic tweezers to control the supercoiling of DNA while quantifying the kinetics and energetics of DNA-histone binding, wrapping and compaction. Using this technique, we have investigated the properties of M. jannaschii chromatin with its most abundant histone protein “A3”. We propose a model for the force-extension properties of Archaeal chromatin, analogous to that for Eukaryotic chromatin, and demonstrate that the force-extension properties are dependent upon protein concentration. We find that, under moderate load, histone binding confers stability to DNA by preventing base-pair unstacking when negative supercoiling is applied, and the chromatin fiber shows a sharp buckling transition between both positive and negative supercoiling regimes. At high load (>5pN), the chromatin fiber is disrupted and the force-extension diagram returns to the worm-like chain, typical of naked DNA. Our model suggests a mechanism by which DNA processing enzymes may shunt or displace nucleosomes, obviating the need for active chromatin remodeling enzymes.