Ranawat, H. M.; Cajili, M. K. M.; Lopez-Barbosa, N.; Quail, T.; Dame, R. T.; Dodonova, S. O.

Asgards are the closest archaeal relatives of eukaryotes, representing an important step in chromatin evolution. However, their chromatin organization has remained enigmatic until now. In this study, we present the first structures of Asgard chromatin assemblies formed by the Hodarchaeal histone HHoB. Our high-resolution cryo-EM structures reveal that this Asgard histone assembles into compact \"closed\" and into extended \"open\" hypernucleosomes. Thus the closed hypernucleosome conformation is conserved across archaeal lineages, while the open conformation resembles a eukaryotic H3-H4 octasome and likely represents an Asgard-specific innovation. Moreover, we show that Mg2+ ions influence Asgard chromatin conformation, suggesting a regulatory role. Overall, our study provides the first structure-based model of Asgard chromatin organization, expanding our understanding of chromatin architecture in evolutionary context.