Viral challenge as a potential driver of histone loss in dinoflagellates

Within canonical eukaryotic nuclei, DNA is bound to highly conserved histone protein octamers, together termed nucleosomes, which facilitate DNA condensation and contribute to genomic regulation. The dinoflagellates, a group of unicellular algae, are a striking exception to this otherwise universal feature and have abandoned histones as their primary DNA packaging proteins. Phylogenetic analyses suggest that histone loss coincides with genome enlargement and the emergence of liquid crystalline chromosomes, the predominant constituent of which appears to be apparently viral-derived proteins termed dinoflagellate-viral-nucleoproteins (DVNPs) . However, the evolutionary mechanisms that drove dinoflagellate chromatin divergence, especially histone depletion, remain unknown. Here, using Saccharomyces cerevisiae as a heterologous model, we show that DVNP antagonizes eukaryotic chromatin and has a toxicity that can be attenuated through histone depletion. Using a combination of ChIP-seq and MNase-seq we demonstrate that DVNP localizes specifically to histone binding sites, displaces histones, and coincides with global transcriptional disruption. Sonication based DVNP ChIP seq in wildtype yeast expressing DVNP-3HA-NLS in triplicate (both ChIPs and inputs). Sonication based Rpb3 (RNAP II) ChIP-seq and Mnase-seq in control and DVNP-3HA-NLS expressing cells done in duplicate.