Chromatin-Mediated Epigenetics in the Archaeon Sulfolobus solfataricus

Epigenetic mechanisms are essential for complex eukaryotic life, allowing for cellular differentiation and multicellularity. However, their potential evolutionary origins have remained unexplored. Archaea use proteins with phylogenetic homology to eukaryotes for molecular processes such as DNA replication, repair, transcription and protein translation. Archaea DNA methylation systems are bacterial-like and not known to have epigenetic properties. However, the phylum crenarchaeota compact their genomic material using small chromatin proteins that are post translationally modified at lysine residues, like eukaryotic histones. To investigate whether archaea engage in epigenetics and the mechanisms this may involve, this project examined strains of the crenarchaeon Sulfolobus solfataricus that displayed epigenetic traits. These strains were generated using adaptive laboratory evolution for increased acid resistance and called Super Acid Resistant Crenarchaeota (SARC). Genetic and transcriptomic data demonstrated that the SARC strains possessed novel, heritable traits and expression patterns in the absence of genetic changes. Recombination-induced chromatin exchanged demonstrated that these traits could be manipulated by replacing native chromatin regions with naïve but genetically identical DNA sequences. Certain chromatin proteins, Cren7 and Sso7D, were found to be heritably hypomethylated in the SARC strains. ChIP-seq found that genome binding patterns of Cren7 and Sso7D varied little between strains, while protein-protein interaction studies found that many proteins interacted differently with Cren7 and Sso7D between the parental and SARC strains cultured under identical conditions. Recombination experiments to replace native chromatin with DNA mixed with Cren7 or Sso7D isolated from parental and SARC strains found that gene expression was modulated by these proteins in a manner dependent on the chromatin donor strain. This work presents new data demonstrating that archaea also share epigenetic processes likely modulated by chromatin protein modification state. The feature conservation between eukaryotes and archaea, coupled with taxonomic analyses support a two-domain tree model in which eukaryotes arose from archaea. Such similarities suggest a powerful opportunity to study these systems in archaea to yield outcomes relevant to eukaryotic and evolutionary science