Archaeal histone-based chromatin forms extended polymeric structures in vivo

Archaeal histone-based chromatin complexes are the evolutionary precursor of the eukaryotic nucleosomal landscape. Histones are encoded by most Archaea and are present in sufficient quantities in many heat-loving species to plausibly completely wrap and condense the genome(s). Establishing whether the in vivo archaeal histone-based chromatin structure(s) align to the repeating extended polymeric structures revealed with purified components in vitro remains an important goal to link the biological roles of archaeal and eukaryotic histone-based chromatin structures. Deploying advanced imaging and cryo-electron tomography techniques with the hyperthermophilic, histone-encoding archaeon Thermococcus kodakarensis, we reveal that the in vivo histone-based chromatin architecture changes dramatically during the growth cycle. While the cytoplasm contains a relatively uniform nucleoid in exponential growth, tightly packed, helical filaments that conform to archaeal histone-based chromatin observed in vitro emerge during the transition to stationary phase. The in vitro extended chromatin conformation of histone-based genome architecture observed in vivo establishes that archaeal information processing machinery can function on tightly packed and regularly organized histone-based chromatin structures. We also observe large, nucleic-acid rich, globular condensates directly alongside the helical filamentous chromatin conformation that may represent an additional conformation of archaeal chromatin. Our results suggest that alternative forms of archaeal chromatin may be achieved without obvious chromatin remodeling complexes or biologically significant levels of post-translational modifications to histone proteins, providing a plausible evolutionary driver for the emergence of more complex mechanisms that protect and regulate expression of eukaryotic genomes.