The packaging of DNA in chromatin is an important determinant of transcription, replication and recombination. Prokaryotic DNA is thought to be permissive and accessible to the transacriptional machinery. In contrast, eukaryotic chromatin is thought to be repressive for transcription (Struhl, 1999). To ask whether histones are sufficient for the transition from a permissive (open) to a repressive (closed) transcriptional state, we introduced histones HMfA and HMfB from the methanogenic archaeon Methanothermus fervidus into a bacterial host, Escherichia coli. We found that archaeal histones form dynamic nucleosomal arrays composed of oligomerising histone dimers in the E. coli genome, just as they do in Archaea. The positioning of archeal histones is determined by the underlying E. coli DNA sequence, as well as bacterial transcription and replication during active growth. Archaeal histones are surprisingly well tolerated in rich medium and under a variety of stresses, with the exception of treatments that directly affect cellular DNA topology or cause DNA damage. Even though E. coli lacks chromatin remodeling enzymes to actively reshape the chromatin landscape, archaeal histones have at best weak repressive local effects on transcription. These findings suggest that archaeal histones, similar to bacterial chromatin components, are not as restrictive as their eukaryotic counterparts, and may define a “proto-restrictive” ground state.