Nucleosomes restrict DNA accessibility throughout eukaryotic genomes, with
repercussions for replication, transcription, and other DNA-templated processes. How this globally
restrictive organization emerged during evolution remains poorly understood. Here, to better
understand the challenges associated with establishing globally restrictive chromatin, we express
histones in a naive system that has not evolved to deal with nucleosomal structures: Escherichia
coli. We find that histone proteins from the archaeon Methanothermus fervidus assemble on the E.
coli chromosome in vivo and protect DNA from micrococcal nuclease digestion, allowing us to map
binding footprints genome-wide. We show that higher nucleosome occupancy at promoters is
associated with lower transcript levels, consistent with local repressive effects. Surprisingly,
however, this sudden enforced chromatinization has only mild repercussions for growth unless cells
experience topological stress. Our results suggest that histones can become established as
ubiquitous chromatin proteins without interfering critically with key DNA-templated processes.