Abstract
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.
Highlights
All cellular systems face the dual challenge of protecting and compacting their resident genomes while making the underlying genetic information dynamically accessible
We find that HMfA and HMfB, heterologously expressed in E. coli, bind to the E. coli genome and protect it from micrococcal nuclease (MNase) digestion, allowing us to map nucleosomes in E. coli in vivo
Given that a tetramer wraps ~60bp of DNA, this implies a supply of histones that is, in principle, sufficient to cover most of the E. coli genome
Summary
All cellular systems face the dual challenge of protecting and compacting their resident genomes while making the underlying genetic information dynamically accessible. Archaeal and eukaryotic nucleosomes preferentially assemble on DNA that is more bendable, a property associated, on average, with elevated GC content and the presence of certain periodically spaced dinucleotides, notably including AA/TT (Ammar et al, 2011; Nalabothula et al, 2013; Pereira & Reeve, 1999; Bailey et al, 2000; 2002; Ioshikhes et al, 2011) They exhibit similar positioning around transcriptional start sites (Ammar et al, 2011; Nalabothula et al, 2013), which are typically depleted of nucleosomes and remain accessible to the core transcription machinery. Whether archaeal histones play a global restrictive role akin to their eukaryotic counterparts, remains poorly understood, as does their involvement in transcription regulation more generally (Gehring et al, 2016)
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