Chromatinization of Escherichia coli with archaeal histones
- London Institute of Medical Sciences (LMS), United Kingdom
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 naïve 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.
Data availability
Sequencing data have been deposited in GEO under accession code GSE127680.
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The role of archaeal histones in gene expression - a synthetic biology perspectiveNCBI Gene Expression Omnibus, GSE127680.
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Transcriptomic profiles of M. barkeri Fusaro DSMZ804 and Pyr+ strainsNCBI Gene Expression Omnibus, GSE70370.
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High-throughput RNA sequencing of methanosarcina grown on methylated sulfur compoundsNCBI Gene Expression Omnibus, GSE64349.
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The pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithiiNCBI Gene Expression Omnibus, GSE25408.
Article and author information
Author details
Matthias Merkenschlager
Funding
Medical Research Council (MC_A658_5TY40)
- Tobias Warnecke
Engineering and Physical Sciences Research Council (EP/R029407/1)
- Tobias Warnecke
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- David M Truong, NYU Langone Health, United States
Version history
- Received: June 4, 2019
- Accepted: November 5, 2019
- Accepted Manuscript published: November 6, 2019 (version 1)
- Version of Record published: November 20, 2019 (version 2)
Copyright
© 2019, Rojec et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Chromatinization of Escherichia coli with archaeal histones
eLife 8:e49038.
https://doi.org/10.7554/eLife.49038
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