Chromatinization of Escherichia coli with archaeal histones

Abstract
Data availability
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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.

The following data sets were generated

(2019) The role of archaeal histones in gene expression - a synthetic biology perspective
NCBI Gene Expression Omnibus, GSE127680.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE127680

The following previously published data sets were used

(2017) RNA-seq on rRNA depleted libraries from exponentially growing Halobacterium salinarum NRC-1 strains Δura3 and Δhlx2
NCBI Gene Expression Omnibus, GSE99730.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE99730
(2015) Transcriptomic profiles of M. barkeri Fusaro DSMZ804 and Pyr+ strains
NCBI Gene Expression Omnibus, GSE70370.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE70370
1. Cho S
2. Kim M
3. Jeong Y
4. Lee B
5. Lee J
6. Kang SG
7. Cho B
(2017) Genome-wide primary transcriptome landscape reveals the diversity of regulatory elements in archaeal genomes
NCBI Gene Expression Omnibus, GSE85760.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE85760
(2015) High-throughput RNA sequencing of methanosarcina grown on methylated sulfur compounds
NCBI Gene Expression Omnibus, GSE64349.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE64349
1. Hansen E
2. Rey F
(2011) The pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii
NCBI Gene Expression Omnibus, GSE25408.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE25408

Article and author information

Author details

Maria Rojec

Institute of Clinical Sciences, London Institute of Medical Sciences (LMS), London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Antoine Hocher

Institute of Clinical Sciences, London Institute of Medical Sciences (LMS), London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Kathryn M Stevens

Institute of Clinical Sciences, London Institute of Medical Sciences (LMS), London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Matthias Merkenschlager

Institute of Clinical Sciences, London Institute of Medical Sciences (LMS), London, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2889-3288
Tobias Warnecke

Institute of Clinical Sciences, London Institute of Medical Sciences (LMS), London, United Kingdom

For correspondence
tobias.warnecke@imperial.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4936-5428

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.

Copyright

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.