Chromatinization of Escherichia coli with archaeal histones

  1. Maria Rojec
  2. Antoine Hocher
  3. Kathryn M Stevens
  4. Matthias Merkenschlager
  5. Tobias Warnecke  Is a corresponding author
  1. 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.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. 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.
  2. 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.
  3. 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.
  4. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2889-3288
  5. 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.
    ORCID icon "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.

Reviewing Editor

  1. David M Truong, NYU Langone Health, United States

Publication history

  1. Received: June 4, 2019
  2. Accepted: November 5, 2019
  3. Accepted Manuscript published: November 6, 2019 (version 1)
  4. 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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  1. Maria Rojec
  2. Antoine Hocher
  3. Kathryn M Stevens
  4. Matthias Merkenschlager
  5. Tobias Warnecke
(2019)
Chromatinization of Escherichia coli with archaeal histones
eLife 8:e49038.
https://doi.org/10.7554/eLife.49038
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