The DNA-binding protein HTa from Thermoplasma acidophilum is an archaeal histone analog

  1. Antoine Hocher  Is a corresponding author
  2. Maria Rojec
  3. Jacob B Swadling
  4. Alexander Esin
  5. Tobias Warnecke  Is a corresponding author
  1. MRC London Institute of Medical Sciences (LMS), United Kingdom

Abstract

Histones are a principal constituent of chromatin in eukaryotes and fundamental to our understanding of eukaryotic gene regulation. In archaea, histones are widespread but not universal: several lineages have lost histone genes. What prompted or facilitated these losses and how archaea without histones organize their chromatin remains largely unknown. Here, we elucidate primary chromatin architecture in an archaeon without histones, Thermoplasma acidophilum, which harbours a HU family protein (HTa) that protects part of the genome from micrococcal nuclease digestion. Charting HTa-based chromatin architecture in vitro, in vivo and in an HTa-expressing E. coli strain, we present evidence that HTa is an archaeal histone analog. HTa preferentially binds to GC-rich sequences, exhibits invariant positioning throughout the growth cycle, and shows archaeal histone-like oligomerization behaviour. Our results suggest that HTa, a DNA-binding protein of bacterial origin, has converged onto an architectural role filled by histones in other archaea.

Data availability

All sequencing data generated for this study have been deposited in GEO under accession code GSE127728.

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

Article and author information

Author details

  1. Antoine Hocher

    MRC London Institute of Medical Sciences (LMS), London, United Kingdom
    For correspondence
    a.hocher@lms.mrc.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  2. Maria Rojec

    MRC London Institute of Medical Sciences (LMS), London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Jacob B Swadling

    MRC London Institute of Medical Sciences (LMS), London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexander Esin

    MRC London Institute of Medical Sciences (LMS), London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Tobias Warnecke

    MRC 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

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Joseph Thomas Wade, Wadsworth Center, New York State Department of Health, United States

Version history

  1. Received: October 7, 2019
  2. Accepted: November 10, 2019
  3. Accepted Manuscript published: November 11, 2019 (version 1)
  4. Version of Record published: November 25, 2019 (version 2)

Copyright

© 2019, Hocher 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. Antoine Hocher
  2. Maria Rojec
  3. Jacob B Swadling
  4. Alexander Esin
  5. Tobias Warnecke
(2019)
The DNA-binding protein HTa from Thermoplasma acidophilum is an archaeal histone analog
eLife 8:e52542.
https://doi.org/10.7554/eLife.52542

Share this article

https://doi.org/10.7554/eLife.52542

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