Archaeal chromatin 'slinkies' are inherently dynamic complexes with deflected DNA wrapping pathways

  1. Samuel Bowerman
  2. Jeff Wereszczynski
  3. Karolin Luger  Is a corresponding author
  1. HHMI and University of Colorado, Boulder, United States
  2. Illinois Institute of Technology, United States

Abstract

Eukaryotes and many archaea package their DNA with histones. While the four eukaryotic histones wrap ~147 DNA base pairs into nucleosomes, archaeal histones form 'nucleosome-like' complexes that continuously wind between 60 - 500 base pairs of DNA ('archaeasomes'), suggested by crystal contacts and analysis of cellular chromatin. Solution structures of large archaeasomes (>90 DNA base pairs) have never been directly observed. Here, we utilize molecular dynamics simulations, analytical ultracentrifugation, and cryoEM to structurally characterize the solution state of archaeasomes on longer DNA. Simulations reveal dynamics of increased accessibility without disruption of DNA-binding or tetramerization interfaces. Mg2+ concentration influences compaction, and cryoEM densities illustrate that DNA is wrapped in consecutive substates arranged 90o out-of-plane with one another. Without ATP-dependent remodelers, archaea may leverage these inherent dynamics to balance chromatin packing and accessibility.

Data availability

cryoEM datasets have been uploaded to EMPIAR (EMD-23403, EMD-23404). The pdb files are submitted as supplementary information. MD trajectories will be stored on CU storage resources (PetaLibrary) and made available upon request through file transfer or shipping of external hard drives.

Article and author information

Author details

  1. Samuel Bowerman

    Department of Chemistry and Biochemistry, HHMI and University of Colorado, Boulder, Boulder, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jeff Wereszczynski

    Department of Physics, Illinois Institute of Technology, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Karolin Luger

    Department of Chemistry and Biochemistry, HHMI and University of Colorado, Boulder, Boulder, United States
    For correspondence
    karolin.luger@colorado.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5136-5331

Funding

National Science Foundation (1552743)

  • Jeff Wereszczynski

National Institute of General Medical Sciences (R35GM119647)

  • Jeff Wereszczynski

Howard Hughes Medical Institute (NA)

  • Karolin Luger

National Institute of General Medical Sciences (F32GM137496)

  • Samuel Bowerman

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

Reviewing Editor

  1. Sebastian Deindl, Uppsala University, Sweden

Publication history

  1. Received: December 9, 2020
  2. Accepted: February 16, 2021
  3. Accepted Manuscript published: March 2, 2021 (version 1)
  4. Version of Record published: March 24, 2021 (version 2)

Copyright

© 2021, Bowerman 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. Samuel Bowerman
  2. Jeff Wereszczynski
  3. Karolin Luger
(2021)
Archaeal chromatin 'slinkies' are inherently dynamic complexes with deflected DNA wrapping pathways
eLife 10:e65587.
https://doi.org/10.7554/eLife.65587

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