Ion counting demonstrates a high electrostatic field generated by the nucleosome

  1. Magdalena Gebala  Is a corresponding author
  2. Stephanie L Johnson
  3. Geeta J Narlikar
  4. Daniel Herschlag  Is a corresponding author
  1. Stanford University, United States
  2. University of California, San Francisco, United States

Abstract

The first step towards the eukaryotic nuclear DNA compaction process is the formation of a nucleosome, which comprises of the negatively charged DNA wrapped around a positively charged histone protein octamer. Often, it is assumed that the complexation of the DNA into the nucleosome completely attenuates the DNA charge and hence the electrostatic field generated by the molecule. In contrast, theoretical and computational studies suggest that the nucleosome retains a strong, negative electrostatic field. Despite their fundamental implications for chromatin organization and function, these opposing views of nucleosome electrostatics have not been experimentally tested. Herein, we directly measure nucleosome electrostatics and find that while nucleosome formation reduces the complex charge by half, the nucleosome nevertheless maintains a strong negative electrostatic field. Our studies highlight the importance of considering the polyelectrolyte nature of the nucleosome and its impact on processes ranging from factor binding to DNA compaction.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data and source code files have been provided for Figures 3 and 4.

Article and author information

Author details

  1. Magdalena Gebala

    Department of Biochemistry, Stanford University, Stanford, United States
    For correspondence
    mgebala@stanford.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1086-5548
  2. Stephanie L Johnson

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    Competing interests
    No competing interests declared.
  3. Geeta J Narlikar

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    Competing interests
    Geeta J Narlikar, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1920-0147
  4. Daniel Herschlag

    Department of Biochemistry, Stanford University, Stanford, United States
    For correspondence
    herschla@stanford.edu
    Competing interests
    No competing interests declared.

Funding

National Institutes of Health (P01GM066275)

  • Daniel Herschlag

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

Version history

  1. Received: January 9, 2019
  2. Accepted: June 8, 2019
  3. Accepted Manuscript published: June 11, 2019 (version 1)
  4. Version of Record published: June 19, 2019 (version 2)

Copyright

© 2019, Gebala 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. Magdalena Gebala
  2. Stephanie L Johnson
  3. Geeta J Narlikar
  4. Daniel Herschlag
(2019)
Ion counting demonstrates a high electrostatic field generated by the nucleosome
eLife 8:e44993.
https://doi.org/10.7554/eLife.44993

Share this article

https://doi.org/10.7554/eLife.44993

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