Ribosome surface properties may impose limits on the nature of the cytoplasmic proteome

  1. Paul E Schavemaker
  2. Wojciech M Śmigiel
  3. Bert Poolman  Is a corresponding author
  1. University of Groningen, Netherlands

Abstract

Much of the molecular motion in the cytoplasm is diffusive, which possibly limits the tempo of processes. We studied the dependence of protein mobility on protein surface properties and ionic strength. We used surface-modified fluorescent proteins (FPs) and determined their translational diffusion coefficients (D) in the cytoplasm of Escherichia coli, Lactococcus lactis and Haloferax volcanii. We find that in E. coli D depends on the net charge and its distribution over the protein, with positive proteins diffusing up to 100-fold slower than negative ones. This effect is weaker in L. lactis and Hfx. volcanii due to electrostatic screening. The decrease in mobility is probably caused by interaction of positive FPs with ribosomes as shown in in vivo diffusion measurements and confirmed in vitro with purified ribosomes. Ribosome surface properties may thus limit the composition of the cytoplasmic proteome. This finding lays bare a paradox in the functioning of prokaryotic (endo)symbionts.

Data availability

The following previously published data sets were used

Article and author information

Author details

  1. Paul E Schavemaker

    Department of Biochemistry, University of Groningen, Groningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  2. Wojciech M Śmigiel

    Department of Biochemistry, University of Groningen, Groningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Bert Poolman

    Department of Biochemistry, University of Groningen, Groningen, Netherlands
    For correspondence
    b.poolman@rug.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1455-531X

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (TOP-PUNT.13.006)

  • Bert Poolman

H2020 European Research Council (Advanced Grant (ABC Volume))

  • Wojciech M Śmigiel

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

Reviewing Editor

  1. Victor Sourjik, Max Planck Institute for Terrestrial Microbiology, Germany

Publication history

  1. Received: June 30, 2017
  2. Accepted: November 14, 2017
  3. Accepted Manuscript published: November 20, 2017 (version 1)
  4. Version of Record published: December 12, 2017 (version 2)

Copyright

© 2017, Schavemaker 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. Paul E Schavemaker
  2. Wojciech M Śmigiel
  3. Bert Poolman
(2017)
Ribosome surface properties may impose limits on the nature of the cytoplasmic proteome
eLife 6:e30084.
https://doi.org/10.7554/eLife.30084

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