1. Microbiology and Infectious Disease
  2. Structural Biology and Molecular Biophysics
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Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism

  1. Robert J Nichols
  2. Benjamin LaFrance
  3. Naiya R Phillips
  4. Devon R Radford
  5. Luke M Oltrogge
  6. Luis E Valentin-Alvarado
  7. Amanda J Bischoff
  8. Eva Nogales  Is a corresponding author
  9. David F Savage  Is a corresponding author
  1. University of California, Berkeley, United States
  2. University of Toronto, Canada
  3. Lawrence Berkeley National Laboratory, United States
Research Article
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Cite this article as: eLife 2021;10:e59288 doi: 10.7554/eLife.59288

Abstract

Prokaryotic nanocompartments, also known as encapsulins, are a recently discovered proteinaceous organelle-like compartments in prokaryotes that compartmentalize cargo enzymes. While initial studies have begun to elucidate the structure and physiological roles of encapsulins, bioinformatic evidence suggests that a great diversity of encapsulin nanocompartments remains unexplored. Here, we describe a novel encapsulin in the freshwater cyanobacterium Synechococcus elongatus PCC 7942. This nanocompartment is upregulated upon sulfate starvation and encapsulates a cysteine desulfurase enzyme via an N-terminal targeting sequence. Using cryo-electron microscopy, we have determined the structure of the nanocompartment complex to 2.2 Å resolution. Lastly, biochemical characterization of the complex demonstrated that the activity of the cysteine desulfurase is enhanced upon encapsulation. Taken together, our discovery, structural analysis, and enzymatic characterization of this prokaryotic nanocompartment provide a foundation for future studies seeking to understand the physiological role of this encapsulin in various bacteria.

Data availability

Cryo-EM maps of holo and apo-SrpI have been deposited at the EM Data Resource with accession codes EMD-22094 and EMD-22095 respectively. The refined coordinate model has been deposited at the Protein Data Bank (PDB) with accession code 6X8M and 6X8T.

The following data sets were generated

Article and author information

Author details

  1. Robert J Nichols

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Benjamin LaFrance

    Department of Molecular and Cell Biology,, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Naiya R Phillips

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Devon R Radford

    Department of Molecular Genetics, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Luke M Oltrogge

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5716-9980
  6. Luis E Valentin-Alvarado

    Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Amanda J Bischoff

    Department of Chemistry,, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Eva Nogales

    Molecular Biophysics and Integrative Bio-Imaging Division, Lawrence Berkeley National Laboratory, Berkeley, United States
    For correspondence
    enogales@lbl.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9816-3681
  9. David F Savage

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    savage@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0042-2257

Funding

U.S. Department of Energy (Grant DE-SC00016240 (to D.F.S))

  • Robert J Nichols
  • Naiya R Phillips
  • Luke M Oltrogge
  • David F Savage

National Science Foundation (GRFP-1106400)

  • Benjamin LaFrance

Howard Hughes Medical Institute

  • Eva Nogales

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

Reviewing Editor

  1. Sriram Subramaniam, University of British Columbia, Canada

Publication history

  1. Received: May 25, 2020
  2. Accepted: April 4, 2021
  3. Accepted Manuscript published: April 6, 2021 (version 1)
  4. Version of Record published: April 15, 2021 (version 2)

Copyright

© 2021, Nichols 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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