Structural characterization of encapsulated ferritin provides insight into iron storage in bacterial nanocompartments

Abstract

Ferritins are ubiquitous proteins that oxidise and store iron within a protein shell to protect cells from oxidative damage. We have characterized the structure and function of a new member of the ferritin superfamily that is sequestered within an encapsulin capsid. We show that this encapsulated ferritin (EncFtn) has two main alpha helices, which assemble in a metal dependent manner to form a ferroxidase center at a dimer interface. EncFtn adopts an open decameric structure that is topologically distinct from other ferritins. While EncFtn acts as a ferroxidase, it cannot mineralize iron. Conversely, the encapsulin shell associates with iron, but is not enzymatically active, and we demonstrate that EncFtn must be housed within the encapsulin for iron storage. This encapsulin nanocompartment is widely distributed in bacteria and archaea and represents a distinct class of iron storage system, where the oxidation and mineralization of iron are distributed between two proteins.

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Author details

  1. Didi He

    Institute of Quantitative Biology, Biochemistry and Biotechnology, The University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Sam Hughes

    The School of Chemistry, The University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Sally Vanden-Hehir

    The School of Chemistry, The University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Atanas Georgiev

    Institute of Quantitative Biology, Biochemistry and Biotechnology, The University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Kirsten Altenbach

    Institute of Quantitative Biology, Biochemistry and Biotechnology, The University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Emma J Tarrant

    Institute for Cell and Molecular Biosciences, Newcastle University, Newcasle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. C Logan Mackay

    The School of Chemistry, The University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Kevin J Waldron

    Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5577-7357
  9. David J Clarke

    The School of Chemistry, The University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    dave.clarke@ed.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  10. Jon Marles-Wright

    Institute of Quantitative Biology, Biochemistry and Biotechnology, The University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    jon.marles-wright1@ncl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9156-3284

Funding

Royal Society (RG130585)

  • Jon Marles-Wright

China Scholarship Council

  • Didi He

Biotechnology and Biological Sciences Research Council (BB/N005570/1)

  • David J Clarke
  • Jon Marles-Wright

Wellcome Trust (098375/Z/12/Z)

  • Emma J Tarrant
  • Kevin J Waldron

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

Reviewing Editor

  1. Richard Losick, Harvard University, United States

Version history

  1. Received: June 24, 2016
  2. Accepted: August 14, 2016
  3. Accepted Manuscript published: August 16, 2016 (version 1)
  4. Accepted Manuscript updated: August 24, 2016 (version 2)
  5. Version of Record published: September 6, 2016 (version 3)

Copyright

© 2016, He 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. Didi He
  2. Sam Hughes
  3. Sally Vanden-Hehir
  4. Atanas Georgiev
  5. Kirsten Altenbach
  6. Emma J Tarrant
  7. C Logan Mackay
  8. Kevin J Waldron
  9. David J Clarke
  10. Jon Marles-Wright
(2016)
Structural characterization of encapsulated ferritin provides insight into iron storage in bacterial nanocompartments
eLife 5:e18972.
https://doi.org/10.7554/eLife.18972

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https://doi.org/10.7554/eLife.18972

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