Lipoate-binding proteins and specific lipoate-protein ligases in microbial sulfur oxidation reveal an atypcial role for an old cofactor

  1. Xinyun Cao
  2. Tobias Koch
  3. Lydia Steffens
  4. Julia Finkensieper
  5. Renate Zigann
  6. John E Cronan
  7. Christiane Dahl  Is a corresponding author
  1. University of Illinois, United States
  2. Rheinische Friedrich-Wilhelms-Universität Bonn, Germany

Abstract

Many Bacteria and Archaea employ the heterodisulfide reductase (Hdr)-like sulfur oxidation pathway. The relevant genes are inevitably associated with genes encoding lipoate-binding proteins (LbpA). Here, deletion of the gene identified LbpA as an essential component of the Hdr-like sulfur-oxidizing system in the Alphaproteobacterium Hyphomicrobium denitrificans. Thus, a biological function was established for the universally conserved cofactor lipoate that is markedly different from its canonical roles in central metabolism. LbpAs likely function as sulfur-binding entities presenting substrate to different catalytic sites of the Hdr-like complex, similar to the substrate-channeling function of lipoate in carbon-metabolizing multienzyme complexes, e.g. pyruvate dehydrogenase. LbpAs serve a specific function in sulfur oxidation, cannot functionally replace the related GcvH protein in Bacillus subtilis and are not modified by the canonical E. coli and B. subtilis lipoyl attachment machineries. Instead, LplA-like lipoate-protein ligases encoded in or in immediate vicinity of hdr-lpbA gene clusters act specifically on these proteins.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2 and 3.

Article and author information

Author details

  1. Xinyun Cao

    Department of Biochemistry, University of Illinois, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7346-3909
  2. Tobias Koch

    Institut für Mikrobiologie and Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Lydia Steffens

    Institut für Mikrobiologie and Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Julia Finkensieper

    Institut für Mikrobiologie and Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Renate Zigann

    Institut für Mikrobiologie and Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. John E Cronan

    Department of Biochemistry, University of Illinois, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Christiane Dahl

    Institut für Mikrobiologie and Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
    For correspondence
    ChDahl@uni-bonn.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8288-7546

Funding

Deutsche Forschungsgemeinschaft (Da 351/8-1)

  • Christiane Dahl

National Institutes of Health (AI15650)

  • John E Cronan

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

Reviewing Editor

  1. Dianne K Newman, Howard Hughes Medical Institute, California Institute of Technology, United States

Version history

  1. Received: April 10, 2018
  2. Accepted: July 12, 2018
  3. Accepted Manuscript published: July 13, 2018 (version 1)
  4. Version of Record published: July 31, 2018 (version 2)

Copyright

© 2018, Cao 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. Xinyun Cao
  2. Tobias Koch
  3. Lydia Steffens
  4. Julia Finkensieper
  5. Renate Zigann
  6. John E Cronan
  7. Christiane Dahl
(2018)
Lipoate-binding proteins and specific lipoate-protein ligases in microbial sulfur oxidation reveal an atypcial role for an old cofactor
eLife 7:e37439.
https://doi.org/10.7554/eLife.37439

Share this article

https://doi.org/10.7554/eLife.37439

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