1. Evolutionary Biology
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Microbial eukaryotes have adapted to hypoxia by horizontal acquisitions of a gene involved in rhodoquinone biosynthesis

  1. Courtney W Stairs
  2. Laura Eme
  3. Sergio Muñoz-Gómez
  4. Alejandro Cohen
  5. Graham Dellaire
  6. Jennifer N Shepherd
  7. James P Fawcett
  8. Andrew J Roger  Is a corresponding author
  1. Dalhousie University, Canada
  2. Gonzaga University, United States
Research Article
  • Cited 24
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Cite this article as: eLife 2018;7:e34292 doi: 10.7554/eLife.34292

Abstract

Under hypoxic conditions, some organisms use an electron transport chain consisting of only complex I and II (CII) to generate the proton gradient essential for ATP production. In these cases, CII functions as a fumarate reductase that accepts electrons from a low electron potential quinol, rhodoquinol (RQ). To clarify the origins of RQ-mediated fumarate reduction in eukaryotes, we investigated the origin and function of rqua, a gene encoding an RQ biosynthetic enzyme. Rqua is very patchily distributed across eukaryotes and bacteria adapted to hypoxia. Phylogenetic analyses suggest lateral gene transfer (LGT) of rqua from bacteria to eukaryotes occurred at least twice and the gene was transferred multiple times amongst protists. We demonstrate that RQUA functions in the mitochondrion-related organelles of the anaerobic protist Pygsuia and is correlated with the presence of RQ. These analyses reveal the role of gene transfer in the evolutionary remodeling of mitochondria in adaptation to hypoxia.

Data availability

All data is available on Dryad DOI: https://doi.org/10.5061/dryad.qp745

The following data sets were generated

Article and author information

Author details

  1. Courtney W Stairs

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6650-0970
  2. Laura Eme

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Sergio Muñoz-Gómez

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Alejandro Cohen

    Proteomics Core Facility, Life Sciences Research Institute, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Graham Dellaire

    Department of Pathology, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3466-6316
  6. Jennifer N Shepherd

    Department of Chemistry and Biochemistry, Gonzaga University, Spokane, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. James P Fawcett

    Proteomics Core Facility, Dalhousie University, Halifax, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Andrew J Roger

    Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada
    For correspondence
    Andrew.Roger@Dal.Ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1370-9820

Funding

Canadian Institutes of Health Research (MOP 142349)

  • Andrew J Roger

National Institutes of Health (1R15GM096398-01)

  • Jennifer N Shepherd

Natural Sciences and Engineering Research Council of Canada

  • Courtney W Stairs

Killam Trusts

  • Courtney W Stairs

Natural Sciences and Engineering Research Council of Canada (RGPIN 05616)

  • Graham Dellaire

Canadian Institutes of Health Research (MOP 341174)

  • James P Fawcett

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

Reviewing Editor

  1. John McCutcheon, University of Montana

Publication history

  1. Received: December 12, 2017
  2. Accepted: April 25, 2018
  3. Accepted Manuscript published: April 26, 2018 (version 1)
  4. Version of Record published: May 15, 2018 (version 2)
  5. Version of Record updated: May 18, 2018 (version 3)

Copyright

© 2018, Stairs 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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