Homologue replacement in the import motor of the mitochondrial inner membrane of trypanosomes

  1. Corinne von Känel
  2. Sergio A Muñoz-Gómez
  3. Silke Oeljeklaus
  4. Christoph Wenger
  5. Bettina Warscheid
  6. Jeremy G Wideman  Is a corresponding author
  7. Anke Harsman  Is a corresponding author
  8. Andre Schneider  Is a corresponding author
  1. University of Berne, Switzerland
  2. Arizona State University, United States
  3. University of Freiburg, Germany

Abstract

Many mitochondrial proteins contain N-terminal presequences that direct them to the organelle. The main driving force for their translocation across the inner membrane is provided by the presequence translocase-associated motor (PAM) which contains the J-protein Pam18. Here, we show that in the PAM of Trypanosoma brucei the function of Pam18 has been replaced by the non-orthologous euglenozoan-specific J-protein TbPam27. TbPam27 is specifically required for the import of mitochondrial presequence-containing but not for carrier proteins. Similar to yeast Pam18, TbPam27 requires an intact J-domain to function. Surprisingly, T. brucei still contains a bona fide Pam18 orthologue that, while essential for normal growth, is not involved in protein import. Thus, during evolution of kinetoplastids, Pam18 has been replaced by TbPam27. We propose that this replacement is linked to the transition from two ancestral and functionally distinct TIM complexes, found in most eukaryotes, to the single bifunctional TIM complex present in trypanosomes.

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All produced data are contained within the manuscript (e.g. Data Source files)

Article and author information

Author details

  1. Corinne von Känel

    Department of Chemistry and Biochemistry, University of Berne, Bern, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Sergio A Muñoz-Gómez

    Center for Mechanisms of Evolution, Arizona State University, Arizona, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Silke Oeljeklaus

    Biochemistry and Functional Proteomics, Institute of Biology II, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Christoph Wenger

    Department of Chemistry and Biochemistry, University of Berne, Bern, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Bettina Warscheid

    Biochemistry and Functional Proteomics, Institute of Biology II, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5096-1975
  6. Jeremy G Wideman

    Center for Mechanisms of Evolution, Biodesign Institute, Arizona State University, Tempe, United States
    For correspondence
    Jeremy.Wideman@asu.edu
    Competing interests
    The authors declare that no competing interests exist.
  7. Anke Harsman

    Department of Chemistry and Biochemistry, University of Berne, Bern, Switzerland
    For correspondence
    anke.harsman@web.de
    Competing interests
    The authors declare that no competing interests exist.
  8. Andre Schneider

    Department of Chemistry and Biochemistry, University of Berne, Bern, Switzerland
    For correspondence
    andre.schneider@dcb.unibe.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5421-0909

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (175563)

  • Andre Schneider

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (NCCR RNA and Disease)

  • Andre Schneider

ERC Consolidator grant (648235)

  • Bettina Warscheid

Deutsche Forschungsgemeinschaft (403222702/SFB 1381)

  • Bettina Warscheid

Germany's Excellence Strategy (CIBSS - EXC-2189 - Project ID 390939984)

  • Bettina Warscheid

Excellence Initiative of the German Federal and State Governments (EXC 294 BIOSS)

  • Bettina Warscheid

Peter und Traudl Engelhorn foundation

  • Anke Harsman

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

Reviewing Editor

  1. Agnieszka Chacinska, University of Warsaw, Poland

Version history

  1. Received: October 8, 2019
  2. Accepted: February 26, 2020
  3. Accepted Manuscript published: February 27, 2020 (version 1)
  4. Version of Record published: March 10, 2020 (version 2)

Copyright

© 2020, von Känel 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. Corinne von Känel
  2. Sergio A Muñoz-Gómez
  3. Silke Oeljeklaus
  4. Christoph Wenger
  5. Bettina Warscheid
  6. Jeremy G Wideman
  7. Anke Harsman
  8. Andre Schneider
(2020)
Homologue replacement in the import motor of the mitochondrial inner membrane of trypanosomes
eLife 9:e52560.
https://doi.org/10.7554/eLife.52560

Share this article

https://doi.org/10.7554/eLife.52560

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