IDEAS home Printed from https://ideas.repec.org/a/plo/pbio00/3000098.html
   My bibliography  Save this article

Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in Trichomonas vaginalis

Author

Listed:
  • Abhijith Makki
  • Petr Rada
  • Vojtěch Žárský
  • Sami Kereïche
  • Lubomír Kováčik
  • Marian Novotný
  • Tobias Jores
  • Doron Rapaport
  • Jan Tachezy

Abstract

Mitochondria originated from proteobacterial endosymbionts, and their transition to organelles was tightly linked to establishment of the protein import pathways. The initial import of most proteins is mediated by the translocase of the outer membrane (TOM). Although TOM is common to all forms of mitochondria, an unexpected diversity of subunits between eukaryotic lineages has been predicted. However, experimental knowledge is limited to a few organisms, and so far, it remains unsettled whether the triplet-pore or the twin-pore structure is the generic form of TOM complex. Here, we analysed the TOM complex in hydrogenosomes, a metabolically specialised anaerobic form of mitochondria found in the excavate Trichomonas vaginalis. We demonstrate that the highly divergent β-barrel T. vaginalis TOM (TvTom)40-2 forms a translocation channel to conduct hydrogenosomal protein import. TvTom40-2 is present in high molecular weight complexes, and their analysis revealed the presence of four tail-anchored (TA) proteins. Two of them, Tom36 and Tom46, with heat shock protein (Hsp)20 and tetratricopeptide repeat (TPR) domains, can bind hydrogenosomal preproteins and most likely function as receptors. A third subunit, Tom22-like protein, has a short cis domain and a conserved Tom22 transmembrane segment but lacks a trans domain. The fourth protein, hydrogenosomal outer membrane protein 19 (Homp19) has no known homology. Furthermore, our data indicate that TvTOM is associated with sorting and assembly machinery (Sam)50 that is involved in β-barrel assembly. Visualisation of TvTOM by electron microscopy revealed that it forms three pores and has an unconventional skull-like shape. Although TvTOM seems to lack Tom7, our phylogenetic profiling predicted Tom7 in free-living excavates. Collectively, our results suggest that the triplet-pore TOM complex, composed of three conserved subunits, was present in the last common eukaryotic ancestor (LECA), while receptors responsible for substrate binding evolved independently in different eukaryotic lineages.The highly divergent outer membrane translocase (TOM) from the Trichomonas hydrogenosome (an organelle related to mitochondria) is composed of conserved core and lineage-specific subunits, and has an unconventional skull-like triplet-pore structure.Author summary: Mitochondria carry out many vital functions in the eukaryotic cells, from energy metabolism to programmed cell death. These organelles descended from bacterial endosymbionts, and during their evolution, the cell established a mechanism to transport nuclear-encoded proteins into mitochondria. Embedded in the mitochondrial outer membrane is a molecular machine, known as the translocase of the outer membrane (TOM) complex, that plays a key role in protein import and biogenesis of the organelle. Here, we provide evidence that the TOM complex of hydrogenosomes, a metabolically specialised anaerobic form of mitochondria in Trichomonas vaginalis, is composed of highly divergent core subunits and lineage-specific peripheral subunits. Despite the evolutionary distance, the T. vaginalis TOM (TvTOM) complex has a conserved triplet-pore structure but with a unique skull-like shape suggesting that the TOM in the early mitochondrion could have formed three pores. Our results contribute to a better understanding of the evolution and adaptation of protein import machinery in anaerobic forms of mitochondria.

Suggested Citation

  • Abhijith Makki & Petr Rada & Vojtěch Žárský & Sami Kereïche & Lubomír Kováčik & Marian Novotný & Tobias Jores & Doron Rapaport & Jan Tachezy, 2019. "Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in Trichomonas vaginalis," PLOS Biology, Public Library of Science, vol. 17(1), pages 1-32, January.
  • Handle: RePEc:plo:pbio00:3000098
    DOI: 10.1371/journal.pbio.3000098
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3000098
    Download Restriction: no

    File URL: https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3000098&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pbio.3000098?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Jan Mani & Silvia Desy & Moritz Niemann & Astrid Chanfon & Silke Oeljeklaus & Mascha Pusnik & Oliver Schmidt & Carolin Gerbeth & Chris Meisinger & Bettina Warscheid & André Schneider, 2015. "Mitochondrial protein import receptors in Kinetoplastids reveal convergent evolution over large phylogenetic distances," Nature Communications, Nature, vol. 6(1), pages 1-12, May.
    2. Ivan Hrdy & Robert P. Hirt & Pavel Dolezal & Lucie Bardonová & Peter G. Foster & Jan Tachezy & T. Martin Embley, 2004. "Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I," Nature, Nature, vol. 432(7017), pages 618-622, December.
    3. Joran Martijn & Julian Vosseberg & Lionel Guy & Pierre Offre & Thijs J. G. Ettema, 2018. "Deep mitochondrial origin outside the sampled alphaproteobacteria," Nature, Nature, vol. 557(7703), pages 101-105, May.
    4. T. Martin Embley & William Martin, 2006. "Eukaryotic evolution, changes and challenges," Nature, Nature, vol. 440(7084), pages 623-630, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Pavel Dolezal & Michael J Dagley & Maya Kono & Peter Wolynec & Vladimir A Likić & Jung Hock Foo & Miroslava Sedinová & Jan Tachezy & Anna Bachmann & Iris Bruchhaus & Trevor Lithgow, 2010. "The Essentials of Protein Import in the Degenerate Mitochondrion of Entamoeba histolytica," PLOS Pathogens, Public Library of Science, vol. 6(3), pages 1-13, March.
    2. Tara A. Mahendrarajah & Edmund R. R. Moody & Dominik Schrempf & Lénárd L. Szánthó & Nina Dombrowski & Adrián A. Davín & Davide Pisani & Philip C. J. Donoghue & Gergely J. Szöllősi & Tom A. Williams & , 2023. "ATP synthase evolution on a cross-braced dated tree of life," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Zhongyi Lu & Runyue Xia & Siyu Zhang & Jie Pan & Yang Liu & Yuri I. Wolf & Eugene V. Koonin & Meng Li, 2024. "Evolution of optimal growth temperature in Asgard archaea inferred from the temperature dependence of GDP binding to EF-1A," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    4. Heaps Sarah E. & Nye Tom M.W. & Boys Richard J. & Williams Tom A. & Embley T. Martin, 2014. "Bayesian modelling of compositional heterogeneity in molecular phylogenetics," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 13(5), pages 589-609, October.
    5. Florent Waltz & Thalia Salinas-Giegé & Robert Englmeier & Herrade Meichel & Heddy Soufari & Lauriane Kuhn & Stefan Pfeffer & Friedrich Förster & Benjamin D. Engel & Philippe Giegé & Laurence Drouard &, 2021. "How to build a ribosome from RNA fragments in Chlamydomonas mitochondria," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    6. Anaïs Gibert & Danièle Magda & Laurent Hazard, 2015. "Interplay between Endophyte Prevalence, Effects and Transmission: Insights from a Natural Grass Population," PLOS ONE, Public Library of Science, vol. 10(10), pages 1-17, October.
    7. Caroline E. Dewar & Silke Oeljeklaus & Jan Mani & Wignand W. D. Mühlhäuser & Corinne Känel & Johannes Zimmermann & Torsten Ochsenreiter & Bettina Warscheid & André Schneider, 2022. "Mistargeting of aggregation prone mitochondrial proteins activates a nucleus-mediated posttranscriptional quality control pathway in trypanosomes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Tom A Williams & T Martin Embley & Eva Heinz, 2011. "Informational Gene Phylogenies Do Not Support a Fourth Domain of Life for Nucleocytoplasmic Large DNA Viruses," PLOS ONE, Public Library of Science, vol. 6(6), pages 1-11, June.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pbio00:3000098. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosbiology (email available below). General contact details of provider: https://journals.plos.org/plosbiology/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.