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Variable microtubule architecture in the malaria parasite

Author

Listed:
  • Josie L. Ferreira

    (Centre for Structural Systems Biology
    Leibniz Institute for Virology (LIV)
    Bernhard Nocht Institute for Tropical Medicine
    Birkbeck, University of London)

  • Vojtěch Pražák

    (Centre for Structural Systems Biology
    Leibniz Institute for Virology (LIV)
    University of Oxford)

  • Daven Vasishtan

    (Centre for Structural Systems Biology
    Leibniz Institute for Virology (LIV)
    University of Oxford)

  • Marc Siggel

    (Centre for Structural Systems Biology
    European Molecular Biology Laboratory)

  • Franziska Hentzschel

    (Heidelberg University Medical School
    German Center for Infection Research, DZIF Partner Site Heidelberg)

  • Annika M. Binder

    (Heidelberg University Medical School)

  • Emma Pietsch

    (Centre for Structural Systems Biology
    Bernhard Nocht Institute for Tropical Medicine
    University of Hamburg)

  • Jan Kosinski

    (Centre for Structural Systems Biology
    European Molecular Biology Laboratory
    Structural and Computational Biology Unit, EMBL)

  • Friedrich Frischknecht

    (Heidelberg University Medical School
    German Center for Infection Research, DZIF Partner Site Heidelberg)

  • Tim W. Gilberger

    (Centre for Structural Systems Biology
    Bernhard Nocht Institute for Tropical Medicine
    University of Hamburg)

  • Kay Grünewald

    (Centre for Structural Systems Biology
    Leibniz Institute for Virology (LIV)
    University of Oxford
    University of Hamburg)

Abstract

Microtubules are a ubiquitous eukaryotic cytoskeletal element typically consisting of 13 protofilaments arranged in a hollow cylinder. This arrangement is considered the canonical form and is adopted by most organisms, with rare exceptions. Here, we use in situ electron cryo-tomography and subvolume averaging to analyse the changing microtubule cytoskeleton of Plasmodium falciparum, the causative agent of malaria, throughout its life cycle. Unexpectedly, different parasite forms have distinct microtubule structures coordinated by unique organising centres. In merozoites, the most widely studied form, we observe canonical microtubules. In migrating mosquito forms, the 13 protofilament structure is further reinforced by interrupted luminal helices. Surprisingly, gametocytes contain a wide distribution of microtubule structures ranging from 13 to 18 protofilaments, doublets and triplets. Such a diversity of microtubule structures has not been observed in any other organism to date and is likely evidence of a distinct role in each life cycle form. This data provides a unique view into an unusual microtubule cytoskeleton of a relevant human pathogen.

Suggested Citation

  • Josie L. Ferreira & Vojtěch Pražák & Daven Vasishtan & Marc Siggel & Franziska Hentzschel & Annika M. Binder & Emma Pietsch & Jan Kosinski & Friedrich Frischknecht & Tim W. Gilberger & Kay Grünewald, 2023. "Variable microtubule architecture in the malaria parasite," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36627-5
    DOI: 10.1038/s41467-023-36627-5
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    References listed on IDEAS

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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Jiahong Li & Gerald J. Shami & Ellie Cho & Boyin Liu & Eric Hanssen & Matthew W. A. Dixon & Leann Tilley, 2022. "Repurposing the mitotic machinery to drive cellular elongation and chromatin reorganisation in Plasmodium falciparum gametocytes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    4. Sylwia D. Boltryk & Armin Passecker & Arne Alder & Eilidh Carrington & Marga Vegte-Bolmer & Geert-Jan Gemert & Alex Starre & Hans-Peter Beck & Robert W. Sauerwein & Taco W. A. Kooij & Nicolas M. B. Br, 2021. "CRISPR/Cas9-engineered inducible gametocyte producer lines as a valuable tool for Plasmodium falciparum malaria transmission research," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    5. David A. Baker & Lindsay B. Stewart & Jonathan M. Large & Paul W. Bowyer & Keith H. Ansell & María B. Jiménez-Díaz & Majida El Bakkouri & Kristian Birchall & Koen J. Dechering & Nathalie S. Bouloc & P, 2017. "A potent series targeting the malarial cGMP-dependent protein kinase clears infection and blocks transmission," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    6. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
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