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Cryo-tomography reveals rigid-body motion and organization of apicomplexan invasion machinery

Author

Listed:
  • Long Gui

    (University of Texas, Southwestern Medical Center)

  • William J. O’Shaughnessy

    (University of Texas, Southwestern Medical Center)

  • Kai Cai

    (University of Texas, Southwestern Medical Center
    University of Texas, Southwestern Medical Center)

  • Evan Reetz

    (University of Texas, Southwestern Medical Center)

  • Michael L. Reese

    (University of Texas, Southwestern Medical Center
    University of Texas, Southwestern Medical Center)

  • Daniela Nicastro

    (University of Texas, Southwestern Medical Center)

Abstract

The apical complex is a specialized collection of cytoskeletal and secretory machinery in apicomplexan parasites, which include the pathogens that cause malaria and toxoplasmosis. Its structure and mechanism of motion are poorly understood. We used cryo-FIB-milling and cryo-electron tomography to visualize the 3D-structure of the apical complex in its protruded and retracted states. Averages of conoid-fibers revealed their polarity and unusual nine-protofilament arrangement with associated proteins connecting and likely stabilizing the fibers. Neither the structure of the conoid-fibers nor the architecture of the spiral-shaped conoid complex change during protrusion or retraction. Thus, the conoid moves as a rigid body, and is not spring-like and compressible, as previously suggested. Instead, the apical-polar-rings (APR), previously considered rigid, dilate during conoid protrusion. We identified actin-like filaments connecting the conoid and APR during protrusion, suggesting a role during conoid movements. Furthermore, our data capture the parasites in the act of secretion during conoid protrusion.

Suggested Citation

  • Long Gui & William J. O’Shaughnessy & Kai Cai & Evan Reetz & Michael L. Reese & Daniela Nicastro, 2023. "Cryo-tomography reveals rigid-body motion and organization of apicomplexan invasion machinery," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37327-w
    DOI: 10.1038/s41467-023-37327-w
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    References listed on IDEAS

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    1. Shrawan Kumar Mageswaran & Amandine Guérin & Liam M. Theveny & William David Chen & Matthew Martinez & Maryse Lebrun & Boris Striepen & Yi-Wei Chang, 2021. "In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Shrawan Kumar Mageswaran & Amandine Guérin & Liam M. Theveny & William David Chen & Matthew Martinez & Maryse Lebrun & Boris Striepen & Yi-Wei Chang, 2021. "Author Correction: In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    3. Shaojun Long & Bryan Anthony & Lisa L. Drewry & L. David Sibley, 2017. "A conserved ankyrin repeat-containing protein regulates conoid stability, motility and cell invasion in Toxoplasma gondii," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    4. Javier Periz & Mario Rosario & Alexandra McStea & Simon Gras & Colin Loney & Lin Wang & Marisa L. Martin-Fernandez & Markus Meissner, 2019. "A highly dynamic F-actin network regulates transport and recycling of micronemes in Toxoplasma gondii vacuoles," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
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    1. Nicolas Dos Santos Pacheco & Albert Tell i Puig & Amandine Guérin & Matthew Martinez & Bohumil Maco & Nicolò Tosetti & Estefanía Delgado-Betancourt & Matteo Lunghi & Boris Striepen & Yi-Wei Chang & Do, 2024. "Sustained rhoptry docking and discharge requires Toxoplasma gondii intraconoidal microtubule-associated proteins," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Matthew Martinez & Shrawan Kumar Mageswaran & Amandine Guérin & William David Chen & Cameron Parker Thompson & Sabine Chavin & Dominique Soldati-Favre & Boris Striepen & Yi-Wei Chang, 2023. "Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Vincent Louvel & Romuald Haase & Olivier Mercey & Marine H. Laporte & Thibaut Eloy & Étienne Baudrier & Denis Fortun & Dominique Soldati-Favre & Virginie Hamel & Paul Guichard, 2023. "iU-ExM: nanoscopy of organelles and tissues with iterative ultrastructure expansion microscopy," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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