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

• Published in: Nature communications Vol. 14; no. 1; pp. 1775 - 14
• Main Authors: Gui, Long, O’Shaughnessy, William J., Cai, Kai, Reetz, Evan, Reese, Michael L., Nicastro, Daniela
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 30.03.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 101/28; 13/106; 631/326/417/1716; 631/535/1258/1260; 631/80/2373; Actin; Cell Membrane - ultrastructure; Compressibility; Cytoskeleton; Cytoskeleton - ultrastructure; Electron Microscope Tomography; Fibers; Filaments; Humanities and Social Sciences; Malaria; Milling (machining); multidisciplinary; Neospora - cytology; Neospora - ultrastructure; Organelles; Parasites; Rigid-body dynamics; Science; Science (multidisciplinary); Tomography; Toxoplasma - cytology; Toxoplasma - ultrastructure; Toxoplasmosis; Tubulin - ultrastructure; Vector-borne diseases
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-37327-w

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. In this study, the authors use cryo-focused-ion-beammilling and cryo-electron tomography to image the apical complex of parasites in their native states. They report insights into the parasite invasion machinery in its protruded and retracted states in three dimensions, including all cytoskeletal assemblies, secretory organelles, and membranes intact.