In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems

Shrawan Kumar Mageswaran, Amandine Guérin, Liam M. Theveny, William David Chen, Matthew Martinez, Maryse Lebrun, Boris Striepen and Yi-Wei Chang ()
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Shrawan Kumar Mageswaran: University of Pennsylvania
Amandine Guérin: University of Pennsylvania
Liam M. Theveny: University of Pennsylvania
William David Chen: University of Pennsylvania
Matthew Martinez: University of Pennsylvania
Maryse Lebrun: Université de Montpellier
Boris Striepen: University of Pennsylvania
Yi-Wei Chang: University of Pennsylvania

Nature Communications, 2021, vol. 12, issue 1, 1-12

Abstract: Abstract Parasites of the phylum Apicomplexa cause important diseases including malaria, cryptosporidiosis and toxoplasmosis. These intracellular pathogens inject the contents of an essential organelle, the rhoptry, into host cells to facilitate invasion and infection. However, the structure and mechanism of this eukaryotic secretion system remain elusive. Here, using cryo-electron tomography and subtomogram averaging, we report the conserved architecture of the rhoptry secretion system in the invasive stages of two evolutionarily distant apicomplexans, Cryptosporidium parvum and Toxoplasma gondii. In both species, we identify helical filaments, which appear to shape and compartmentalize the rhoptries, and an apical vesicle (AV), which facilitates docking of the rhoptry tip at the parasite’s apical region with the help of an elaborate ultrastructure named the rhoptry secretory apparatus (RSA); the RSA anchors the AV at the parasite plasma membrane. Depletion of T. gondii Nd9, a protein required for rhoptry secretion, disrupts the RSA ultrastructure and AV-anchoring. Moreover, T. gondii contains a line of AV-like vesicles, which interact with a pair of microtubules and accumulate towards the AV, leading to a working model for AV-reloading and discharging of multiple rhoptries. Together, our analyses provide an ultrastructural framework to understand how these important parasites deliver effectors into host cells.

Date: 2021
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DOI: 10.1038/s41467-021-25309-9

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