Essential function of the alveolin network in the subpellicular microtubules and conoid assembly in Toxoplasma gondii

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Abstract

The coccidian subgroup of Apicomplexa possesses an apical complex harboring a conoid, made of unique tubulin polymer fibers. This enigmatic organelle extrudes in extracellular invasive parasites and is associated to the apical polar ring (APR). The APR serves as microtubule-organizing center for the 22 subpellicular microtubules (SPMTs) that are linked to a patchwork of flattened vesicles, via an intricate network composed of alveolins. Here, we capitalize on ultrastructure expansion microscopy (U-ExM) to localize the Toxoplasma gondii Apical Cap protein 9 (AC9) and its partner AC10, identified by BioID, to the alveolin network and intercalated between the SPMTs. Parasites conditionally depleted in AC9 or AC10 replicate normally but are defective in microneme secretion and fail to invade and egress from infected cells. Electron microscopy revealed that the mature parasite mutants are conoidless, while U-ExM highlighted the disorganization of the SPMTs which likely results in the catastrophic loss of APR and conoid.

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All data generated or analysed during this study are included in the manuscript and supplementary file 1

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Nicolò Tosetti

Department of Microbiology and Molecular Medicine, University of Geneva, Geneva, Switzerland

Competing interests
No competing interests declared.
Nicolas Dos Santos Pacheco

Department of Microbiology and Molecular Medicine, University of Geneva, Geneva, Switzerland

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0003-1959-194X
Eloïse Bertiaux

Department of Cell Biology, University of Geneva, Geneva, Switzerland

Competing interests
No competing interests declared.
Bohumil Maco

Department of Microbiology and Molecular Medicine, University of Geneva, Geneva, Switzerland

Competing interests
No competing interests declared.
Lorène Bournonville

Department of Cell Biology, University of Geneva, Geneva, Switzerland

Competing interests
No competing interests declared.
Virginie Hamel

Department of Cell Biology, University of Geneva, Geneva, Switzerland

Competing interests
No competing interests declared.
Paul Guichard

Department of Cell Biology, University of Geneva, Geneva, Switzerland

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-0363-1049
Dominique Soldati-Favre

Department of Microbiology and Molecular Medicine, University of Geneva, Geneva, Switzerland

For correspondence
Dominique.Soldati-Favre@unige.ch

Competing interests
Dominique Soldati-Favre, Senior editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0003-4156-2109

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030_185325 and PP00P3_187198)

Dominique Soldati-Favre

H2020 European Research Council (695596 and 695596)

Dominique Soldati-Favre

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.