Stable endocytic structures navigate the complex pellicle of apicomplexan parasites

Ludek Koreny, Brandon N. Mercado-Saavedra, Christen M. Klinger, Konstantin Barylyuk, Simon Butterworth, Jennifer Hirst, Yolanda Rivera-Cuevas, Nathan R. Zaccai, Victoria J. C. Holzer, Andreas Klingl, Joel B. Dacks, Vern B. Carruthers, Margaret S. Robinson, Simon Gras () and Ross F. Waller ()
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Ludek Koreny: University of Cambridge
Brandon N. Mercado-Saavedra: University of Cambridge
Christen M. Klinger: University of Alberta
Konstantin Barylyuk: University of Cambridge
Simon Butterworth: University of Cambridge
Jennifer Hirst: University of Cambridge
Yolanda Rivera-Cuevas: University of Michigan Medical School
Nathan R. Zaccai: University of Cambridge
Victoria J. C. Holzer: Plant Development, Ludwig-Maximilians-University Munich
Andreas Klingl: Plant Development, Ludwig-Maximilians-University Munich
Joel B. Dacks: University of Alberta
Vern B. Carruthers: University of Michigan Medical School
Margaret S. Robinson: University of Cambridge
Simon Gras: Ludwig-Maximilians-University Munich
Ross F. Waller: University of Cambridge

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract Apicomplexan parasites have immense impacts on humanity, but their basic cellular processes are often poorly understood. Where endocytosis occurs in these cells, how conserved this process is with other eukaryotes, and what the functions of endocytosis are across this phylum are major unanswered questions. Using the apicomplexan model Toxoplasma, we identified the molecular composition and behavior of unusual, fixed endocytic structures. Here, stable complexes of endocytic proteins differ markedly from the dynamic assembly/disassembly of these machineries in other eukaryotes. We identify that these endocytic structures correspond to the ‘micropore’ that has been observed throughout the Apicomplexa. Moreover, conserved molecular adaptation of this structure is seen in apicomplexans including the kelch-domain protein K13 that is central to malarial drug-resistance. We determine that a dominant function of endocytosis in Toxoplasma is plasma membrane homeostasis, rather than parasite nutrition, and that these specialized endocytic structures originated early in infrakingdom Alveolata likely in response to the complex cell pellicle that defines this medically and ecologically important ancient eukaryotic lineage.

Date: 2023
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DOI: 10.1038/s41467-023-37431-x

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