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.

Cambridge Institute for Medical Research University of Cambridge Cambridge CB2 1QW UK

Department of Biochemistry University of Cambridge Cambridge CB2 1QW UK

Department of Microbiology and Immunology University of Michigan Medical School Ann Arbor MI 48109 USA

Division of Infectious Diseases Department of Medicine University of Alberta Edmonton AB T6G 2R3 Canada

Experimental Parasitology Department for Veterinary Sciences Ludwig Maximilians University Munich Planegg Martinsried 82152 Germany

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice 370 05 Czech Republic

Plant Development Ludwig Maximilians University Munich Planegg Martinsried 82152 Germany

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