Stable endocytic structures navigate the complex pellicle of apicomplexan parasites
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 unans...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-04-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-37431-x |
| _version_ | 1797845856140918784 |
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| author | 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 Ross F. Waller |
| author_facet | 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 Ross F. Waller |
| author_sort | Ludek Koreny |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-09T17:45:44Z |
| format | Article |
| id | doaj.art-1f2579bc796c4acc84f4b66c62b1aa83 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-04-09T17:45:44Z |
| publishDate | 2023-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-1f2579bc796c4acc84f4b66c62b1aa832023-04-16T11:18:05ZengNature PortfolioNature Communications2041-17232023-04-0114111910.1038/s41467-023-37431-xStable endocytic structures navigate the complex pellicle of apicomplexan parasitesLudek Koreny0Brandon N. Mercado-Saavedra1Christen M. Klinger2Konstantin Barylyuk3Simon Butterworth4Jennifer Hirst5Yolanda Rivera-Cuevas6Nathan R. Zaccai7Victoria J. C. Holzer8Andreas Klingl9Joel B. Dacks10Vern B. Carruthers11Margaret S. Robinson12Simon Gras13Ross F. Waller14Department of Biochemistry, University of CambridgeDepartment of Biochemistry, University of CambridgeDivision of Infectious Diseases, Department of Medicine, University of AlbertaDepartment of Biochemistry, University of CambridgeDepartment of Biochemistry, University of CambridgeCambridge Institute for Medical Research, University of CambridgeDepartment of Microbiology and Immunology, University of Michigan Medical SchoolCambridge Institute for Medical Research, University of CambridgePlant Development, Ludwig-Maximilians-University MunichPlant Development, Ludwig-Maximilians-University MunichDivision of Infectious Diseases, Department of Medicine, University of AlbertaDepartment of Microbiology and Immunology, University of Michigan Medical SchoolCambridge Institute for Medical Research, University of CambridgeExperimental Parasitology, Department for Veterinary Sciences, Ludwig-Maximilians-University MunichDepartment of Biochemistry, University of CambridgeAbstract 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.https://doi.org/10.1038/s41467-023-37431-x |
| spellingShingle | 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 Ross F. Waller Stable endocytic structures navigate the complex pellicle of apicomplexan parasites Nature Communications |
| title | Stable endocytic structures navigate the complex pellicle of apicomplexan parasites |
| title_full | Stable endocytic structures navigate the complex pellicle of apicomplexan parasites |
| title_fullStr | Stable endocytic structures navigate the complex pellicle of apicomplexan parasites |
| title_full_unstemmed | Stable endocytic structures navigate the complex pellicle of apicomplexan parasites |
| title_short | Stable endocytic structures navigate the complex pellicle of apicomplexan parasites |
| title_sort | stable endocytic structures navigate the complex pellicle of apicomplexan parasites |
| url | https://doi.org/10.1038/s41467-023-37431-x |
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