Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography
Abstract The phylum Apicomplexa comprises important eukaryotic parasites that invade host tissues and cells using a unique mechanism of gliding motility. Gliding is powered by actomyosin motors that translocate host-attached surface adhesins along the parasite cell body. Actin filaments (F-actin) ge...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-08-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-40520-6 |
| _version_ | 1797558701788233728 |
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| author | Matthew Martinez Shrawan Kumar Mageswaran Amandine Guérin William David Chen Cameron Parker Thompson Sabine Chavin Dominique Soldati-Favre Boris Striepen Yi-Wei Chang |
| author_facet | Matthew Martinez Shrawan Kumar Mageswaran Amandine Guérin William David Chen Cameron Parker Thompson Sabine Chavin Dominique Soldati-Favre Boris Striepen Yi-Wei Chang |
| author_sort | Matthew Martinez |
| collection | DOAJ |
| description | Abstract The phylum Apicomplexa comprises important eukaryotic parasites that invade host tissues and cells using a unique mechanism of gliding motility. Gliding is powered by actomyosin motors that translocate host-attached surface adhesins along the parasite cell body. Actin filaments (F-actin) generated by Formin1 play a central role in this critical parasitic activity. However, their subcellular origin, path and ultrastructural arrangement are poorly understood. Here we used cryo-electron tomography to image motile Cryptosporidium parvum sporozoites and reveal the cellular architecture of F-actin at nanometer-scale resolution. We demonstrate that F-actin nucleates at the apically positioned preconoidal rings and is channeled into the pellicular space between the parasite plasma membrane and the inner membrane complex in a conoid extrusion-dependent manner. Within the pellicular space, filaments on the inner membrane complex surface appear to guide the apico-basal flux of F-actin. F-actin concordantly accumulates at the basal end of the parasite. Finally, analyzing a Formin1-depleted Toxoplasma gondii mutant pinpoints the upper preconoidal ring as the conserved nucleation hub for F-actin in Cryptosporidium and Toxoplasma. Together, we provide an ultrastructural model for the life cycle of F-actin for apicomplexan gliding motility. |
| first_indexed | 2024-03-10T17:35:11Z |
| format | Article |
| id | doaj.art-13a350adc2704a6a8ba35bd0fb27a960 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:35:11Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-13a350adc2704a6a8ba35bd0fb27a9602023-11-20T09:52:31ZengNature PortfolioNature Communications2041-17232023-08-0114111610.1038/s41467-023-40520-6Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomographyMatthew Martinez0Shrawan Kumar Mageswaran1Amandine Guérin2William David Chen3Cameron Parker Thompson4Sabine Chavin5Dominique Soldati-Favre6Boris Striepen7Yi-Wei Chang8Department of Biochemistry and Biophysics, Perelman School of Medicine, University of PennsylvaniaDepartment of Biochemistry and Biophysics, Perelman School of Medicine, University of PennsylvaniaDepartment of Pathobiology, School of Veterinary Medicine, University of PennsylvaniaDepartment of Biochemistry and Biophysics, Perelman School of Medicine, University of PennsylvaniaPennsylvania Muscle Institute, Perelman School of Medicine, University of PennsylvaniaDepartment of Physics and Astronomy, University of PennsylvaniaDepartment of Microbiology and Molecular Medicine, Faculty of Medicine, University of GenevaDepartment of Pathobiology, School of Veterinary Medicine, University of PennsylvaniaDepartment of Biochemistry and Biophysics, Perelman School of Medicine, University of PennsylvaniaAbstract The phylum Apicomplexa comprises important eukaryotic parasites that invade host tissues and cells using a unique mechanism of gliding motility. Gliding is powered by actomyosin motors that translocate host-attached surface adhesins along the parasite cell body. Actin filaments (F-actin) generated by Formin1 play a central role in this critical parasitic activity. However, their subcellular origin, path and ultrastructural arrangement are poorly understood. Here we used cryo-electron tomography to image motile Cryptosporidium parvum sporozoites and reveal the cellular architecture of F-actin at nanometer-scale resolution. We demonstrate that F-actin nucleates at the apically positioned preconoidal rings and is channeled into the pellicular space between the parasite plasma membrane and the inner membrane complex in a conoid extrusion-dependent manner. Within the pellicular space, filaments on the inner membrane complex surface appear to guide the apico-basal flux of F-actin. F-actin concordantly accumulates at the basal end of the parasite. Finally, analyzing a Formin1-depleted Toxoplasma gondii mutant pinpoints the upper preconoidal ring as the conserved nucleation hub for F-actin in Cryptosporidium and Toxoplasma. Together, we provide an ultrastructural model for the life cycle of F-actin for apicomplexan gliding motility.https://doi.org/10.1038/s41467-023-40520-6 |
| spellingShingle | Matthew Martinez Shrawan Kumar Mageswaran Amandine Guérin William David Chen Cameron Parker Thompson Sabine Chavin Dominique Soldati-Favre Boris Striepen Yi-Wei Chang Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography Nature Communications |
| title | Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography |
| title_full | Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography |
| title_fullStr | Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography |
| title_full_unstemmed | Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography |
| title_short | Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography |
| title_sort | origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo electron tomography |
| url | https://doi.org/10.1038/s41467-023-40520-6 |
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