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Emergent Actin Flows Explain Diverse Parasite Gliding Modes

View ORCID ProfileChristina L. Hueschen, View ORCID ProfileLi-av Segev Zarko, View ORCID ProfileJian-Hua Chen, Mark A. LeGros, View ORCID ProfileCarolyn A. Larabell, View ORCID ProfileJohn C. Boothroyd, View ORCID ProfileRob Phillips, View ORCID ProfileAlexander R. Dunn
doi: https://doi.org/10.1101/2022.06.08.495399
Christina L. Hueschen
1Dept. of Chemical Engineering, Stanford University, Palo Alto, CA
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  • For correspondence: chueschen@gmail.com alex.dunn@stanford.edu
Li-av Segev Zarko
2Dept. of Microbiology and Immunology, Stanford University, Palo Alto, CA
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Jian-Hua Chen
3Dept. of Anatomy, University of California San Francisco, San Francisco, CA
4National Center for X-ray Tomography, Lawrence Berkeley National Laboratory, Berkeley, CA
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Mark A. LeGros
3Dept. of Anatomy, University of California San Francisco, San Francisco, CA
4National Center for X-ray Tomography, Lawrence Berkeley National Laboratory, Berkeley, CA
5Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA
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Carolyn A. Larabell
3Dept. of Anatomy, University of California San Francisco, San Francisco, CA
4National Center for X-ray Tomography, Lawrence Berkeley National Laboratory, Berkeley, CA
5Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA
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John C. Boothroyd
2Dept. of Microbiology and Immunology, Stanford University, Palo Alto, CA
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Rob Phillips
6Dept. of Physics, California Institute of Technology, Pasadena, CA
7Div. of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA
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Alexander R. Dunn
1Dept. of Chemical Engineering, Stanford University, Palo Alto, CA
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  • ORCID record for Alexander R. Dunn
  • For correspondence: chueschen@gmail.com alex.dunn@stanford.edu
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Summary

During host infection, single-celled apicomplexan parasites like Plasmodium and Toxoplasma use a motility mechanism called gliding, which differs fundamentally from other known mechanisms of eukaryotic cell motility. Gliding is thought to be powered by a thin layer of flowing filamentous (F)-actin1– 3 sandwiched between the plasma membrane and a myosin-coated4,5 inner membrane complex. How this surface actin layer drives the diverse apicomplexan gliding modes observed experimentally - helical, circular, and twirling6,7, and patch8, pendulum9, or rolling2 – presents a rich biophysical puzzle. Here, we use single-molecule imaging to track individual actin filaments and myosin complexes in live Toxoplasma gondii. Based on these data, we hypothesize that F-actin flows arise by self-organization, rather than following a microtubule-based template as previously believed. We develop a continuum model of emergent F-actin flow within the unusual confines provided by parasite geometry. In the presence of F-actin turnover, our model predicts the emergence of a steady-state mode in which actin transport is largely rearward. Removing actin turnover leads to actin patches that recirculate up and down the cell, a “cyclosis” that we observe experimentally for drug-stabilized actin bundles in live parasites. These findings provide a mechanism by which actin turnover governs a transition between distinct self-organized F-actin states, whose properties can account for the diverse gliding modes known to occur. More broadly, we illustrate how different forms of gliding motility can emerge as an intrinsic consequence of the self-organizing properties of F-actin flow in a confined geometry.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 09, 2022.
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Emergent Actin Flows Explain Diverse Parasite Gliding Modes
Christina L. Hueschen, Li-av Segev Zarko, Jian-Hua Chen, Mark A. LeGros, Carolyn A. Larabell, John C. Boothroyd, Rob Phillips, Alexander R. Dunn
bioRxiv 2022.06.08.495399; doi: https://doi.org/10.1101/2022.06.08.495399
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Emergent Actin Flows Explain Diverse Parasite Gliding Modes
Christina L. Hueschen, Li-av Segev Zarko, Jian-Hua Chen, Mark A. LeGros, Carolyn A. Larabell, John C. Boothroyd, Rob Phillips, Alexander R. Dunn
bioRxiv 2022.06.08.495399; doi: https://doi.org/10.1101/2022.06.08.495399

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