Emergent actin flows explain distinct modes of gliding motility

Christina L Hueschen; Li-Av Segev-Zarko; Jian-Hua Chen; Mark A LeGros; Carolyn A Larabell; John C Boothroyd; Rob Phillips; Alexander R Dunn

doi:10.1038/s41567-024-02652-4

Emergent actin flows explain distinct modes of gliding motility

Nat Phys. 2024;20(12):1989-1996. doi: 10.1038/s41567-024-02652-4. Epub 2024 Oct 8.

Authors

Christina L Hueschen^{1

2}, Li-Av Segev-Zarko³, Jian-Hua Chen^{4

5}, Mark A LeGros^{4

5

6}, Carolyn A Larabell^{4

5

6}, John C Boothroyd³, Rob Phillips^{7

8}, Alexander R Dunn¹

Affiliations

¹ Dept. of Chemical Engineering, Stanford University, Palo Alto, CA USA.
² Present Address: Dept. of Cell and Developmental Biology, University of California San Diego, La Jolla, CA USA.
³ Dept. of Microbiology and Immunology, Stanford University, Palo Alto, CA USA.
⁴ Dept. of Anatomy, University of California San Francisco, San Francisco, CA USA.
⁵ National Center for X-ray Tomography, Lawrence Berkeley National Laboratory, Berkeley, CA USA.
⁶ Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA USA.
⁷ Dept. of Physics, California Institute of Technology, Pasadena, CA USA.
⁸ Div. of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA USA.

Abstract

During host infection, Toxoplasma gondii and related unicellular parasites move using 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)-actin sandwiched between the plasma membrane and a myosin-covered inner membrane complex. How this surface actin layer drives the various gliding modes observed in experiments-helical, circular, twirling and patch, pendulum or rolling-is unclear. Here we suggest that F-actin flows arise through self-organization and develop a continuum model of emergent F-actin flow within the confines provided by Toxoplasma geometry. In the presence of F-actin turnover, our model predicts the emergence of a steady-state mode in which actin transport is largely directed rearward. Removing F-actin turnover leads to actin patches that recirculate up and down the cell, which we observe experimentally for drug-stabilized actin bundles in live Toxoplasma gondii parasites. These distinct self-organized actin states can account for observed gliding modes, illustrating 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.

Keywords: Biological physics; Cellular motility.