Distinct self-organized actin patterns explain diverse parasite gliding modes

Abstract

During host infection, single-celled apicomplexan parasites like Plasmodium and Toxoplasma use a unique form of locomotion called gliding that differs fundamentally from the swim-or-crawl paradigm of eukaryotic cell motility. Gliding is powered by a thin layer of actin and a specialized myosin sandwiched between the plasma membrane and an inner membranous scaffold. How is this actomyosin network organized to generate coherent traction forces, and drive the diverse cell movements observed during gliding? Here, we used single-molecule imaging to track individual actin filaments and myosin complexes in living Toxoplasma gondii. Based on these data, we drew on flocking theory to develop a continuum model of actin self-organization in the unusual confines provided by parasite geometry. Deriving a parameterization-free surface formulation of our governing equations enabled finite element method simulations on detailed reconstructions of the Toxoplasma cell surface. In the presence of rapid actin filament depolymerization, our model predicts the emergence of rearward steady-state actin flows. By contrast, at low depolymerization rates, emergent stable actin patches recirculate up and down the cell in a "cyclosis" that we observed experimentally for drug-stabilized actin bundles in live parasites. These findings indicate that actin turnover governs a transition between distinct self-organized actin states, whose different properties can account for the disparate gliding modes observed experimentally: unidirectional (helical, circular, twirling) and bidirectional (patch, pendulum, rolling). More broadly, our experimental observations and theoretical model illustrate how different forms of gliding motility can emerge as an intrinsic consequence of the self-organizing properties of actin filament flow in a complex confined geometry.

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