Emergent Actin Flows Explain Diverse Parasite Gliding Modes

Abstract

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)–actin sandwiched between the plasma membrane and a myosin–coated inner membrane complex. How this surface actin layer drives the diverse apicomplexan gliding modes observed experimentally – helical, circular, and twirling, and patch, pendulum, or rolling – 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.