Mechanics of behavior: Comprehensive search behavior encoded in cytoskeletal dynamics of single cell <i>Lacrymaria olor</i>

Complex animal behavior arises from interplay between actuators and sensors. Surprisingly, single eukaryotic cells such as protists are also capable of complex behavior, but how an algorithm such as search might be encoded in intrinsic dynamics of a single cell remains unknown. Here we elucidate the mechanics of search behavior in the predatory ciliate Lacrymaria olor, which has the ability to extend and contract its “neck” seven body lengths in a second while efficiently searching the space around it for prey in minutes. Our recent work establishes that L. olor’s search strategy is encoded in antagonistic active systems: subcellular structures that use surface cilia and the cortical cytoskeleton (Coyle et al, 2019). Here we reveal the underlying geometrical features of the cytoskeleton, and membrane and volume constraints, that together program extension and contraction dynamics of this active filament. Through force spectroscopy and membrane tension experiments in live cells, we reveal the role of this dynamic force landscape and how it shapes the search phase space. Our work combines theoretical active filament models with experimental data to unravel how active mechanics leads to emergent behavior in single cells.