A self-organizing single-cell morphology circuit optimizes Podophrya collini predatory trap structure

Abstract Cellular structure self-organizes through an interplay between internal mechanisms and external cues. In predatory ciliates, structures that capture prey obtain the resources needed for their construction, creating feedback between environmental inputs and morphological outputs. Here, we describe a self-organizing single-cell morphology circuit that adaptively optimizes the predatory trap structure of the suctorian Podophrya collini. These trap structures ensnare large cellular targets using an array of straw-like tentacles that siphon out prey cytoplasm upon contact with their tips. We find that trap architecture scales anisotropically, favoring tentacle number over length, to construct traps that maximize capture probability for the resources on hand. Drug perturbations, transcriptomics, proteomics, and expansion microscopy define distinct molecular and structural requirements that regulate trap structure maintenance and tentacle biogenesis. We integrate these findings into a mathematical model that explains the adaptive scaling of the trap and that makes predictions we confirm experimentally. More broadly, this circuit’s architecture provides a general-purpose control logic for organizing the number and size of sub-cellular structures applicable to other natural and engineered cellular systems. Competing Interest Statement The authors have declared no competing interest.