Bioelectric control of locomotor gaits in the walking ciliate Euplotes

Abstract

Diverse animal species exhibit highly stereotyped behavioral actions and locomotor sequences as they explore their natural environments. In many such cases, the neural basis of behavior is well established, where dedicated neural circuitry contributes to the initiation and regulation of certain response sequences. At the microscopic scale, single-celled eukaryotes (protists) also exhibit remarkably complex behaviors and yet are completely devoid of nervous systems. Here, to address the question of how single cells control behavior, we study locomotor patterning in the exemplary hypotrich ciliate Euplotes, a highly polarized cell, which actuates a large number of leg-like appendages called cirri (each a bundle of ∼25-50 cilia) to swim in fluids or walk on surfaces. As it navigates its surroundings, a walking Euplotes cell is routinely observed to perform side-stepping reactions, one of the most sophisticated maneuvers ever observed in a single-celled organism. These are spontaneous and stereotyped reorientation events involving a transient and fast backward motion followed by a turn. Combining high-speed imaging with simultaneous time-resolved electrophysiological recordings, we show that this complex coordinated motion sequence is tightly regulated by rapid membrane depolarization events, which orchestrate the activity of different cirri on the cell. Using machine learning and computer vision methods, we map detailed measurements of cirri dynamics to the cell's membrane bioelectrical activity, revealing a differential response in the front and back cirri. We integrate these measurements with a minimal model to understand how Euplotes-a unicellular organism-manipulates its membrane potential to achieve real-time control over its motor apparatus.