Flagellar beat state switching in microswimmers to select between positive and negative phototaxis

Microorganisms have evolved various sensor-actuator circuits to respond to environmental stimuli. However, how a given circuit can select efficiently between positive vs. negative taxis under desired vs. undesired stimuli is poorly understood. Here, we investigate how the cellular mechanism by which the chiral microswimmer Euglena gracilis can select between positive vs. negative phototaxis under low vs. high light intensity conditions, respectively. We propose three general selection mechanisms for microswimmer phototaxis. A generic biophysical model demonstrates the effectiveness of all mechanisms, but which varies for each depending on specific conditions. Experiments reveal that only a ‘photoresponse in-version’ mechanism is compatible with E. gracilis phototaxis. Specifically, a light-intensity dependent transition on the sub-second time scale between two flagellar beat states responsible for forward swimming vs. sideway turning ultimately generates positive phototaxis at low light intensity via a run-and-tumble strategy and negative phototaxis at high light intensity via a helical klinotaxis strategy. More generally, a picture emerges where a variety of E. gracilis behaviors over a wide range of light intensities as reported in the literature can be explained by the coordinated switching between just these two flagellar beating states over time. These results provide design principles for simple two-state switching mechanisms in natural and synthetic microswimmers to operate under both noisy and saturated stimulus conditions. LAY ABSTRACT Our experimental and theoretical results explain how the single cell Euglena gracilis achieves both positive and negative phototaxis. Our insights are then able to synthesise a larger number of previously described observations on E. gracilis photoresponses and photobehaviors due to a concise two-state model of flagellar beating. These insight will likely inform the behaviors of other natural microswimmers as well as the design of synthetic ones.