Light-dependent switching between two flagellar beating states selects versatile phototaxis strategies in microswimmers

Microorganisms have evolved sophisticated sensor-actuator circuits to perform taxis in response to various environmental stimuli. How any given circuit can select between different taxis responses in noisy vs. saturated stimuli conditions is unclear. Here, we investigate how Euglena gracilis can select between positive vs. negative phototaxis under low vs. high light intensities, respectively. We propose three general selection mechanisms for phototactic microswimmers, and biophysical modeling demonstrates their effectiveness. Perturbation and high-speed imaging experiments show that of these three mechanisms, the “photoresponse inversion mechanism” is implemented in E. gracilis: a fast, light-intensity-dependent switching between two flagellar beat states responsible for swimming and turning causes positive vs. negative phototaxis at low vs. high light intensity via run-and-tumble vs. helical klinotaxis strategies, respectively. This coordinated beat-switching mechanism then also accounts for a larger set of previously reported E. gracilis behaviors; furthermore, it suggests key design principles for other natural as well as synthetic microswimmers.