Intermediate light adaptation induces oscillatory phototaxis switching and pattern formation in Chlamydomonas.

Abstract

Biological microswimmers exhibit intricate taxis behaviors in response to environmental stimuli and swim in complex trajectories to navigate their environment. How microswimmers respond to stimulus instantaneously, and how adaptation to stimulus influences their long-term behavioral changes, remains largely unclear. Here, we report an oscillatory phototaxis observed in Chlamydomonas reinhardtii at intermediate light intensities, where cells swim back-and-forth under a constant, unidirectional light stimulus due to alternation between positive and negative phototaxis. The phototaxis switching can be captured by the change in phase relationship between eyespot and helical swimming. Oscillatory phototaxis of individual cells leads to a global pattern of millimeter-scale propagating density bands that persists for [Formula: see text]30 min. High-speed imaging and long-time tracking experiments at single-cell level verify a unified phototaxis mechanism that couples light detection, light adaptation, flagella responses, and behavioral switching. By experimentally tracking steady swimming and transient turning states, we verify that phototaxis transition is achieved via the modulation of flagella waveforms and flagella phase difference, which can be captured by a hydrodynamic model accounting for photoresponses. Adaptation acts effectively as an oscillator damper to mediate multipurpose tasking across multiple system levels (subcellular flagella beats, oscillatory phototaxis, colonial pattern formation) and timescales (from milliseconds to over 30 min). This adaptive phototaxis mechanism provides a comprehensive understanding of how microswimmers achieve complex behavioral changes across multiple temporal scales with a single sensor-actuator circuit featuring relatively simple adaptive feedback responses.