Adaptive phototactic behaviors and navigation strategies in Chlamydomonas

Abstract

Swimming microorganisms play fundamental roles in ecosystems, influencing nutrient cycling and energy transfer. To thrive in dynamic environments, these microswimmers have evolved a variety of locomotion and adaptive behaviors. They respond to diverse environmental cues by modulating their motility and navigation strategies across different spatial and temporal scales. Among these stimuli, light serves as a versatile signal, eliciting phototactic responses critical for survival and ecological interactions. Understanding how microorganisms respond to light is fundamental for uncovering their ecological roles and advancing light-responsive artificial microrobots. However, the mechanisms by which microswimmers coordinate individual and colony behaviors and adapt their navigation strategies to light remain poorly understood. This thesis investigates adaptive phototactic behaviors and navigation strategies in the model microorganism Chlamydomonas reinhardtii, focusing on their responses to changing light environments across multiple temporal scales. Chapter 2 presents the discovery of oscillatory phototaxis in Chlamydomonas, where cells swim along oscillatory trajectories under constant unidirectional light, rather than exhibiting typical positive or negative phototaxis. This oscillatory behavior at the single-cell level leads to the emergence of propagating millimeter-scale density bands. High-speed imaging and single-cell tracking reveal a unified phototaxis mechanism integrating light detection, adaptation, flagellar response, and behavioral switching, driven by transitions between two flagellar waveforms and phase modulation of the cis- and trans-flagellum. This phototaxis mechanism resolves longstanding questions regarding the transition between positive and negative phototaxis in Chlamydomonas. Chapter 3 explores the role of adaptation and the formation of density bands at the colony level. Light intensity thresholds for positive and negative phototaxis in Chlamydomonas dynamically vary with adaptation rates, which depend on light intensity and time. Oscillatory phototaxis arises from overlapping thresholds and shifts over time due to adaptation, eventually leading cells to positive phototaxis. The diversity in adaptation rates of individual cells and the change in phototaxis switching rate over time can further lead to long-term colonial pattern formation. Adaptation acts effectively as an oscillator damper to mediate multi-purpose tasking across multiple system levels (subcellular flagella beats, oscillatory phototaxis, colonial pattern formation) and timescales (from milliseconds to over 30 mins). This adaptation-driven mechanism may provide an alternative route to control complex spatiotemporal patterns for active systems. Chapter 4 demonstrates that Chlamydomonas actively modulates both the curvature and handedness of its swimming trajectory in response to orthogonal light stimuli. The cells swim in circles, switching trajectory handedness with light intensity: counterclockwise under low light and clockwise under high light. This switching arises from light-dependent regulation of subcellular flagellar beating, including changes in beat extension, phase, and—most critically—beat plane orientation. Using high-speed imaging and hydrodynamic modeling, we show that beat plane reorientation is essential for Chlamydomonas to swim orthogonal to light and dynamically tune trajectory curvature, enabling transitions between broad exploration and localized searching in structured light fields. Our findings establish beat plane reorientation as a general mechanism for curvature control in microswimmer navigation.