Collective Phototaxis of Chlamydomonas reinhardtii Cells

Abstract

Microorganisms are omnipresent in our life and the environment, such as microbes in the gut, spermatozoa in reproductive organs, algae and protozoa in the aquatic ecosystem, and bacterial colonization and infection. Motility in microorganisms is an essential feature of life that facilitates the search for food, avoidance of possible life-threatening cues, and spatially distributing cells for thriving. Often taxis phenomena wherein microorganisms exhibit directed motion in response to external physio-chemical stimuli or nutrient gradients constitute a coordinated complex movement of a large collection of microorganisms such as phototaxis of phytoplankton in response to light and chemotaxis of bacteria or sperm cells in response to a chemical gradient. Therefore, it is essential to understand the effect and origin of emerging collective behavior in dense suspension and the nature of crossover from an individual cell to the population level.

This thesis presents a comprehensive experimental study of collective behavior in phototaxis of Chlamydomonas reinhardtii (CR) cells, a single-cell biflagellate microswimmer widely considered as model organism. We divide the study of phototaxis into three major parts - (i) steady-state phototactic response of cells (when cells are already oriented towards the light exhibiting directed motion), (ii) Response: transition from random motion of cells to steady-state directed phototactic motion when light is switched on (iii) Recovery: transition from steady-state directed phototactic motion of cells to random motion when light is switched off.

In the first part of the thesis, we describe the steady-state phototactic response of CR cells. We show that at a given light intensity, the phototactic efficiency of CR cells is minimal (even lower than a single isolated cell) at a well-defined threshold cell concentration, above which the efficiency of a large collection of cells can even exceed the efficiency obtainable from a single isolated cell. We demonstrate that the origin of enhancement in phototactic efficiency in collective regime lies in the slowing down cell speed, leading them to better light sensing capabilities. We further show that the steady-state phenomenology observed in this study is well captured by modeling the phototactic response as an active Brownian particle subject to density-dependent external aligning torque.

In the second part, we discuss the kinetics of phototactic reorientation during - (i) Response and (ii) Recovery. Due to the single eyespot in unicellular microorganisms, navigation to the light source in a three-dimensional world entails a specific control mechanism. The mechanism consists of detecting light direction by comparing light intensity while moving on a helical path and then translating that information to motility apparatus such as flagella which consequently turns the microorganism towards the light source. We show that the response kinetics, i.e., dynamics of photo turn of a population of CR cells, depends on the cell concentration and light intensity. The response time is faster and independent of stimulus light intensity at low cell concentrations. In contrast, at high cell concentrations, the response is slower and depends non-monotonically on the light intensity. We show that such effects on the response kinetics originate from the coupling between swim speed and received photon flux.

Further, in the second part, we present the results on the recovery (orientational diffusion) of cells that have already achieved a steady state phototactic motion. The kinetics of orientational recovery of oriented cell population reveals a characteristic time independent of their cell concentration and light intensity. Finally, we extend our model of active Brownian particle subject to aligning torque to capture the time-dependent reorientation process.

These results demonstrate that cell populations modulate fundamental quantities such as phototactic efficiency and response time. Coupling between collective effects and external physio-chemical stimuli results in complex modulation of single-cell behavior in the dense suspension. We have elucidated a simple physical and phenomenological mechanism governing such complex collective behavior.