Short-term Memory Effects in the Phototactic Behavior of Microalgae: Abstract and Introduction

Table of Links

Abstract and Introduction

Methods

Results

Model

Discussion, Acknowledgements and References

Supplementary Material

Abstract

Phototaxis, the directed motion in response to a light stimulus, is crucial for motile microorganisms that rely on photosynthesis, such as the unicellular microalga Chlamydomonas reinhardtii. It is well known that microalgae adapt to ambient light stimuli. On time scales of several dozen minutes, when stimulated long enough, the response of the microalga evolves as if the light intensity were decreasing [Mayer, Nature (1968)]. Here, we show experimentally that microalgae also have a shortterm memory, on the time scale of a couple of minutes, which is the opposite of adaptation. At these short time scales, when stimulated consecutively, the response of C. reinhardtii evolves as if the light intensity were increasing. Our experimental results are rationalized by the introduction of a simplified model of phototaxis. Memory comes from the interplay between an internal biochemical time scale and the time scale of the stimulus; as such, these memory effects are likely to be widespread in phototactic microorganisms.

I. INTRODUCTION

Phototaxis, the directed motion of organisms in response to a light stimulus, is widespread both in prokaryotes and single-cell eukaryotes [1]. One of the cellular models for eukaryotic phototaxis is the microalga Chlamydomonas reinhardtii, which responds to bluegreen light [2, 3]. When light hits the eyespot of the microalga, it induces photocurrents, whose amplitude depend on the light intensity. These photocurrents then induce flagellar currents which change the beating pattern of the flagella, leading to reorientation and eventually phototaxis [3, 4].

At low light intensities, wild-type C. reinhardtii cells swim towards the light, while they swim away from the light at high light intensities. This corresponds to positive and negative phototaxis, respectively [5]. What sets the change in phototactic behavior? The answer to this question is not fully settled [3].

Several biochemical parameters were found to affect the sign of phototaxis of C. reinhardtii, such as the amount of calcium ions in the surrounding medium [6–8], photosynthetic activity of the microalgae [9], the amount of intracellular reactive oxygen species [10], or the phosphorylation of channelrhodopsin-1, one of the photoreceptors of C. reinhardtii [11]. It is also known that the history of the alga plays a role in its phototactic response: like many unicellular organisms [12–14], C. reinhardtii adapt to their environment. A naive cell population, kept in the dark, exhibits negative phototaxis in response to an intense light stimulus; the same cell population, exposed to the same intense light stimulus, undergoes positive phototaxis when it has been previously exposed to light for a couple dozens minutes [15]. This change in phototactic behavior of a population depending on the history of irradiation is consistent with results obtained at the single-cell level by R¨uffer and Nultsch [4], who monitored the change in beating of the two flagella of C. reinhardtii in response to increasing and decreasing light-stimuli. Such a history-dependent change in the phototactic response occurs on long time scales, of the order of a couple dozen minutes.

Here, we show experimentally that the change in phototactic behavior also depends on the recent history of the cell, where the time scale is of the order of a couple minutes. At these short time scales, the algae exhibit a behavior that is the exact opposite of the long-term adaptation: they integrate consecutive signals over time. When subjected to two consecutive, closely spaced identical stimuli, an alga essentially adds up the second stimulus to the first one, and acts as if the second stimulus were of higher intensity than the first one. Such a signal integration has, to the best of our knowledge, never been observed in the phototactic response of microalgae. Our results are rationalized by the introduction of a simplified model of phototaxis. The memory emerges in the model from the interplay between two time scales, the time between successive stimuli and the relaxation time of an inner biochemical process. Since the model is generic, similar short-term memory effects are likely to be widespread in other organisms that experience phototaxis.