Phototaxis of Chlamydomonas arises from a tuned adaptive photoresponse shared with multicellular Volvocine green algae

Abstract

A fundamental issue in biology is the nature of evolutionary transitions from unicellular to multicellular organisms. Volvocine algae are models for this transition, as they span from the unicellular biflagellate Chlamydomonas to multicellular species of Volvox with up to 50,000 Chlamydomonas -like cells on the surface of a spherical extracellular matrix. The mechanism of phototaxis in these species is of particular interest since they lack a nervous system and intercellular connections; steering is a consequence of the response of individual cells to light. Studies of Volvox and Gonium , a 16-cell organism with a plate-like structure, have shown that the flagellar response to changing illumination of the cellular photosensor is adaptive, with a recovery time tuned to the rotation period of the colony around its primary axis. Here, combining high-resolution studies of the flagellar photoresponse of micropipette-held Chlamydomonas with 3D tracking of freely swimming cells, we show that such tuning also underlies its phototaxis. A mathematical model is developed based on the rotations around an axis perpendicular to the flagellar beat plane that occur through the adaptive response to oscillating light levels as the organism spins. Exploiting a separation of timescales between the flagellar photoresponse and phototurning, we develop an equation of motion that accurately describes the observed photoalignment. In showing that the adaptive timescales in Volvocine algae are tuned to the organisms’ rotational periods across three orders of magnitude in cell number, our results suggest a unified picture of phototaxis in green algae in which the asymmetry in torques that produce phototurns arise from the individual flagella of Chlamydomonas , the flagellated edges of Gonium , and the flagellated hemispheres of Volvox .

Flagellar beat state switching in microswimmers to select between positive and negative phototaxis

“…To experimentally test the delay mechanism (Fig. 3c), we used micropipette aspiration [16] to fix E. gracilis cells in place (Fig. 5a) and measure the response of flagellar beat pattern upon changes in light intensity.…”

“…Furthermore, during negative phototaxis under highest light intensity the photosensory organ might be protected against photodamage (and also be more sensitive) by being shaded from the whole cell body, while during positive phototaxis the sensor points mostly towards the light source and would thereby be able to capture more of the scarce photons that would be adsorbed by the cell body otherwise. This design rule might be extensible to other phototactic cells such as Chlamydomonas [14, 16].…”

“…To experimentally test the delay mechanism (Fig. 3c), we used micropipette aspiration [16] to fix E.…”

“…Natural microswimmers perform versatile feedback control strategies by selecting cell motility behaviors in response to environmental stimuli [1][2][3][4][5][6][7][8][9][10][11]: Bacteria alternate between running and tumbling states to navigate chemical gradients [3][4][5][6]. Chlamydomonas reinhardtii coordinate their cis and trans flagellum to transition between positive and negative phototaxis [12][13][14][15][16]. Volvox carteri control their positive and negative phototaxis by accelerating or ceasing their anterior flagella [17,18].…”

Short-term memory effects in the phototactic behavior of microalgae

“…38 A more physical model of phototaxis was recently introduced by Leptos et al to describe the response of C. reinhardtii to light. 39 In their model, Leptos et al took into account the rotation of the microalga around its axis, while swimming, and the resulting oscillating light intensity seen by the eyespot. The consecutive step-up and step-down stimuli sensed by the eyespot during one body rotation lead to a realignment of the trajectory towards the light source.…”