Adaptive phototaxis ofChlamydomonasand the evolutionary transition to multicellularity in Volvocine green algae

Abstract

AbstractA 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 biflagellateChlamydomonasto multicellular species ofVolvoxwith up to 50,000Chlamydomonas-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 ofVolvoxandGonium, 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 with 3D tracking of freely-swimming cells, we show that such tuning also underlies phototaxis ofChlamydomonas. 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 time scales between the flagellar photoresponse and phototurning, we develop an equation of motion that accurately describes the observed photoalignment. In showing that the adaptive time scale is tuned to the organisms’ rotational period 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 ofChlamydomonas, the flagellated edges ofGoniumand the flagellated hemispheres ofVolvox.