Abstract
Green algae of the Volvocine lineage, spanning from unicellular Chlamydomonas to vastly larger Volvox, are models for the study of the evolution of multicellularity, flagellar dynamics, and developmental processes. Phototactic steering in these organisms occurs without a central nervous system, driven solely by the response of individual cells. All such algae spin about a body-fixed axis as they swim; directional photosensors on each cell thus receive periodic signals when that axis is not aligned with the light. The flagella of Chlamydomonas and Volvox both exhibit an adaptive response to such signals in a manner that allows for accurate phototaxis, but in the former the two flagella have distinct responses, while the thousands of flagella on the surface of spherical Volvox colonies have essentially identical behavior. The planar 16-cell species Gonium pectorale thus presents a conundrum, for its central 4 cells have a Chlamydomonas-like beat that provide propulsion normal to the plane, while its 12 peripheral cells generate rotation around the normal through a Volvox-like beat. Here we combine experiment, theory, and computations to reveal how Gonium, perhaps the simplest differentiated colonial organism, achieves phototaxis. High-resolution cell tracking, particle image velocimetry of flagellar driven flows, and high-speed imaging of flagella on micropipette-held colonies show how, in the context of a recently introduced model for Chlamydomonas phototaxis, an adaptive response of the peripheral cells alone leads to photoreorientation of the entire colony. The analysis also highlights the importance of local variations in flagellar beat dynamics within a given colony, which can lead to enhanced reorientation dynamics.
Highlights
We have presented a detailed study of motility and phototaxis of Gonium pectorale, an organism of intermediate complexity within the Volvocine green algae
In its flagellar dynamics it combines beating patterns found in Chlamydomonas and Volvox and has a distinct symmetry compared to the approximate bilateral symmetry of the former and the axisymmetry of the latter
Our experimental observations are consistent with a theory based on adaptive response exhibited solely by the peripheral cells, on a timescale comparable to the rotation period of the colony around the axis normal to the body plane
Summary
Chlamydomonas, the simplest member of the Volvocine family, swims typically by actuation of its two flagella in a breast stroke, combining propulsion and slow body rotation It possesses an eye spot, a small area highly sensitive to light [14,15], which triggers the two flagella differently [16]. Despite lacking a central nervous system to coordinate its cells, Volvox exhibits accurate phototaxis This is achieved by an adaptive response to changing light levels, with a response time tuned to the colony rotation period which creates a differential. The flagella structure of Gonium reinforces its key position as intermediate in the evolution toward multicellularity and cell differentiation These small flat assemblies show intriguing swimming along helical trajectories—with their body plane almost normal to the swimming direction—that have attracted the attention of naturalists since the 18th century [25,26,30]. That response is shown to be adaptive, and we extend a previously introduced model for such a response to the geometry of Gonium and show how the characteristic relaxation times are finely tuned to the Gonium body shape and rotation rate to perform efficient phototaxis
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