Fidelity of adaptive phototaxis

Abstract

Along the evolutionary path from single cells to multicellular organisms with a central nervous system are species of intermediate complexity that move in ways suggesting high-level coordination, yet have none. Instead, organisms of this type possess many autonomous cells endowed with programs that have evolved to achieve concerted responses to environmental stimuli. Here experiment and theory are used to develop a quantitative understanding of how cells of such organisms coordinate to achieve phototaxis, by using the colonial alga Volvox carteri as a model. It is shown that the surface somatic cells act as individuals but are orchestrated by their relative position in the spherical extracellular matrix and their common photoresponse function to achieve colony-level coordination. Analysis of models that range from the minimal to the biologically faithful shows that, because the flagellar beating displays an adaptive down-regulation in response to light, the colony needs to spin around its swimming direction and that the response kinetics and natural spinning frequency of the colony appear to be mutually tuned to give the maximum photoresponse. These models further predict that the phototactic ability decreases dramatically when the colony does not spin at its natural frequency, a result confirmed by phototaxis assays in which colony rotation was slowed by increasing the fluid viscosity.adaptation | evolution | flagella | fluid dynamics | multicellularity

Batchelor Prize Lecture Fluid dynamics at the scale of the cell

“…For sure the Stokeslet field, falling off as 1/r, should dominate sufficiently far from the organism, but the lack of precise uniformity of the surface somatic cell density and the presence of the colony surface itself should induce contributions that would be appreciable at small separations. This led to an investigation (Drescher et al 2010b) of the flow field around freely swimming colonies. For Volvox, the experimental set-up consisted of a chamber with a dilute suspension of colonies and fluorescent microspheres, illuminated with a laser light sheet and observed from the side by a lightweight CCD camera on a long-working-distance microscope.…”

“…This provides ex post facto justification for the use of Squires' result for the lateral advection of Stokeslets in explaining the infalling trajectories of colonies forming a hydrodynamic bound state. Measurements of the flow fields around individual freely swimming cells were then extended to the case of bacteria using a different method (Drescher et al 2010b(Drescher et al , 2011. Here, rather than using a tracking microscope, we adopted a fixed (horizontal) field of view on an inverted microscope, with a typically narrow focal plane width, and monitored swimming cells and advected tracer particles.…”

“…The answer to the latter question turns out to involve phototaxis, directed movement toward light. Detailed study (Drescher, Goldstein & Tuval 2010b) shows that there is a rather precise tuning of the organism's rotational period and the internal relaxation time of the flagellar response to the periodic illumination by light of a directional photosensor on the cell body. As these organisms do not have a central nervous system, this tuning turns out to be a mechanism to achieve organism-scale synchrony of otherwise autonomous units.…”

A steering mechanism for phototaxis in Chlamydomonas

“…Drescher et al [28] developed a model to study phototaxis in Volvox carteri, a colonial alga with thousands of cells like Chlamydomonas on the surface of a spherical extracellular matrix. Each individual cell responds to a step-up in light by decreasing its flagellar activity, then after some time adapting to its baseline.…”

Swimming like algae: biomimetic soft artificial cilia

“…While micro-organisms use cilia to swim through fluids [1], higher organisms use cilia to control internal fluid motion, for example to transport mucus within the bronchial system [2]. Multicellular organisms often use many closely packed cilia that synchronize to collectively achieve a muchenhanced fluid motion [3], or to achieve organism-level coordination that is robust to the failure of individual cilia [4]. Cilia are usually between 1 and 20 mm long and move fluids by an asymmetric beating cycle that is efficient in very viscous environments.…”