Sharp turns and gyrotaxis modulate surface accumulation of microorganisms.

The accumulation of swimming microorganisms at surfaces is an essential feature of various physical, chemical, and biological processes in confined spaces. To date, this accumulation is mainly assumed to depend on the change of swimming speed and angular velocity caused by cell-wall contact and hydrodynamic interaction. Here, we measured the swimming trajectories of Heterosigma akashiwo (a biflagellate marine alga) near vertical and horizontal rigid boundaries. We observed that the probability of sharp turns is greatly increased near a vertical wall, resulting in significant changes in the distributions of average swimming speed, angular velocity, and rotational diffusivity near the wall (a quantity that has not previously been investigated) as functions of both distance from the wall and swimming orientation. These cannot be satisfactorily explained by standard hydrodynamic models. Detailed examination of an individual cell trajectory shows that wall contact by the leading flagellum triggers complex changes in the behavior of both flagella that cannot be incorporated in a mechanistic model. Our individual-based model for predicting cell concentration using the measured distributions of swimming speed, angular velocity, and rotational diffusivity agrees well with the experiment. The experiments and model are repeated for a cell suspension in a vertical plane, bounded above by a horizontal wall. The cell accumulation beneath the wall, expected from gyrotaxis, is considerably amplified by cell-wall interaction. These findings may shed light on the prediction and control of cell distribution mediated by gyrotaxis and cell-wall contact.

Hydrodynamic synchronization and metachronal waves on the surface of the colonial alga Volvox carteri.

From unicellular ciliates to the respiratory epithelium, carpets of cilia display metachronal waves, long-wavelength phase modulations of the beating cycles, which theory suggests may arise from hydrodynamic coupling. Experiments have been limited by a lack of organisms suitable for systematic study of flagella and the flows they create. Using time-resolved particle image velocimetry, we report the discovery of metachronal waves on the surface of the colonial alga Volvox carteri, whose large size and ease of visualization make it an ideal model organism for these studies. An elastohydrodynamic model of weakly coupled compliant oscillators, recast as interacting phase oscillators, reveals that orbit compliance can produce fast, robust synchronization in a manner essentially independent of boundary conditions, and offers an intuitive understanding of a possible mechanism leading to the emergence of metachronal waves.

Metachronal waves in the flagellar beating of Volvox and their hydrodynamic origin.

Groups of eukaryotic cilia and flagella are capable of coordinating their beating over large scales, routinely exhibiting collective dynamics in the form of metachronal waves. The origin of this behavior--possibly influenced by both mechanical interactions and direct biological regulation--is poorly understood, in large part due to a lack of quantitative experimental studies. Here we characterize in detail flagellar coordination on the surface of the multicellular alga Volvox carteri, an emerging model organism for flagellar dynamics. Our studies reveal for the first time that the average metachronal coordination observed is punctuated by periodic phase defects during which synchrony is partial and limited to specific groups of cells. A minimal model of hydrodynamically coupled oscillators can reproduce semi-quantitatively the characteristics of the average metachronal dynamics, and the emergence of defects. We systematically study the model's behaviour by assessing the effect of changing intrinsic rotor characteristics, including oscillator stiffness and the nature of their internal driving force, as well as their geometric properties and spatial arrangement. Our results suggest that metachronal coordination follows from deformations in the oscillators' limit cycles induced by hydrodynamic stresses, and that defects result from sufficiently steep local biases in the oscillators' intrinsic frequencies. Additionally, we find that random variations in the intrinsic rotor frequencies increase the robustness of the average properties of the emergent metachronal waves.

Dancing volvox: hydrodynamic bound states of swimming algae.

The spherical alga Volvox swims by means of flagella on thousands of surface somatic cells. This geometry and its large size make it a model organism for studying the fluid dynamics of multicellularity. Remarkably, when two nearby Volvox colonies swim close to a solid surface, they attract one another and can form stable bound states in which they "waltz" or "minuet" around each other. A surface-mediated hydrodynamic attraction combined with lubrication forces between spinning, bottom-heavy Volvox explains the formation, stability, and dynamics of the bound states. These phenomena are suggested to underlie observed clustering of Volvox at surfaces.