Sharp turns and gyrotaxis modulate surface accumulation of microorganisms

Abstract

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.