Hopping trajectories due to long-range interactions determine surface accumulation of microalgae

Abstract

The accumulation of motile cells at solid interfaces increases the rate of surface encounters and the likelihood of surface attachment, leading to surface colonization and biofilm formation. The cell density distribution in the vicinity of a physical boundary is influenced by the interactions between the microswimmers and their physical environment, including hydrodynamic and steric interactions, as well as by stochastic effects. Disentangling the contributions of these effects remains an experimental challenge. Here, we use a custom-made four-camera view microscope to track a population of motile puller-type Chlamydomonas reinhardtii in a relatively unconstrained three-dimensional (3D) domain. Our experiments yield an extensive sample of 3D trajectories including cell-surface encounters with a planar wall, from which we extract a full description of the dynamics and the stochasticity of swimming cells. We use this large data sample and combine it with Monte Carlo simulations to determine the link between the dynamics at the single-cell level and the cell density. Our experiments demonstrate that the near-wall scattering is bimodal, corresponding to steric and hydrodynamic effects. We find, however, that this near-wall dynamics has little influence on the cell accumulation at the surface. On the other hand, we present evidence of a cell-induced surface-directed rotation leading to a vertical orbiting behavior and hopping trajectories, consistent with long-range hydrodynamic effects. We identify this long-range effect to be at the origin of the significant surface accumulation of cells.

Sharp turns and gyrotaxis modulate surface accumulation of microorganisms

“…We have experimentally found, as others have (18,23,30), that there is accumulation of swimming cells (here, H. akashiwo) near plane boundaries, both vertical and horizontal. We have found that the trajectories of swimming cells and the probability of a cell undergoing a sharp turn are significantly influenced by the proximity of a wall.…”

“…The orientational response to the gravity-viscous torque balance is known as gyrotaxis (21). The third is contact with the wall by the cell body or its propulsive organelles (cilia or flagella) (22,23). In this case, accumulation is attributed to the preferential surface scattering (24,25) and sliding (18,26) caused by collisions with the surface (17).…”

“…In ref. 23, measurements were reported of the threedimensional trajectories of microswimmers near the top and bottom rigid walls of a chamber containing a dilute suspension of C. reinhardtii. The authors examined many trajectories within 30 μm of the wall and found that cells that approached the wall at shallow angles (less than about 20 • ) tended to reflect smoothly from the wall at approximately the same angle and speed, exhibiting a relatively weak wall repulsion, consistent with the hydrodynamic theory of ref.…”

Swimming in Complex Fluids

“…Hydrodynamic effects can be substantial, metallic synthetic swimmers can even swim upwards against gravity using the hydrodynamic interaction with a wall (Figure 7d) (103). Surface accumulation may also be a statement of mean behavior, with individual swimmers undergoing periodic departure and return (108,119).…”

Characterization of the RpoN regulon reveals the regulation of motility, T6SS2 and metabolism in Vibrio parahaemolyticus

“…Loss of rpoN enhances the colonization of V. parahaemolyticus in part due to the decrease of motility in the ΔrpoN strain (Whitaker et al, 2014). Furthermore, bacterial motility plays an essential role in colonization, adhesion, and biofilm formation (Brescia et al, 2020;Khan et al, 2020;Buchner et al, 2021;Mea et al, 2021). V. parahaemolyticus contains dual flagellar systems to adapt to different circumstances: the polar flagellar system was used when growing in liquids and the lateral flagellar system was used when growing on surfaces or in dense environments (McCarter, 2004).…”