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Abstract:
Blood is a remarkable habitat: it is highly viscous, contains a dense packaging of cells and perpetually flows at velocities
varying over three orders of magnitude. Only few pathogens endure the harsh physical conditions within the vertebrate
bloodstream and prosper despite being constantly attacked by host antibodies. African trypanosomes are strictly
extracellular blood parasites, which evade the immune response through a system of antigenic variation and incessant
motility. How the flagellates actually swim in blood remains to be elucidated. Here, we show that the mode and dynamics of
trypanosome locomotion are a trait of life within a crowded environment. Using high-speed fluorescence microscopy and
ordered micro-pillar arrays we show that the parasites mode of motility is adapted to the density of cells in blood.
Trypanosomes are pulled forward by the planar beat of the single flagellum. Hydrodynamic flow across the asymmetrically
shaped cell body translates into its rotational movement. Importantly, the presence of particles with the shape, size and
spacing of blood cells is required and sufficient for trypanosomes to reach maximum forward velocity. If the density of
obstacles, however, is further increased to resemble collagen networks or tissue spaces, the parasites reverse their flagellar
beat and consequently swim backwards, in this way avoiding getting trapped. In the absence of obstacles, this flagellar beat
reversal occurs randomly resulting in irregular waveforms and apparent cell tumbling. Thus, the swimming behavior of
trypanosomes is a surprising example of micro-adaptation to life at low Reynolds numbers. For a precise physical
interpretation, we compare our high-resolution microscopic data to results from a simulation technique that combines the
method of multi-particle collision dynamics with a triangulated surface model. The simulation produces a rotating cell body
and a helical swimming path, providing a functioning simulation method for a microorganism with a complex swimming
strategy.
