Trypanosome Motion Represents an Adaptation to the Crowded Environment of the Vertebrate Bloodstream

PLoS Pathogens

Timothy Krüger¹  Erik Stellamanns¹  Niko Heddergott¹  Markus Engstler²  Sujin B. Babu³  Sravanti Uppaluri⁴  Holger Stark⁴  Thomas Pfohl⁴  Ai Wei⁵ 

[1] Department of Cell and Developmental Biology, Biocenter, University of Würzburg, Würzburg, Germany;Department of Chemistry, University of Basel, Basel, Switzerland;Institute of Theoretical Physics, Technische Universität Berlin, Berlin, Germany;Max-Planck-Institute for Dynamics and Self-Organization, Göttingen, Germany;Physics Department, Malaviya National Institute of Technology Jaipur, JLN Marg, Jaipur, Rajasthan, India

关键词: Trypanosoma;    Swimming;    Flagella;    Flagellar rotation;    Blood;    Viscosity;    Fluorescence imaging;    Cell motility;   

DOI  :  10.1371/journal.ppat.1003023

学科分类：生物科学（综合）

来源: Public Library of Science

【 摘 要 】

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.

【 授权许可】

CC BY