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

Trypanosome Motion Represents an Adaptation to the Crowded Environment of the Vertebrate Bloodstream
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DOI:
10.1371/journal.ppat.1003023
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发表时间:
2012-11-01
期刊:
影响因子:
6.7
通讯作者:
Engstler, Markus
Engstler, Markus
中科院分区:
医学1区
文献类型:
--
作者:
Heddergott, Niko;Krueger, Timothy;Engstler, Markus

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血液是一个非凡的栖息地:它是高粘性的,包含细胞的密集包装,并且以超过三个数量级的速度持续流动。只有少数病原体能忍受脊椎动物血液中的恶劣物理条件,尽管不断受到宿主抗体的攻击,但仍能繁荣发展。非洲锥虫是严格意义上的细胞外血液寄生虫,它们通过抗原变异和不断运动的系统逃避免疫反应。鞭毛虫如何在血液中游动仍有待阐明。在这里,我们表明,锥虫运动的模式和动力学是一个拥挤的环境中的生活特征。使用高速荧光显微镜和有序微柱阵列,我们表明,寄生虫的运动模式是适应血液中的细胞密度。锥虫被单个鞭毛的平面搏动向前拉。穿过不对称形状的细胞体的流体动力学流动转化为其旋转运动。重要的是,具有血细胞的形状、大小和间距的颗粒的存在是锥虫达到最大向前速度所必需的并且是足够的。然而,如果障碍物的密度进一步增加到类似于胶原网络或组织空间,寄生虫就会逆转鞭毛的跳动,从而向后游,以这种方式避免被困。在没有障碍物的情况下,这种鞭毛节拍逆转随机发生,导致不规则波形和明显的细胞翻滚。因此,锥虫的游泳行为是低雷诺数下微适应生命的一个令人惊讶的例子。对于一个精确的物理解释,我们比较我们的高分辨率微观数据的模拟技术,结合了多粒子碰撞动力学的方法与三角形表面模型的结果。该模拟产生了旋转的细胞体和螺旋形的游泳路径,为具有复杂游泳策略的微生物提供了功能性的模拟方法。
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.