Species-Specific Adaptations of Trypanosome Morphology and Motility to the Mammalian Host

Abstract

African trypanosomes thrive in the bloodstream and tissue spaces of a wide range of mammalian hosts. Infections of cattle cause an enormous socio-economic burden in sub-Saharan Africa. A hallmark of the trypanosome lifestyle is the flagellate’s incessant motion. This work details the cell motility behavior of the four livestock-parasites Trypanosoma vivax, T. brucei, T. evansi and T. congolense. The trypanosomes feature distinct swimming patterns, speeds and flagellar wave frequencies, although the basic mechanism of flagellar propulsion is conserved, as is shown by extended single flagellar beat analyses. Three-dimensional analyses of the trypanosomes expose a high degree of dynamic pleomorphism, typified by the ‘cellular waveform’. This is a product of the flagellar oscillation, the chirality of the flagellum attachment and the stiffness of the trypanosome cell body. The waveforms are characteristic for each trypanosome species and are influenced by changes of the microenvironment, such as differences in viscosity and the presence of confining obstacles. The distinct cellular waveforms may be reflective of the actual anatomical niches the parasites populate within their mammalian host. T. vivax displays waveforms optimally aligned to the topology of the bloodstream, while the two subspecies T. brucei and T. evansi feature distinct cellular waveforms, both additionally adapted to motion in more confined environments such as tissue spaces. T. congolense reveals a small and stiff waveform, which makes these parasites weak swimmers and destined for cell adherence in low flow areas of the circulation. Thus, our experiments show that the differential dissemination and annidation of trypanosomes in their mammalian hosts may depend on the distinct swimming capabilities of the parasites.

Author Summary

African trypanosomes are protist flagellates that are successful parasites in a wide spectrum of hosts. These include humans, where they cause the deadly sleeping sickness, and livestock, where they cause nagana. Nagana has a tremendous negative impact in wide regions of sub-Saharan Africa. The motility of these parasites has been shown to be essential for their survival in all the different environments they inhabit, from the bloodstream of mammals to the gut of the tsetse fly vector. The complex swimming mechanism of trypanosomes has only recently been elucidated in detail, using Trypanosoma brucei cells that have been in long term culture. We aimed to characterise and compare the swimming behaviour of several important livestock-infective trypanosome species, isolated directly from the bloodstream. This was done using state of the art microscopy, allowing measurement of their motility with high spatiotemporal resolution. While showing that the basic flagellar propulsion mechanism is the same in all species, we related the trypanosomes motility to their characteristic morphology. We quantified distinct behaviours in the analysed species, which could specifically be manipulated by experimental variations in the physical environment. Importantly, we show that the trypanosome’s morphology and swimming performance could determine the anatomical niche the parasite populates in the host. This would allow differential dissemination of distinct trypanosome species in the mixed infections, which are frequently observed in the wild.