Date Published: February 12, 2016
Publisher: Public Library of Science
Author(s): Joel L. Bargul, Jamin Jung, Francis A. McOdimba, Collins O. Omogo, Vincent O. Adung’a, Timothy Krüger, Daniel K. Masiga, Markus Engstler, Mark Carrington.
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.
Trypanosomes are extracellular parasites with an exceptionally broad host range . These flagellates thrive in all vertebrate classes and cause severe diseases in man and livestock. Human African trypanosomiasis (HAT), commonly known as sleeping sickness, is a devastating neglected disease of poverty, and trypanosome infestations of livestock cause additional massive economic burden in sub-Saharan Africa. The animal African trypanosomiases (AAT) comprise a set of veterinary diseases, of which the cattle sickness nagana and the equine plague surra are the most prominent. Trypanosoma vivax and T. congolense are the nagana pathogens of cattle, but can also cause disease in other mammals, including sheep, goats, pigs, horses, camels and even dogs. Both species have additionally been identified in a wide range of wild animals, including ruminants and suids, but also lions or hyaenas . T. brucei is pathogenic to camels, horses and dogs, but is also prevalent in sheep, goats, cattle and pigs as well as in a wide variety of wildlife species. The broad host range is shared by the human sleeping sickness parasite T. b. rhodesiense in east and southern Africa. T. b. gambiense causes HAT in west and central Africa and has been reported only in pigs and some wildlife hosts .
African trypanosomes thrive in diverse host environments ranging from tissues and circulation of many vertebrates to the digestive tract of the tsetse fly. Cell motility appears to be crucial for the completion of the trypanosome life cycles in the fly and vertebrate hosts [19,21,33,34], and studies investigating motility-dependent mechanisms, like antibody clearance , have led to efforts to elucidate and quantify the exact mechanism of the complex three-dimensional movement of the cells . The results obtained, in turn, led to the concept of how the physical environment could affect the motility of trypanosomes, with implications for the parasites behaviour in the diverse fluids and tissues of their varied hosts [24,36].