The highly motile and versatile protozoan pathogen Trypanosoma
brucei undergoes a complex life cycle in the tsetse fly. Here we
introduce the host insect as an expedient model environment for microswimmer
research, as it allows examination of microbial motion within a diversified, secluded
and yet microscopically tractable space. During their week-long journey through the
different microenvironments of the fly´s interior organs, the incessantly swimming
trypanosomes cross various barriers and confined surroundings, with concurrently
occurring major changes of parasite cell architecture. Multicolour light sheet
fluorescence microscopy provided information about tsetse tissue topology with
unprecedented resolution and allowed the first 3D analysis of the infection process.
High-speed fluorescence microscopy illuminated the versatile behaviour of trypanosome
developmental stages, ranging from solitary motion and near-wall swimming to
collective motility in synchronised swarms and in confinement. We correlate the
microenvironments and trypanosome morphologies to high-speed motility data, which
paves the way for cross-disciplinary microswimmer research in a naturally evolved
environment.DOI:
http://dx.doi.org/10.7554/eLife.27656.001
Trypanosoma vivax is the most prevalent trypanosome species in African cattle. It is thought to be transmitted by tsetse flies after cyclical development restricted to the vector mouthparts. Here, we investigated the kinetics of T. vivax development in Glossina morsitans morsitans by serial dissections over 1 week to reveal differentiation and proliferation stages. After 3 days, stable numbers of attached epimastigotes were seen proliferating by symmetric division in the cibarium and proboscis, consistent with colonization and maintenance of a parasite population for the remaining lifespan of the tsetse fly. Strikingly, some asymmetrically dividing cells were also observed in proportions compatible with a continuous production of pre- metacyclic trypomastigotes. The involvement of this asymmetric division in T. vivax metacyclogenesis is discussed and compared to other trypanosomatids.
African trypanosomes cause sleeping sickness in humans and nagana in cattle. These unicellular parasites are transmitted by the bloodsucking tsetse fly. In the mammalian host's circulation, proliferating slender stage cells differentiate into cell cycle-arrested stumpy stage cells when they reach high population densities. This stage transition is thought to fulfil two main functions: first, it auto-regulates the parasite load in the host; second, the stumpy stage is regarded as the only stage capable of successful vector transmission. Here, we show that proliferating slender stage trypanosomes express the mRNA and protein of a known stumpy stage marker, complete the complex life cycle in the fly as successfully as the stumpy stage, and require only a single parasite for productive infection. These findings suggest a reassessment of the traditional view of the trypanosome life cycle. They may also provide a solution to a long-lasting paradox, namely the successful transmission of parasites in chronic infections, despite low parasitemia.
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