Developmental adaptations of trypanosome motility to the tsetse fly host environments unravel a multifaceted in vivo microswimmer system

Abstract

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 bruceicolonises the tsetse gut via an immature peritrophic matrix in the proventriculus

“…One clue, however, came from the lengths of individual trypanosomes from inside the (3D-reconstructed) cyst, which were longer than average midgut procyclics (~20μm; see example in Fig. 3f) and so similar in size to mesocyclic proventricular forms [31, 33] (see also Fig. 7).…”

“…8). Alternatively, there is strong evidence for trypanosome CoMo within infected tsetse tissues [31], although this may not be operative during an early proventricular infection. However, both phenomena (SoMo vs .…”

A fine-tuned vector-parasite dialogue in tsetse’s cardia determines peritrophic matrix integrity and trypanosome transmission success

“…We challenged flies with BSF trypanosomes as teneral adults and then administered blood meals containing dsRNA-cs on day 6, 8 and 10 post parasite acquisition. This is the time interval when we expect the parasites colonizing the ES of the midgut to bypass the PM barrier in the cardia to re-enter into the lumen [19, 33, 34]. Control groups similarly received dsRNA targeting green fluorescent protein (dsRNA-gfp).…”

Toolbox for In Vivo Imaging of Host–Parasite Interactions at Multiple Scales

“…In parasitology, uses have included the generation of optically cleared guts from Tsetse flies (vectors of Trypanosoma brucei) [79] (Figure 1c) and optically transparent Anopheles mosquitoes (vectors of Plasmodium) (Figure 1d-1e). Importantly, the use of mesoscopic methods in parasitology has remained scarce, despite their relatively easy implementation and use.…”