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.

Highlights

  • Microswimmers have intrigued the scientific mind since the very first observations of bacteria, protists and spermatozoa (Dobell, 1932)

  • As we show in this work, the systems motile occupants exhibit all kinds of behaviour posing prevailing questions in microswimmer research on the one hand, and having possible implications for the cell and developmental biology of the parasites on the other hand

  • In order to make the trypanosome-tsetse system experimentally accessible, we first detailed the in vivo boundary conditions that could influence the motile behaviour of the different developmental stages of T. brucei within the tsetse alimentary tract

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Summary

Introduction

Microswimmers have intrigued the scientific mind since the very first observations of bacteria, protists and spermatozoa (Dobell, 1932). More than 300 years ago, Leeuwenhoek observed free swimming organisms, and studiedanimalculesfrom animal and human environments, especially the fate of spermatozoa in the female genital tract (Leeuwenhoek, 1685). The significance of the physical properties of the female genital tract for sperm motility and internal fertilisation success has been recognised (Fauci and Dillon, 2006; Kirkman-Brown and Smith, 2011), but this system naturally remains challenging for in vivo analysis. Another major microswimmer model is E. coli. There is great interest in the collective behaviour of prokaryotes and the implications of real life surroundings, as cells seldom stay alone or move without encountering

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