Trends in Parasitology
Volume 34, Issue 12, December 2018, Pages 1056-1067
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Review
Beyond Blood: African Trypanosomes on the Move

https://doi.org/10.1016/j.pt.2018.08.002Get rights and content

Highlights

The bloodstream may not be the primary habitat for bloodstream trypanosomes.

The interstitial system may serve as a systemic and well-connected trypanosome niche.

The motion pattern of the diverse trypanosome life cycle stages represent adaptations to changing microenvironments.

Little is known about life cycle stages in the brain.

The tsetse fly is a tractable model system for studies on the mechanobiology of host–parasite interactions.

While the African trypanosomes are among the best-studied parasites, almost everything we know about them is based on the brucei group, which includes the human-infective sleeping sickness parasites and the causative agent of the cattle plague nagana. The past decades have seen an ever-more detailed molecular dissection of Trypanosoma brucei, which today is an accepted cell biological model system. Therefore, recent work on some fundamental aspects of trypanosome biology surprises, as we realise that our knowledge about parasite motility and tropism in the changing host microenvironments is far from definitive. In this review, we highlight a few examples of neglected parasitological questions, which may open (or reopen) a new chapter of trypanosome research.

Section snippets

Parasites Are Motile and Manoeuvre to Spread in Their Hosts

Parasites are expert travellers. They explore their environment by swimming or crawling, to infest their habitats once the destination has been reached. At first sight this seems trivial. But do we really know how parasites navigate, and how the life conditions in the rather diverse microenvironments influence their motion? When compared to free-living species, parasites thrive in small worlds. Their host habitats are secluded, largely homeostatic, and thus fairly predictable. Furthermore,

The Trypanosome Swimming Apparatus

The structure of the T. brucei flagellum and its attachment to the cell body have been concisely reviewed 7, 8.

The basic morphological architecture is modified in a series of developmental stage transitions, possibly in order to adapt to specific niches of the host bodies. The dynamic extension of the microtubule corset allows the repositioning of the flagellar pocket with the connected basal body along the anterior–posterior axis. This changes the emergence point of the flagellum and its

The Cellular Waveform Describes the Dynamic Pleomorphism of Trypanosomes

The complex three-dimensional movement of the various trypanosome stages has been analysed in some detail. Cellular waveforms describe the combined, effective oscillatory and rotational actuation relevant to the characteristic locomotion of a specific morphotype 1, 2. The chirality of the attached flagellum determines the rotational motion of trypomastigotes, while the flagellar wave that is generated by axonemal oscillations deforms the attached, elastic cell body with characteristic

Lifelong Motion

As strictly extracellular parasites, African trypanosomes do not feature an immotile life cycle stage, which distinguishes them from, for example, Plasmodium, Trypanosoma cruzi or Leishmania. An active flagellum is always present, albeit varying in length from a few μm to several tens of μm. Hence, the most obvious function of transporting a cell through body fluids is accomplished with largely varying efficiency 1, 2.

Concluding Remarks

The apparently simple questions of parasitology, namely those related to life cycles, motile behaviour, or host niches, need some reconsideration (see Outstanding Questions). The precise mode of trypanosome annidation in the mammalian hosts, for example, or the impact of the ever-changing microenvironments on parasite swimming styles and performance, are poorly understood. The methods required to close those gaps, in a statistically sound manner, are available; however, standardised protocols

Acknowledgments

We are grateful to Ines Subota for sharing her tsetse expertise, and wish to thank Christian Reuter for helpful discussions. ME is supported by DFG grants EN305, GRK2157 (3D Tissue Models to Study Microbial Infections by Obligate Human Pathogens), and SPP1726 (Microswimmers – From Single Particle Motion to Collective Behaviour). ME is a member of the Wilhelm Conrad Roentgen Center for Complex Material Systems (RCCM).

Glossary

Ectoperitrophic space
the volume within insect midguts that is separated by the peritrophic matrix from the food bolus.
Interstitial space
contains the main part of extracellular body fluid and fills the spaces between cells and tissue-specific structures.
Peritrophic matrix
a dynamic extracellular sheet that lines the midgut of the tsetse fly and other insects.
Proventriculus
a muscular organ that is connected to the crop of some insects (such as the tsetse fly) and assists with the grinding of food.

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