Identification of Positive Chemotaxis in the Protozoan Pathogen Trypanosoma brucei

Abstract

To complete its infectious cycle, the protozoan parasite Trypanosoma brucei must navigate through diverse tissue environments in both its tsetse fly and mammalian hosts. This is hypothesized to be driven by yet unidentified chemotactic cues. Prior work has shown that parasites engaging in social motility in vitro alter their trajectory to avoid other groups of parasites, an example of negative chemotaxis. However, movement of T. brucei toward a stimulus, positive chemotaxis, has so far not been reported. Here, we show that upon encountering Escherichia coli, socially behaving T. brucei parasites exhibit positive chemotaxis, redirecting group movement toward the neighboring bacterial colony. This response occurs at a distance from the bacteria and involves active changes in parasite motility. By developing a quantitative chemotaxis assay, we show that the attractant is a soluble, diffusible signal dependent on actively growing E. coli. Time-lapse and live video microscopy revealed that T. brucei chemotaxis involves changes in both group and single cell motility. Groups of parasites change direction of group movement and accelerate as they approach the source of attractant, and this correlates with increasingly constrained movement of individual cells within the group. Identification of positive chemotaxis in T. brucei opens new opportunities to study mechanisms of chemotaxis in these medically and economically important pathogens. This will lead to deeper insights into how these parasites interact with and navigate through their host environments. IMPORTANCE Almost all living things need to be able to move, whether it is toward desirable environments or away from danger. For vector-borne parasites, successful transmission and infection require that these organisms be able to sense where they are and use signals from their environment to direct where they go next, a process known as chemotaxis. Here, we show that Trypanosoma brucei, the deadly protozoan parasite that causes African sleeping sickness, can sense and move toward an attractive cue. To our knowledge, this is the first report of positive chemotaxis in these organisms. In addition to describing a new behavior in T. brucei, our findings enable future studies of how chemotaxis works in these pathogens, which will lead to deeper understanding of how they move through their hosts and may lead to new therapeutic or transmission-blocking strategies.

Cyclic AMP signalling and glucose metabolism mediate pH taxis by African trypanosomes

“…Interestingly, there is strong evidence that CARP3 is N-myristoylated 40 This would enable parasites to follow cues provided by the fly as they migrate to different compartments. It is established that procyclic forms respond chemotactically to other effectors 20,21 , but their identities are unknown. Chemotaxis may also explain how parasites in the mammalian host disperse from the bloodstream into other tissues [42][43][44] .…”

Revisiting Plant–Microbe Interactions and Microbial Consortia Application for Enhancing Sustainable Agriculture: A Review

“…The molecular and gene expression studies on Pratylenchus coffeae have been conducted to specify the genes (related to cell wall degrading enzyme) regulated in the presence and absence of root exudates, and it was observed that their activity changed with respect to the host-specific root exudate components provided for the assay ( Bell et al, 2019 ). The protozoan parasite Trypanosoma brucei generally displays its movement away from the other inhabited microbial groups; however, DeMarco et al (2020) have recently observed their positive chemotactic effect toward the colonized area of Escherichia coli . It is due to the presence of attractant that is a soluble, diffusible signal dependent on actively growing E. coli .…”

Right place, right time: Environmental sensing and signal transduction directs cellular differentiation and motility in Trypanosoma brucei

“…This supports at least two signaling events: one to control SoMo initiation and a second to enable avoidance behavior. In a recent advance, DeMarco and colleagues provided the first evidence of positive chemotaxis (DeMarco et al., 2020). Using SoMo assays with procyclic T. brucei , they identified a behavior termed “BacSoMo,” in which parasites dramatically alter their movement toward bacteria (DeMarco et al., 2020).…”

“…In a recent advance, DeMarco and colleagues provided the first evidence of positive chemotaxis (DeMarco et al., 2020). Using SoMo assays with procyclic T. brucei , they identified a behavior termed “BacSoMo,” in which parasites dramatically alter their movement toward bacteria (DeMarco et al., 2020). This study showed that procyclic forms are attracted to a soluble factor derived from living E. coli that acts at a distance to alter parasite motility.…”