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Abstract
Trichomonas vaginalis and Tritrichomonas foetus are extracellular flagellated parasites that inhabit humans and other mammals, respectively. In addition to motility, flagella act in a variety of biological processes in different cell types, and extra-axonemal structures (EASs) have been described as fibrillar structures that provide mechanical support and act as metabolic, homeostatic, and sensory platforms in many organisms. It has been assumed that T. vaginalis and T. foetus do not have EASs. However, here, we used complementary electron microscopy techniques to reveal the ultrastructure of EASs in both parasites. Such EASs are thin filaments (3–5 nm diameter) running longitudinally along the axonemes and surrounded by the flagellar membrane, forming prominent flagellar swellings. We observed that the formation of EAS increases after parasite adhesion on the host cells, fibronectin, and precationized surfaces. A high number of rosettes, clusters of intramembrane particles that have been proposed as sensorial structures, and microvesicles protruding from the membrane were observed in the EASs. Our observations demonstrate that T. vaginalis and T. foetus can connect to themselves by EASs present in flagella. The protein VPS32, a member of the ESCRT-III complex crucial for diverse membrane remodeling events, the pinching off and release of microvesicles, was found in the surface as well as in microvesicles protruding from EASs. Moreover, we demonstrated that the formation of EAS also increases in parasites overexpressing VPS32 and that T. vaginalis-VPS32 parasites showed greater motility in semisolid agar. These results provide valuable data about the role of the flagellar EASs in the cell-to-cell communication and pathogenesis of these extracellular parasites.
Highlights
The eukaryotic flagella are highly conserved microtubule-based organelles that extend from the cell surface
In T. vaginalis, the recurrent flagellum (RF) runs along two-thirds of the cell and no free portion is developed, whereas in T. foetus, the RF reaches the posterior end of the cell and extends beyond the undulating membrane as a free tip (Figure 1)
The presence of flagellar swellings in the tip or along the anterior flagella (AF) and RF was observed in 1%– 11% of T. vaginalis and 2%–5% of T. foetus parasites analyzed by scanning electron microscopy (SEM) (Figure 2A)
Summary
The eukaryotic flagella are highly conserved microtubule-based organelles that extend from the cell surface These structures, beyond being essential for cell locomotion and movement of fluids across the tissues and cells, are signaling platforms that receive and send information to drive cellular responses (Carter and Blacque, 2019; Akella et al, 2020). In addition to cell movement (Imhof et al, 2019) and sensory functions (Maric et al, 2010), a variety of microorganisms employ flagella to control feeding (Dolger et al, 2017), mating (Fussy et al, 2017), cytokinesis (Ralston et al, 2006; Hardin et al, 2017), cell morphogenesis (Vaughan, 2010), cell communication (Szempruch et al, 2016), and cell adhesion (Frolov et al, 2018) Among these microorganisms, there are important human and veterinary parasitic protists, i.e., trichomonads, trypanosomatids, diplomonads, and apicomplexa, that exert a devastating economic burden on global healthcare systems and agriculture (Kruger and Engstler, 2015). Tritrichomonas foetus lives as a commensal in the nasal and gastrointestinal mucosa of pigs (Dabrowska et al, 2020)
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