If host is refractory, insistent parasite goes berserk: Trypanosomatid Blastocrithidia raabei in the dock bug Coreus marginatus

Abstract

Here we characterized the development of the trypanosomatid Blastocrithidia raabei in the dock bug Coreus marginatus using light and electron microscopy. This parasite has been previously reported to occur in the host hemolymph, which is rather typical for dixenous trypanosomatids transmitted to a plant or vertebrate with insect's saliva. In addition, C. marginatus has an unusual organization of the intestine, which makes it refractory to microbial infections: two impassable segments isolate the anterior midgut portion responsible for digestion and absorption from the posterior one containing symbiotic bacteria. Our results refuted the possibility of hemolymph infection, but revealed that the refractory nature of the host provokes very aggressive behavior of the parasite and makes its life cycle more complex, reminiscent of that in some dixenous trypanosomatids. In the pre-barrier midgut portion, the epimastigotes of B. raabei attach to the epithelium and multiply similarly to regular insect trypanosomatids. However, when facing the impassable constricted region, the parasites rampage and either fiercely break through the isolating segments or attack the intestinal epithelium in front of the barrier. The cells of the latter group pass to the basal lamina and accumulate there, causing degradation of the epitheliocytes and thus helping the epimastigotes of the former group to advance posteriorly. In the symbiont-containing post-barrier midgut segment, the parasites either attach to bacterial cells and produce cyst-like amastigotes (CLAs) or infect enterocytes. In the rectum, all epimastigotes attach either to the cuticular lining or to each other and form CLAs. We argue that in addition to the specialized life cycle B. raabei possesses functional cell enhancements important either for the successful passage through the intestinal barriers (enlarged rostrum and well-developed Golgi complex) or as food reserves (vacuoles in the posterior end).

Development of two species of the Trypanosoma theileri complex in tabanids

“…Our detection of trypanosomes outside the ileum lumen is especially intriguing. In contrast to other trypanosomatids that traverse the intestinal wall, because it is an indispensable part of their development within the host [ 60 – 62 ], the exit process could not be captured here, and we observed only its result. Furthermore, the number of parasite cells located from outside of the intestinal epithelium was always modest, further indicating that this may occur inadvertently.…”

Multiple and frequent trypanosomatid co-infections of insects: the Cuban case study

“…While the last decade has seen a significant expansion of the known diversity of insect and plant trypanosomatids including some studies from Asia, Europe and Africa (Votýpka et al, 2010(Votýpka et al, , 2012aLukeš et al, 2018;Frolov et al, 2019Frolov et al, , 2020, it was continental South and Central America where most sampling occurred (Teixeira et al, 1997(Teixeira et al, , 2011Maslov et al, 2007Maslov et al, , 2010Borghesan et al, 2013;Kozminsky et al, 2015;Dario et al, 2021). However, except for a single study conducted on the island of Curacao (Votýpka et al, 2019), so far, no information was available on these interesting protists in the Caribbean.…”

“…This likely reflects the transmission of the former species among its hosts through cells leaving the digestive tract, whereas the latter flagellate has no benefit in leaving the host, as its life cycle proceeds following the ingestion of an infected tabanid (Malysheva et al, 2022). In another case, in the herbivorous species of true bug Coreus marginatus, Phytomonas is transmitted to the host plant via infected salivary glands (Frolov et al, 2019), while the transmission of co-infecting Blastocrithidia among insect hosts occurs by a cyst-like stage, which is formed in the midgut and rectum (Frolov et al, 2020), resulting in functional niche partitioning. Indeed, the coinfections of Phytomonas and Obscuromonas or Blastocrithidia appears to be common among Coreidae, Rhopalidae, Alydidae and Pentatomidae (Votýpka et al, 2012a(Votýpka et al, , 2019this study).…”

Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host

“…The evolutionarily primary and still most frequent localization of these flagellates within the insect host is the intestine [49], which allows direct access to the digested food, while both the entry and exit from this organ are straightforward. However, the parasites have to evolve adaptations preventing their premature discharge, typically by attaching to the intestinal wall via various modifications of the flagellum [50][51][52][53][54][55][56][57][58]. Although Vickermania thrives in the midgut, it cannot implement attachment, since in its fly host the midgut wall is separated from the lumen by a semipermeable continuous structure known as the peritrophic membrane [59].…”