Colonization of Rhodnius prolixus gut by Trypanosoma cruzi involves an extensive parasite killing

Abstract

Trypanosoma cruzi, the etiological agent of Chagas disease, is ingested by triatomines during their bloodmeal on an infected mammal. Aiming to investigate the development and differentiation of T. cruzi inside the intestinal tract of Rhodnius prolixus at the beginning of infection we fed insects with cultured epimastigotes and blood trypomastigotes from infected mice to determine the amount of recovered parasites after ingestion. Approximately 20% of the ingested parasites was found in the insect anterior midgut (AM) 3 h after feeding. Interestingly, a significant reduction (80%) in the numbers of trypomastigotes was observed after 24 h of infection suggesting that parasites were killed in the AM. Moreover, few parasites were found in that intestinal portion after 96 h of infection. The evaluation of the numbers of parasites in the posterior midgut (PM) at the same periods showed a reduced parasite load, indicating that parasites were not moving from the AM. Additionally, incubation of blood trypomastigotes with extracts from R. prolixus AMs revealed that components of this tissue could induce significant death of T. cruzi. Finally, we observed that differentiation from trypomastigotes to epimastigotes is not completed in the AM; instead we suggest that trypomastigotes change to intermediary forms before their migration to the PM, where differentiation to epimastigotes takes place. The present work clarifies controversial points concerning T. cruzi development in insect vector, showing that parasite suffers a drastic decrease in population size before epimastigonesis accomplishment in PM.

Recently differentiated epimastigotes from Trypanosoma cruzi are infective to the mammalian host

“…Some recent data show that epimastigogenesis is accomplished only when ama-like/intermediary forms reach PM (Haydock et al, 2015;Ferreira et al, 2016;Guarneri and Lorenzo, 2016), corroborating the classical description of Dias (1934) and the results of the present work. AM seems an inhospitable environment for T. cruzi, since incoming trypomastigotes in a blood meal suffer an extensive parasite killing (population bottleneck) in the first hours after triatomine infection (Dias Fde et al, 2015;Ferreira et al, 2016). Hence, primary epimastigogenesis seems to be completed only in the PM.…”

“…Interestingly, we never observed epimastigote forms in AM. In accordance with a recent work of our group using CL Brener strain (Ferreira et al, 2016) and with a classical work on T. cruzi biology (Dias, 1934), epimastigotes first appear only in triatomine PM (Fig. 7).…”

“…Blood trypomastigotes are very labile forms that lose the flagellum and differentiate to amastigote‐like forms in first hours of AM infection, corroborating the labile characteristic also observed for cell derived trypomastigotes on in vitro epimastigogenesis analysis (Fig. ); the amastigote like forms are agglutinated in AM after one or two days of AM residence, but the reason for this agglutination is unknown, perhaps a response to extensive parasite killing in AM (Ferreira et al ., ). After 5 days of triatomine infection, remaining parasites still showed an ama‐like form in AM but with a more elongated body.…”

The Influence of Environmental Cues on the Development of Trypanosoma cruzi in Triatominae Vector

“…Midgut colonization by T. cruzi was recently revisited by Ferreira and collaborators, and as reported by Dias (1934), epimastigogenesis was shown to be completed in the PM of R. prolixus (Ferreira et al, 2016) and not in the anterior midgut, as was assumed for quite some time. Furthermore, the AM seems to be an inhospitable environment for the parasite, since the trypomastigote population is severely reduced 24 h after invading this portion of the gut (Dias et al, 2015;Ferreira et al, 2016;reviewed in Guarneri and Lorenzo, 2017). During this initial interval, it is assumed that the remaining parasites differentiate into intermediate or amastigotelike forms and quickly travel to the PM, where they will start to replicate (Guarneri and Lorenzo, 2017).…”

“…This indicates dynamic behavior in which both metacyclogenesis and secondary epimastigogenesis can occur in the triatomine rectum (Kessler et al, 2017). Midgut colonization by T. cruzi was recently revisited by Ferreira and collaborators, and as reported by Dias (1934), epimastigogenesis was shown to be completed in the PM of R. prolixus (Ferreira et al, 2016) and not in the anterior midgut, as was assumed for quite some time. Furthermore, the AM seems to be an inhospitable environment for the parasite, since the trypomastigote population is severely reduced 24 h after invading this portion of the gut (Dias et al, 2015;Ferreira et al, 2016;reviewed in Guarneri and Lorenzo, 2017).…”