Trypanosoma cruzi Immune Response Modulation Decreases Microbiota in Rhodnius prolixus Gut and Is Crucial for Parasite Survival and Development

Abstract

Trypanosoma cruzi in order to complete its development in the digestive tract of Rhodnius prolixus needs to overcome the immune reactions and microbiota trypanolytic activity of the gut. We demonstrate that in R. prolixus following infection with epimastigotes of Trypanosoma cruzi clone Dm28c and, in comparison with uninfected control insects, the midgut contained (i) fewer bacteria, (ii) higher parasite numbers, and (iii) reduced nitrite and nitrate production and increased phenoloxidase and antibacterial activities. In addition, in insects pre-treated with antibiotic and then infected with Dm28c, there were also reduced bacteria numbers and a higher parasite load compared with insects solely infected with parasites. Furthermore, and in contrast to insects infected with Dm28c, infection with T. cruzi Y strain resulted in a slight decreased numbers of gut bacteria but not sufficient to mediate a successful parasite infection. We conclude that infection of R. prolixus with the T. cruzi Dm28c clone modifies the host gut immune responses to decrease the microbiota population and these changes are crucial for the parasite development in the insect gut.

Rhodnius prolixus Life History Outcomes Differ when Infected with Different Trypanosoma cruzi I Strains

“…This parasite concentration is similar to that used in several other published studies of T. cruzi infection in triatomines, 9,44,46,50,[54][55][56][57][58][59] and blood meals taken by triatomines at this parasite concentration lead to infective doses that fall within the range of peak parasitemias observed in mice and guinea pigs experimentally infected with T. cruzi. 25,27,[60][61][62][63] Insect infection: insect preparation and feeding.…”

Genome of Rhodnius prolixus , an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

“…These findings strongly indicate that either T. cruzi infection does not activate the insect's immune system or that the parasite is not affected by antimicrobial peptides that are produced in response to parasitism or the ingestion of a blood meal. A plausible hypothesis for these data is that T. cruzi developed active evasion or tolerance mechanisms, because activation of these immune pathways did not control T. cruzi populations, as previously suggested (18,19).…”

Physalin B inhibits Trypanosoma cruzi infection in the gut of Rhodnius prolixus by affecting the immune system and microbiota

“…A preliminary test of parasite infection was made with control insects and physalin oral treated insects from 6 to 30 days alter feeding. The infection, when established in the midgut, is more intense from 8 to 13 days (Castro et al, 2012). In the case of the physalins group the parasites did not succeed in maintaining the infection for the full period of 30 days.…”

“…The kinetics of microbiota growth in infected and non-infected insects was investigated daily for 30 days after feeding. The results demonstrated a peak of bacteria concentration at 8 days after feeding and a significant difference between infected and non-infected insects (Castro et al, 2012). Therefore the entire digestive tract was dissected under sterile conditions (without contact of the samples with the outside cuticle of the insect and inside a biological safety flow cabinet) eight days after treatments and homogenized in 1 mL of sterile PBS.…”