A Kazal-type inhibitor is modulated by Trypanosoma cruzi to control microbiota inside the anterior midgut of Rhodnius prolixus

Soares, Tatiane S.; Buarque, Diego S.; Queiroz, Bruna R.; Gomes, Cícera M.; Braz, Glória R.C.; Araújo, Ricardo Nascimento; Pereira, Marcos H.; Guarneri, Alessandra A.; Tanaka, Aparecida S.

doi:10.1016/j.biochi.2015.02.014

Cited by 32 publications

(22 citation statements)

References 45 publications

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“…The expression of these proteins in the midgut could also play a role in the interaction with pathogens brought by the blood meal. Indeed, an overexpression of R. prolixus trypsin inhibitor RpTI has been observed in the AM following its infection with T. cruzi [ 37 ]. Interestingly, a reduction of the expression of this protein by knockdown showed a significant decrease in the T. cruzi load, while the bacterial load was higher compared to the control insects.…”

Section: Resultsmentioning

confidence: 99%

High-Throughput Identification of the Rhodnius prolixus Midgut Proteome Unravels a Sophisticated Hematophagic Machinery

et al. 2020

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Chagas disease is one of the most common parasitic infections in Latin America, which is transmitted by hematophagous triatomine bugs, of which Rhodnius prolixus is the vector prototype for the study of this disease. The protozoan parasite Trypanosoma cruzi, the etiologic agent of this disease, is transmitted by the vector to humans through the bite wound or mucosa. The passage of the parasite through the digestive tract of its vector constitutes a key step in its developmental cycle. Herewith, by a using high-throughput proteomic tool in order to characterize the midgut proteome of R. prolixus, we describe a set of functional groups of proteins, as well as the biological processes in which they are involved. This is the first proteomic analysis showing an elaborated hematophagy machinery involved in the digestion of blood, among which, several families of proteases have been characterized. The evaluation of the activity of cathepsin D proteases in the anterior part of the digestive tract of the insect suggested the existence of a proteolytic activity within this compartment, suggesting that digestion occurs early in this compartment. Moreover, several heat shock proteins, blood clotting inhibitors, and a powerful antioxidant enzyme machinery against reactive oxygen species (ROS) and cell detoxification have been identified. Highlighting the complexity and importance of the digestive physiology of insects could be a starting point for the selection of new targets for innovative control strategies of Chagas disease.

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Section: Resultsmentioning

confidence: 99%

High-Throughput Identification of the Rhodnius prolixus Midgut Proteome Unravels a Sophisticated Hematophagic Machinery

et al. 2020

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“…prolixus in the first days of infection [ 18 ]. The parasite can induce a Kazal-type protease inhibitor during the first hours of infection, which allows microbiota modulation and thus its successful maintenance in the host [ 66 ].…”

Section: Discussionmentioning

confidence: 99%

Field-collected Triatoma sordida from central Brazil display high microbiota diversity that varies with regard to developmental stage and intestinal segmentation

et al. 2018

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Background/MethodologyTriatomine bugs are the vectors of Trypanosoma cruzi, the agent of Chagas disease. Vector control has for decades relied upon insecticide spraying, but insecticide resistance has recently emerged in several triatomine populations. One alternative strategy to reduce T. cruzi transmission is paratransgenesis, whereby symbiotic bacteria are genetically engineered to produce T. cruzi-killing proteins in the vector’s gut. This approach requires in-depth knowledge of the vectors’ natural gut microbiota. Here, we use metagenomics (16S rRNA 454 pyrosequencing) to describe the gut microbiota of field-caught Triatoma sordida–likely the most common peridomestic triatomine in Brazil. For large nymphs (4th and 5th stage) and adults, we also studied separately the three main digestive-tract segments–anterior midgut, posterior midgut, and hindgut.Principal findingsBacteria of four phyla (12 genera) were present in both nymphs (all five stages) and adults, thus defining T. sordida’s ‘bacterial core’: Actinobacteria (Brevibacterium, Corynebacterium, Dietzia, Gordonia, Nitriliruptor, Nocardia, Nocardiopsis, Rhodococcus, and Williamsia), Proteobacteria (Pseudomonas and Sphingobium), and Firmicutes (Staphylococcus). We found some clear differences in bacterial composition and relative abundance among development stages; overall, Firmicutes and Proteobacteria increased, but Actinobacteria decreased, through development. Finally, the bacterial microbiotas of the bugs’ anterior midgut, posterior midgut, and hindgut were sharply distinct.Conclusions/SignificanceOur results identify the ‘bacterial core set’ of T. sordida and reveal important gut microbiota differences among development stages–particularly between 1st–3rd stage nymphs and adults. Further, we show that, within any given development stage, the vectors’ gut cannot be regarded as a single homogeneous environment. Cultivable, non-pathogenic ‘core’ bacterial species may now be tested as candidates for paratransgenic control of T. cruzi transmission by T. sordida.

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“…This temporal window is not only important for parasite survival, but also for insect homeostasis. For establishing a successful infection, T. cruzi modulates vector immunity increasing the basal response against microbial proliferation after feeding, via an intensified activity of defensive routes including AMPs, phenoloxidases and antimicrobial proteases [15, 56–58] (Fig. 4b).…”

Section: Discussionmentioning

confidence: 99%

Triatomine bugs, their microbiota and Trypanosoma cruzi: asymmetric responses of bacteria to an infected blood meal

et al. 2016

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BackgroundTriatomine bugs (Hemiptera: Reduviidae) are vectors of the flagellate Trypanosoma cruzi, the causative agent of Chagas disease. The study of triatomine gut microbiota has gained relevance in the last years due to its possible role in vector competence and prospective use in control strategies. The objective of this study is to examine changes in the gut microbiota composition of triatomines in response to a T. cruzi-infected blood meal and identifying key factors determining those changes.ResultsWe sampled colony-reared individuals from six triatomine vectors (Panstrongylus megistus, Rhodnius prolixus, Triatoma brasiliensis, T. infestans, T. juazeirensis and T. sherlocki) comparing experimentally T. cruzi strain 0354-challenged and non-challenged insects. The microbiota of gut and gonad tissues was characterized using high throughput sequencing of region V3-V4 of bacterial 16S rRNA gene. The triatomine microbiota had a low intra-individual diversity, and a high inter-individual variation within the same host species. Arsenophonous appeared as the dominant triatomine bacterial symbiont in our study (59% of the total 16S coverage), but there were significant differences in the distribution of bacterial genera among vectors. In Rhodnius prolixus the dominant symbiont was Pectobacterium.Conclusions Trypanosoma cruzi-challenge significantly affects microbiota composition, with challenged vectors harbouring a significantly more diverse bacterial community, both in the gut and the gonads. Our results show that blood-feeding with T. cruzi epimastigotes strongly affects microbiota composition in a species-specific manner. We suggest that triatomine-adapted enterobacteria such as Arsenophonus could be used as stable vectors for genetic transformation of triatomine bugs and control of Chagas disease.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1926-2) contains supplementary material, which is available to authorized users.

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A Kazal-type inhibitor is modulated by Trypanosoma cruzi to control microbiota inside the anterior midgut of Rhodnius prolixus

Cited by 32 publications

References 45 publications

High-Throughput Identification of the Rhodnius prolixus Midgut Proteome Unravels a Sophisticated Hematophagic Machinery

High-Throughput Identification of the Rhodnius prolixus Midgut Proteome Unravels a Sophisticated Hematophagic Machinery

Field-collected Triatoma sordida from central Brazil display high microbiota diversity that varies with regard to developmental stage and intestinal segmentation

Triatomine bugs, their microbiota and Trypanosoma cruzi: asymmetric responses of bacteria to an infected blood meal

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