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

ABSTRACT: Rhodnius prolixus not only has served as a model organism for the study of insect physiology, but also is a major vector of Chagas disease, an illness that affects approximately seven million people worldwide. We sequenced the genome of R. prolixus, generated assembled sequences covering 95% of the genome (? 702 Mb), including 15,456 putative protein-coding genes, and completed comprehensive genomic analyses of this obligate blood-feeding insect. Although immune-deficiency (IMD)-mediated immune responses were observed, R. prolixus putatively lacks key components of the IMD pathway, suggesting a reorganization of the canonical immune signaling network. Although both Toll and IMD effectors controlled intestinal microbiota, neither affected Trypanosoma cruzi, the causal agent of Chagas disease, implying the existence of evasion or tolerance mechanisms. R. prolixus has experienced an extensive loss of selenoprotein genes, with its repertoire reduced to only two proteins, one of which is a selenocysteine-based glutathione peroxidase, the first found in insects. The genome contained actively transcribed, horizontally transferred genes from Wolbachia sp., which showed evidence of codon use evolution toward the insect use pattern. Comparative protein analyses revealed many lineage-specific expansions and putative gene absences in R. prolixus, including tandem expansions of genes related to chemoreception, feeding, and digestion that possibly contributed to the evolution of a blood-feeding lifestyle. The genome assembly and these associated analyses provide critical information on the physiology and evolution of this important vector species and should be instrumental for the development of innovative disease control methods.

SUBMITTER: Mesquita RD

PROVIDER: S-EPMC4672799 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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

Mesquita Rafael D RD Vionette-Amaral Raquel J RJ Lowenberger Carl C Rivera-Pomar Rolando R Monteiro Fernando A FA Minx Patrick P Spieth John J Carvalho A Bernardo AB Panzera Francisco F Lawson Daniel D Torres André Q AQ Ribeiro Jose M C JM Sorgine Marcos H F MH Waterhouse Robert M RM Montague Michael J MJ Abad-Franch Fernando F Alves-Bezerra Michele M Amaral Laurence R LR Araujo Helena M HM Araujo Ricardo N RN Aravind L L Atella Georgia C GC Azambuja Patricia P Berni Mateus M Bittencourt-Cunha Paula R PR Braz Gloria R C GR Calderón-Fernández Gustavo G Carareto Claudia M A CM Christensen Mikkel B MB Costa Igor R IR Costa Samara G SG Dansa Marilvia M Daumas-Filho Carlos R O CR De-Paula Iron F IF Dias Felipe A FA Dimopoulos George G Emrich Scott J SJ Esponda-Behrens Natalia N Fampa Patricia P Fernandez-Medina Rita D RD da Fonseca Rodrigo N RN Fontenele Marcio M Fronick Catrina C Fulton Lucinda A LA Gandara Ana Caroline AC Garcia Eloi S ES Genta Fernando A FA Giraldo-Calderón Gloria I GI Gomes Bruno B Gondim Katia C KC Granzotto Adriana A Guarneri Alessandra A AA Guigó Roderic R Harry Myriam M Hughes Daniel S T DS Jablonka Willy W Jacquin-Joly Emmanuelle E Juárez M Patricia MP Koerich Leonardo B LB Lange Angela B AB Latorre-Estivalis José Manuel JM Lavore Andrés A Lawrence Gena G GG Lazoski Cristiano C Lazzari Claudio R CR Lopes Raphael R RR Lorenzo Marcelo G MG Lugon Magda D MD Majerowicz David D Marcet Paula L PL Mariotti Marco M Masuda Hatisaburo H Masuda Hatisaburo H Megy Karine K Melo Ana C A AC Melo Ana C A AC Missirlis Fanis F Mota Theo T Noriega Fernando G FG Nouzova Marcela M Nunes Rodrigo D RD Oliveira Raquel L L RL Oliveira-Silveira Gilbert G Ons Sheila S Orchard Ian I Pagola Lucia L Paiva-Silva Gabriela O GO Pascual Agustina A Pavan Marcio G MG Pedrini Nicolás N Peixoto Alexandre A AA Pereira Marcos H MH Pike Andrew A Polycarpo Carla C Prosdocimi Francisco F Ribeiro-Rodrigues Rodrigo R Robertson Hugh M HM Salerno Ana Paula AP Salmon Didier D Santesmasses Didac D Schama Renata R Seabra-Junior Eloy S ES Silva-Cardoso Livia L Silva-Neto Mario A C MA Souza-Gomes Matheus M Sterkel Marcos M Taracena Mabel L ML Tojo Marta M Tu Zhijian Jake ZJ Tubio Jose M C JM Ursic-Bedoya Raul R Venancio Thiago M TM Walter-Nuno Ana Beatriz AB Wilson Derek D Warren Wesley C WC Wilson Richard K RK Huebner Erwin E Dotson Ellen M EM Oliveira Pedro L PL

Proceedings of the National Academy of Sciences of the United States of America 20151116 48

Rhodnius prolixus not only has served as a model organism for the study of insect physiology, but also is a major vector of Chagas disease, an illness that affects approximately seven million people worldwide. We sequenced the genome of R. prolixus, generated assembled sequences covering 95% of the genome (∼ 702 Mb), including 15,456 putative protein-coding genes, and completed comprehensive genomic analyses of this obligate blood-feeding insect. Although immune-deficiency (IMD)-mediated immune ...[more]

PMID: 26627243

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Project description:SIFamides are a family of highly conserved neuropeptides in arthropods, and in insects are mainly expressed in four medial neurons in the pars intercerebralis of the brain. Although SIFamide has been shown to influence sexual behavior, feeding, and sleep regulation in holometabolous insects such as Drosophila melanogaster, little is known about its role in hemimetabolous insects, including the blood-sucking bug, Rhodnius prolixus. In this study, we confirm the nucleotide sequence for R. prolixus SIFamide (Rhopr-SIFa) and find characteristic phenotypic expression of SIFamide in four cells of the pars intercerebralis in the brain. In addition to extensive SIFa projections throughout the entire central nervous system, SIFamidergic processes also enter into the corpus cardiacum, and project along the dorsal vessel, suggestive of Rhopr-SIFa acting as a neurohormone. Physiologically, Rhopr-SIFamide induces dose-dependent increases in heartbeat frequency in vitro suggesting the presence of peripheral receptors, and thereby indicating Rhopr-SIFa is released to act upon peripheral targets. We also explore the function of Rhopr-SIFa in R. prolixus, specifically in relation to feeding, since R. prolixus is a blood-gorging insect and a vector for Chagas disease. The intensity of SIFamide-like staining in the neurons in the brain is diminished 2 h following feeding, and restocking of those cells is finished 24 h later, indicating Rhopr-SIFa may be released at feeding. The results of temporal qPCR analysis were consistent with the immunohistochemical findings, showing an increase in Rhopr-SIFa transcript expression in the brain 2 h after feeding. We also observed enhanced feeding (size of meal) in insects injected with Rhopr-SIFa whereas insects with RNAi-mediated knockdown of the Rhopr-SIFa transcript consumed a significantly smaller blood meal relative to controls. These data suggest that the four SIFamidergic neurons and associated arborizations may play an important function in the neuronal circuitry controlling R. prolixus feeding, with Rhopr-SIFa acting as a central and peripheral neuromodulator/neurohormone.

Project description:BackgroundThe causative agent of Chagas disease, Trypanosoma cruzi, and its nonpathogenic relative, Trypanosoma rangeli, are transmitted by haematophagous triatomines and undergo a crucial ontogenetic phase in the insect's intestine. In the process, the parasites interfere with the host immune system as well as the microbiome present in the digestive tract potentially establishing an environment advantageous for development. However, the coherent interactions between host, pathogen and microbiota have not yet been elucidated in detail. We applied a metagenome shotgun sequencing approach to study the alterations in the microbiota of Rhodnius prolixus, a major vector of Chagas disease, after exposure to T. cruzi and T. rangeli focusing also on the functional capacities present in the intestinal microbiome of the insect.ResultsThe intestinal microbiota of R. prolixus was dominated by the bacterial orders Enterobacterales, Corynebacteriales, Lactobacillales, Clostridiales and Chlamydiales, whereas the latter conceivably originated from the blood used for pathogen exposure. The anterior and posterior midgut samples of the exposed insects showed a reduced overall number of organisms compared to the control group. However, we also found enriched bacterial groups after exposure to T. cruzi as well as T rangeli. While the relative abundance of Enterobacterales and Corynebacteriales decreased considerably, the Lactobacillales, mainly composed of the genus Enterococcus, developed as the most abundant taxonomic group. This applies in particular to vectors challenged with T. rangeli and at early timepoints after exposure to vectors challenged with T. cruzi. Furthermore, we were able to reconstruct four metagenome-assembled genomes from the intestinal samples and elucidate their unique metabolic functionalities within the triatomine microbiome, including the genome of a recently described insect symbiont, Candidatus Symbiopectobacterium, and the secondary metabolites producing bacteria Kocuria spp.ConclusionsOur results facilitate a deeper understanding of the processes that take place in the intestinal tract of triatomine vectors during colonisation by trypanosomal parasites and highlight the influential aspects of pathogen-microbiota interactions. In particular, the mostly unexplored metabolic capacities of the insect vector's microbiome are clearer, underlining its role in the transmission of Chagas disease. Video Abstract.

Project description:Chagas disease, caused by the protozoan parasite Trypanosoma cruzi transmitted by blood-sucking insects of the subfamily Triatominae, is a major neglected tropical disease affecting 6 to 7 million of people worldwide. Rhodnius prolixus, one of the most important vectors of Chagas disease in Latin America, is known to be highly sensitive to environmental factors, including temperature. This study aimed to investigate the effects of different temperatures on R. prolixus development and life-cycle, its relationship with T. cruzi, and to gather information about the nutritional habits and energy consumption of R. prolixus. We exposed uninfected and infected R. prolixus to four different temperatures ranging from 24°C to 30°C, and monitored their survival, developmental rate, body and blood meal masses, urine production, and the temporal dynamics of parasite concentration in the excreted urine of the triatomines over the course of their development. Our results demonstrate that temperature significantly impacts R. prolixus development, life-cycle and their relationship with T. cruzi, as R. prolixus exposed to higher temperatures had a shorter developmental time and a higher mortality rate compared to those exposed to lower temperatures, as well as a lower ability to retain weight between blood meals. Infection also decreased the capacity of the triatomines to retain weight gained by blood-feeding to the next developmental stage, and this effect was proportional to parasite concentration in excreted urine. We also showed that T. cruzi multiplication varied depending on temperature, with the lowest temperature having the lowest parasite load. Our findings provide important insights into the potential impact of climate change on the epidemiology of Chagas disease, and can contribute to efforts to model the future distribution of this disease. Our study also raises new questions, highlighting the need for further research in order to understand the complex interactions between temperature, vector biology, and parasite transmission.

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

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

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