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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.

Dataset Information

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

Publications

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

Similar Datasets

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