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

Rafael D. Mesquita, Raquel J. Vionette-Amaral, Carl Lowenberger, Rolando Rivera-Pomar, Fernando A. Monteiro, Patrick Minx, John Spieth, A. Bernardo Carvalho, Francisco Panzera, Daniel Lawson, André Q. Torres, Jose M.C. Ribeiro, Marcos H.F. Sorgine, Robert M. Waterhouse, Michael J. Montague, Fernando Abad-Franch, Michele Alves-Bezerra, Laurence R. Amaral, Helena M. Araujo, Ricardo N. AraujoL. Aravind, Georgia C. Atella, Patricia Azambuja, Mateus Berni, Paula R. Bittencourt-Cunha, Gloria R.C. Braz, Gustavo Calderón-Fernández, Claudia M. Claudia, Mikkel B. Christensen, Igor R. Costa, Samara G. Costa, Marilvia Dansa, Carlos R.O. Daumas-Filho, Iron F. De-Paula, Felipe A. Dias, George Dimopoulos, Scott J. Emrich, Natalia Esponda-Behrens, Patricia Fampa, Rita D. Fernandez-Medina, Rodrigo N. Da Fonseca, Marcio Fontenele, Catrina Fronick, Lucinda A. Fulton, Ana Caroline Gandara, Eloi S. Garcia, Fernando A. Genta, Gloria I. Giraldo-Calderón, Bruno Gomes, Katia C. Gondim, Adriana Granzotto, Alessandra A. Guarneri, Roderic Guigó, Myriam Harry, Daniel S.T. Hughes, Willy Jablonka, Emmanuelle Jacquin-Joly, M. Patricia Juárez, Leonardo B. Koerich, José Manuel Latorre-Estivalis, Andrés Lavore, Cristiano Lazoski, Claudio R. Lazzari, Marcelo G. Lorenzo, David Majerowicz, Marco Mariotti, Hatisaburo Masuda, Karine Megy, Ana C.A. Melo, Fanis Missirlis, Theo Mota, Fernando G. Noriega, Rodrigo D. Nunes, Raquel L.L. Oliveira, Gilbert Oliveira-Silveira, Sheila Ons, Lucia Pagola, Gabriela O. Paiva-Silva, Agustina Pascual, Marcio G. Pavan, Alexandre A. Peixoto, Marcos H. Pereira, Andrew Pike, Carla Polycarpo, Francisco Prosdocimi, Rodrigo Ribeiro-Rodrigues, Hugh M. Robertson, Ana Paula Salerno, Didier Salmon, Didac Santesmasses, Renata Schama, Eloy S. Seabra-Junior, Livia Silva-Cardoso, Mario A.C. Silva-Neto, Matheus Souza-Gomes, Marcos Sterkel, Mabel L. Taracena, Marta Tojo, Zhijian Jake Tu, Jose M.C. Tubio, Raul Ursic-Bedoya, Thiago M. Venancio, Ana Beatriz Walter-Nuno, Derek Wilson, Wesley C. Warren, Richard K. Wilson, Erwin Huebner, Ellen M. Dotson, Pedro L. Oliveira

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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 immunedeficiency (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.

Original languageEnglish
Pages (from-to)14936-14941
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number48
DOIs
StatePublished - Dec 1 2015

Keywords

  • Chagas disease
  • Genome
  • Hematophagy
  • Immunity
  • Rhodnius prolixus

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