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

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...

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Veröffentlicht in:	Proceedings of the National Academy of Sciences - PNAS Jg. 112; H. 48; S. 14936
Hauptverfasser:	Mesquita, Rafael D, Vionette-Amaral, Raquel J, Lowenberger, Carl, Rivera-Pomar, Rolando, Monteiro, Fernando A, Minx, Patrick, Spieth, John, Carvalho, A Bernardo, Panzera, Francisco, Lawson, Daniel, Torres, André Q, Ribeiro, Jose M C, Sorgine, Marcos H F, Waterhouse, Robert M, Montague, Michael J, Abad-Franch, Fernando, Alves-Bezerra, Michele, Amaral, Laurence R, Araujo, Helena M, Araujo, Ricardo N, Aravind, L, Atella, Georgia C, Azambuja, Patricia, Berni, Mateus, Bittencourt-Cunha, Paula R, Braz, Gloria R C, Calderón-Fernández, Gustavo, Carareto, Claudia M A, Christensen, Mikkel B, Costa, Igor R, Costa, Samara G, Dansa, Marilvia, Daumas-Filho, Carlos R O, De-Paula, Iron F, Dias, Felipe A, Dimopoulos, George, Emrich, Scott J, Esponda-Behrens, Natalia, Fampa, Patricia, Fernandez-Medina, Rita D, da Fonseca, Rodrigo N, Fontenele, Marcio, Fronick, Catrina, Fulton, Lucinda A, Gandara, Ana Caroline, Garcia, Eloi S, Genta, Fernando A, Giraldo-Calderón, Gloria I, Gomes, Bruno, Gondim, Katia C, Granzotto, Adriana, Guarneri, Alessandra A, Guigó, Roderic, Harry, Myriam, Hughes, Daniel S T, Jablonka, Willy, Jacquin-Joly, Emmanuelle, Juárez, M Patricia, Koerich, Leonardo B, Lange, Angela B, Latorre-Estivalis, José Manuel, Lavore, Andrés, Lawrence, Gena G, Lazoski, Cristiano, Lazzari, Claudio R, Lopes, Raphael R, Lorenzo, Marcelo G, Lugon, Magda D, Majerowicz, David, Marcet, Paula L, Mariotti, Marco, Masuda, Hatisaburo, Megy, Karine, Melo, Ana C A, Missirlis, Fanis, Mota, Theo, Noriega, Fernando G, Nouzova, Marcela, Nunes, Rodrigo D, Oliveira, Raquel L L, Oliveira-Silveira, Gilbert, Ons, Sheila, Orchard, Ian, Pagola, Lucia, Paiva-Silva, Gabriela O, Pascual, Agustina, Pavan, Marcio G, Pedrini, Nicolás, Peixoto, Alexandre A, Pereira, Marcos H, Pike, Andrew, Polycarpo, Carla, Prosdocimi, Francisco, Ribeiro-Rodrigues, Rodrigo, Robertson, Hugh M, Salerno, Ana Paula, Salmon, Didier, Santesmasses, Didac, Schama, Renata, Seabra-Junior, Eloy S
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States 01.12.2015
Schlagworte:	Adaptation, Physiological - genetics Animals Base Sequence Chagas Disease Gene Transfer, Horizontal Host-Parasite Interactions - genetics Humans Insect Vectors - genetics Insect Vectors - parasitology Molecular Sequence Data Rhodnius - genetics Rhodnius - parasitology Trypanosoma cruzi - physiology Wolbachia - genetics hematophagy Chagas disease genome Rhodnius prolixus immunity
ISSN:	1091-6490, 1091-6490
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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 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.
AbstractList	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. 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.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.
Author	Peixoto, Alexandre A Amaral, Laurence R Nouzova, Marcela Polycarpo, Carla Lopes, Raphael R Pascual, Agustina Fernandez-Medina, Rita D Calderón-Fernández, Gustavo Abad-Franch, Fernando Guarneri, Alessandra A Montague, Michael J Koerich, Leonardo B Lawson, Daniel Melo, Ana C A Torres, André Q Azambuja, Patricia Aravind, L Mota, Theo Ribeiro-Rodrigues, Rodrigo Giraldo-Calderón, Gloria I Santesmasses, Didac Ons, Sheila Costa, Samara G Pagola, Lucia Dias, Felipe A Costa, Igor R Spieth, John Nunes, Rodrigo D da Fonseca, Rodrigo N Megy, Karine Latorre-Estivalis, José Manuel Paiva-Silva, Gabriela O Lavore, Andrés Esponda-Behrens, Natalia Dimopoulos, George Jablonka, Willy Missirlis, Fanis Garcia, Eloi S Robertson, Hugh M Guigó, Roderic Prosdocimi, Francisco Araujo, Helena M Ribeiro, Jose M C Lange, Angela B Lorenzo, Marcelo G Dansa, Marilvia Genta, Fernando A Pavan, Marcio G Gomes, Bruno Salmon, Didier Mesquita, Rafael D Gandara, Ana Caroline Marcet, Paula L Pedrini, Nicolás Alves-Bezerra, Michele Juárez, M Patricia Daumas-Filho, Carlos R O Carareto
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Keywords	hematophagy Chagas disease genome Rhodnius prolixus immunity
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References	26929356 - Proc Natl Acad Sci U S A. 2016 Mar 8;113(10):E1415-6
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Snippet	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...
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SubjectTerms	Adaptation, Physiological - genetics Animals Base Sequence Chagas Disease Gene Transfer, Horizontal Host-Parasite Interactions - genetics Humans Insect Vectors - genetics Insect Vectors - parasitology Molecular Sequence Data Rhodnius - genetics Rhodnius - parasitology Trypanosoma cruzi - physiology Wolbachia - genetics
Title	Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection
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