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Proc Natl Acad Sci U S A. 2015 Dec 1;112(48):14936-41. doi: 10.1073/pnas.1506226112. Epub 2015 Nov 16.

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

Mesquita RD1, Vionette-Amaral RJ2, Lowenberger C3, Rivera-Pomar R4, Monteiro FA5, Minx P6, Spieth J6, Carvalho AB7, Panzera F8, Lawson D9, Torres AQ10, Ribeiro JM11, Sorgine MH12, Waterhouse RM13, Montague MJ6, Abad-Franch F14, Alves-Bezerra M2, Amaral LR15, Araujo HM16, Araujo RN17, Aravind L18, Atella GC12, Azambuja P5, Berni M19, Bittencourt-Cunha PR2, Braz GR20, Calderón-Fernández G21, Carareto CM22, Christensen MB9, Costa IR2, Costa SG23, Dansa M24, Daumas-Filho CR2, De-Paula IF2, Dias FA12, Dimopoulos G25, Emrich SJ26, Esponda-Behrens N27, Fampa P28, Fernandez-Medina RD29, da Fonseca RN30, Fontenele M16, Fronick C6, Fulton LA6, Gandara AC12, Garcia ES5, Genta FA5, Giraldo-Calderón GI31, Gomes B5, Gondim KC12, Granzotto A22, Guarneri AA32, Guigó R33, Harry M34, Hughes DS9, Jablonka W2, Jacquin-Joly E35, Juárez MP21, Koerich LB7, Lange AB36, Latorre-Estivalis JM32, Lavore A27, Lawrence GG37, Lazoski C7, Lazzari CR38, Lopes RR2, Lorenzo MG32, Lugon MD24, Majerowicz D39, Marcet PL37, Mariotti M33, Masuda H12, Megy K9, Melo AC20, Missirlis F40, Mota T41, Noriega FG42, Nouzova M42, Nunes RD12, Oliveira RL43, Oliveira-Silveira G2, Ons S27, Orchard I36, Pagola L27, Paiva-Silva GO12, Pascual A27, Pavan MG23, Pedrini N21, Peixoto AA5, Pereira MH17, Pike A25, Polycarpo C12, Prosdocimi F2, Ribeiro-Rodrigues R44, Robertson HM45, Salerno AP46, Salmon D2, Santesmasses D33, Schama R5, Seabra-Junior ES46, Silva-Cardoso L2, Silva-Neto MA12, Souza-Gomes M15, Sterkel M2, Taracena ML2, Tojo M47, Tu ZJ48, Tubio JM49, Ursic-Bedoya R3, Venancio TM50, Walter-Nuno AB2, Wilson D9, Warren WC6, Wilson RK6, Huebner E51, Dotson EM52, Oliveira PL53.

Author information

1
Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-909, Brazil; Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; rdmesquita@iq.ufrj.br edotson@cdc.gov pedro@bioqmed.ufrj.br.
2
Programa de Biologia Molecular e Biotecnologia, Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-591, Brazil;
3
Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6;
4
Centro Regional de Estudios Genomicos, Universidad Nacional de La Plata, La Plata 1900, Argentina; Centro de Bioinvestigaciones, Universidad Nacional del Noroeste de Buenos Aires, 2700 Pergamino, Argentina;
5
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro 21040-900, Brazil;
6
McDonnell Genome Institute, Washington University School of Medicine, St. Louis, MO 63108;
7
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-590, Brazil;
8
Sección Genética Evolutiva, Facultad de Ciencias, Universidad de la República, Montevideo 11400, Uruguay;
9
European Molecular Biology Laboratory, European Bioinformatics Institute, Welcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, United Kingdom;
10
Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-909, Brazil; Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro 21040-900, Brazil;
11
Section of Vector Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20852;
12
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Programa de Biologia Molecular e Biotecnologia, Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-591, Brazil;
13
Department of Genetic Medicine and Development, University of Geneva Medical School, Geneva 1211, Switzerland; Swiss Institute of Bioinformatics, Geneva 1211, Switzerland; Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, MA 02139; The Broad Institute of MIT and Harvard, Cambridge, MA 02142;
14
Grupo de Pesquisa em Ecologia de Doenças Transmissíveis na Amazônia, Instituto Leônidas e Maria Deane, Fundação Oswaldo Cruz, Amazonas 69057-070, Brazil;
15
Laboratório de Bioinformática e Análises Moleculares, Instituto de Genética e Bioquímica, Faculdade de Computação, Universidade Federal de Uberlândia, Minas Gerais 38700-002, Brazil;
16
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-591, Brazil;
17
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais 31270-901, Brazil;
18
National Library of Medicine, National Center for Biotechnology Information, National Institutes of Health, Rockville, MD 20894;
19
Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-591, Brazil;
20
Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-909, Brazil; Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil;
21
Instituto de Investigaciones Bioquímicas de La Plata, Facultad de Ciencias Médicas, Universidad Nacional de La Plata-CONICET, La Plata 1900, Argentina;
22
Departamento de Biologia, Universidade Estadual Paulista, São José do Rio Preto, São Paulo 15054-000, Brazil;
23
Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro 21040-900, Brazil;
24
Laboratório de Química e Função de Proteínas e Peptídeos, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Rio de Janeiro 28013-602, Brazil;
25
Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, The Johns Hopkins University, Baltimore, MD 21205-2179;
26
Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556;
27
Centro Regional de Estudios Genomicos, Universidad Nacional de La Plata, La Plata 1900, Argentina;
28
Departamento de Biologia Animal, Instituto de Ciências Biológicas e da Saúde, Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro 23897-000, Brazil;
29
Escola Nacional de Saúde Pública, Fundação Oswaldo Cruz, Rio de Janeiro 21040-360, Brazil;
30
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Núcleo de Pesquisas Ecológicas de Macaé, Universidade Federal do Rio de Janeiro, Rio de Janeiro 27910-970, Brazil;
31
Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556;
32
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Minas Gerais 30190-002, Brazil;
33
Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona 08003, Catalonia, Spain; Universitat Pompeu Fabra, Barcelona 08003, Catalonia, Spain;
34
Laboratoire d'Evolution, Génome et Spéciation, Centre National de la Recherche Scientifique UPR9034/UR 072, Institut de Recherche pour le Développement, 91198 Gif sur Yvette, France; Université Paris-Sud, 91400 Orsay, France;
35
French National Institute For Agricultural Research, Institute of Ecology and Environmental Sciences of Paris, 78000 Versailles, France;
36
Department of Biology, University of Toronto, Mississauga, ON L5L 1C6.
37
Division of Parasitic Diseases and Malaria, Entomology Branch, Centers for Disease Control and Prevention, Atlanta, GA 30329;
38
Institut de Recherche sur la Biologie de l'Insecte, UMR7261, Centre National de la Recherche Scientifique, Université François Rabelais, 37200 Tours, France;
39
Programa de Biologia Molecular e Biotecnologia, Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-591, Brazil; Departamento de Biotecnologia Farmacêutica, Faculdade de Farmácia, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-902, Brazil;
40
Department of Physiology, Biophysics and Neuroscience, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Zacatenco, Mexico City 03760, Mexico;
41
Departamento de Fisiologia e Biofísica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Minas Gerais 31270-901, Brazil;
42
Department of Biological Sciences, Florida International University, Miami, FL 11200;
43
Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-909, Brazil;
44
Núcleo de Doenças Infecciosas, Universidade Federal do Espirito Santo, Espirito Santo 29043-900, Brazil;
45
Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801;
46
Instituto Federal de Educação Ciência e Tecnologia do Rio de Janeiro, Rio de Janeiro 20270-021, Brazil;
47
Department of Physiology, School of Medicine-Center for Resesarch in Molecular Medicine and Chronic Diseases, Instituto de Investigaciones Sanitarias, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain;
48
Department of Biochemistry, Virginia Polytechnic Institute, Blacksburg, VA 24061;
49
Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, United Kingdom; and.
50
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Laboratório de Química e Função de Proteínas e Peptídeos, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Rio de Janeiro 28013-602, Brazil;
51
Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada R3T 2N2.
52
Division of Parasitic Diseases and Malaria, Entomology Branch, Centers for Disease Control and Prevention, Atlanta, GA 30329; rdmesquita@iq.ufrj.br edotson@cdc.gov pedro@bioqmed.ufrj.br.
53
Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro 21941-591, Brazil; Programa de Biologia Molecular e Biotecnologia, Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-591, Brazil; rdmesquita@iq.ufrj.br edotson@cdc.gov pedro@bioqmed.ufrj.br.

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.

KEYWORDS:

Chagas disease; Rhodnius prolixus; genome; hematophagy; immunity

PMID:
26627243
PMCID:
PMC4672799
DOI:
10.1073/pnas.1506226112
[Indexed for MEDLINE]
Free PMC Article

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