Under-Expression of Chemosensory Genes in Domiciliary Bugs of the Chagas Disease Vector Triatoma brasiliensis

Axelle Marchant (1, 2, 3, 4, 5) , Florence Mougel (6, 2, 7, 4, 5) , Emmanuelle Joly (8) , Jane Costa (9, 10) , Carlos Eduardo Almeida (11, 12) , Myriam Harry (2, 7, 4, 5)

1 UFR Sciences
2 EGCE - Évolution, génomes, comportement et écologie
3 Université Paris Sud (Paris 11)
4 CNRS - Centre National de la Recherche Scientifique
5 IRD [France-Ouest] - Institut de Recherche pour le Développement
6 UFR Science
7 Université Paris-Saclay
8 iEES - Institut d'écologie et des sciences de l'environnement de Paris
9 FIOCRUZ - Fundação Oswaldo Cruz / Oswaldo Cruz Foundation
10 Laboratório de Biodiversidade Entomológica [Rio de Janeiro]
11 UFPB - Universidade Federal da Paraiba / Federal University of Paraiba
12 UNICAMP - Universidade Estadual de Campinas = University of Campinas

Background In Latin America, the bloodsucking bugs Triatominae are vectors of Trypanosoma cruzi, the parasite that causes Chagas disease. Chemical elimination programs have been launched to control Chagas disease vectors. However, the disease persists because native vectors from sylvatic habitats are able to (re) colonize houses-a process called domiciliation. Triatoma brasiliensis is one example. Because the chemosensory system allows insects to interact with their environment and plays a key role in insect adaption, we conducted a descriptive and comparative study of the chemosensory transcriptome of T. brasiliensis samples from different ecotopes. Methodology/Principal Finding In a reference transcriptome built using de novo assembly, we found transcripts encoding 27 odorant-binding proteins (OBPs), 17 chemosensory proteins (CSPs), 3 odorant receptors (ORs), 5 transient receptor potential channel (TRPs), 1 sensory neuron membrane protein (SNMPs), 25 takeout proteins, 72 cytochrome P450s, 5 gluthatione S-transferases, and 49 cuticular proteins. Using protein phylogenies, we showed that most of the OBPs and CSPs for T. brasiliensis had well supported orthologs in the kissing bug Rhodnius prolixus. We also showed a higher number of these genes within the bloodsucking bugs and more generally within all Hemipterans compared to the other species in the super-order Paraneoptera. Using both DESeq2 and EdgeR software, we performed differential expression analyses between samples of T. brasiliensis, taking into account their environment (sylvatic, peridomiciliary and domiciliary) and sex. We also searched clusters of coexpressed contigs using HTSCluster. Among differentially expressed (DE) contigs, most were under-expressed in the chemosensory organs of the domiciliary bugs compared to the other samples and in females compared to males. We clearly identified DE genes that play a role in the chemosensory system. Conclusion/Significance Chemosensory genes could be good candidates for genes that contribute to adaptation or plastic rearrangement to an anthropogenic system. The domiciliary environment probably includes less diversity of xenobiotics and probably has more stable abiotic parameters than do sylvatic and peridomiciliary environments. This could explain why both detoxification and cuticle protein genes are less expressed in domiciliary bugs. Understanding the molecular basis for how vectors adapt to human dwellings may reveal new tools to control disease vectors; for example, by disrupting chemical communication.

Mots clés: neuron membrane-proteins; pheromone-binding protein; lucorum meyer-dur; rhodnius-prolixus; odorant-binding; insecticide resistance; infestans hemiptera; bloodsucking bug; molecular evolution; northeastern brazil

Domaines: Sciences du Vivant [q-bio]

Axelle Marchant, Florence Mougel, Emmanuelle Joly, Jane Costa, Carlos Eduardo Almeida, et al.. Under-Expression of Chemosensory Genes in Domiciliary Bugs of the Chagas Disease Vector Triatoma brasiliensis. PLoS Neglected Tropical Diseases, 2016, 10 (10), pp.1-26. ⟨10.1371/journal.pntd.0005067⟩. ⟨hal-01602346⟩