The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal

Abstract

Background Triatoma infestans is the main vector of Chagas disease in the Americas, currently transmitting it in Argentina, Paraguay, and Bolivia. Many T. infestans populations present insecticide resistance, reducing the efficiency of control campaigns. Alternative vector control methods are needed, and molecular targets mediating fundamental physiological processes can be a promising option to manipulate kissing bug behavior. Therefore, it is necessary to characterize the main sensory targets, as well as to determine whether they are modulated by physiological factors. In order to identify gene candidates potentially mediating host cue detection, the antennal transcripts of T. infestans fifth instar larvae were sequenced and assembled. Besides, we evaluated whether a blood meal had an effect on transcriptional profiles, as responsiveness to host-emitted sensory cues depends on bug starvation. Results The sensory-related gene families of T. infestans were annotated (127 odorant receptors, 38 ionotropic receptors, 11 gustatory receptors, 41 odorant binding proteins, and 25 chemosensory proteins, among others) and compared to those of several other hemipterans, including four triatomine species. Several triatomine-specific lineages representing sensory adaptations developed through the evolution of these blood-feeding heteropterans were identified. As well, we report here various conserved sensory gene orthogroups shared by heteropterans. The absence of the thermosensor pyrexia, of pickpocket receptor subfamilies IV and VII, together with clearly expanded takeout repertoires, are revealed features of the molecular bases of heteropteran antennal physiology. Finally, out of 2,122 genes whose antennal expression was significantly altered by the ingestion of a blood meal, a set of 41 T. infestans sensory-related genes (9 up-regulated; 32 down-regulated) was detected. Conclusions We propose that the set of genes presenting nutritionally-triggered modulation on their expression represent candidates to mediate triatomine host-seeking behavior. Besides, the triatomine-specific gene lineages found represent molecular adaptations to their risky natural history that involves stealing blood from an enormously diverse set of vertebrates. Heteropteran gene orthogroups identified may represent unknown features of the sensory specificities of this largest group of hemipteroids. Our work is the first molecular characterization of the peripheral modulation of sensory processes in a non-dipteran vector of human disease.

TRPA5 encodes a thermosensitive ankyrin ion channel receptor in a triatomine insect

“…To begin investigating the molecular basis of thermosensation in Rhodnius prolixus , we reanalyzed the genome annotation (version RproC3.3) complemented with transcriptomic resources (see STAR Methods ) to gain insights into gene variation and genomic architecture within the R. prolixus TRP ankyrin family. The genome of R. prolixus 36 and available transcriptomes 45 , 47 , 50 of triatomines, and additional surveyed hemipteran species ( Figures 1 A and S1 ; Table S1 ), harbor members of four TRPA subfamilies. All surveyed heteropteran species appear to lack an ortholog to Pyrexia ( Pyx ) TRP 36 , 50 but possess one gene copy of three canonical ankyrin TRP genes: Waterwitch ( Wtrw ), TRPA1 , and Painless ( Pain ) ( Figures 1 A and S1 ).…”

Local age‐dependent neuromodulation in Rhodnius prolixus antennae

“…The ability of TOs to carry JH has also been pointed out to relate to food intake and foraging behavior, among other functions (Bohbot & Vogt, 2005; Du et al, 2003; Meunier et al, 2007; Sarov‐blat et al, 2000). Indeed, feeding modulates the antennal expression of TO genes in Triatoma infestans , another kissing bug, suggesting a potential association (Latorre Estivalis, Traverso, et al, 2022). Based on that study and our results, we suggest that the expression plasticity observed for these genes in the antennae of triatomines suggests that TOs may be related to the modulation of food source detection.…”

“…et al (2022), in which antennal transcriptomes from unfed fifth instar R. prolixus larvae were sequenced along five different postecdysis age points (0, 2, 4, 6, and 8 days), each age point being replicated seven times (20 antennae per sample). Takeout gene IDs were obtained from Latorre Estivalis, Traverso, et al (2022).…”

“…Nine years after the publication of the genome of R. prolixus and with the addition of subsequent studies in this field, a total of 283 sensory‐related genes have been reported: 116 odorant receptors (ORs), 33 ionotropic receptors (IRs), 28 gustatory receptors (GRs), 27 odorant binding proteins (OBPs), 19 chemosensory proteins (CSPs), four sensory neuron membrane proteins (SNMPs), 32 odorant degrading enzymes (ODEs) that include 10 secreted esterases and 22 members of the cytochrome 4 clade, 14 transient receptor potential channels (TRPs), and 10 pickpockets (PPKs) (Latorre‐Estivalis et al, 2017, 2021; Mesquita et al, 2015). Additionally, a total of 162 neuromodulatory (NM) genes have been annotated for this species: 43 neuropeptides (NPs); 64 G‐protein‐coupled receptors (GPCRs), considering those that act as receptors of NPs, hormones, and biogenic amines (BAs), 23 nuclear receptors (NRs), and 32 takeout (TO) genes (Latorre‐Estivalis et al, 2020; Latorre‐Estivalis, Traverso, et al, 2022; Ons et al, 2016). R. prolixus RNA‐Seq data through the first week after ecdysis showed that 79 sensory‐related (33%) and 78 NM genes (48%) presented an antennal expression higher than five Transcripts per kilobase Per Million mapped reads (TPMs), while these numbers increase to 185 sensory‐related (65%) and 118 NM (73%) genes when 1 TPM is considered as threshold (Latorre‐Estivalis, Große‐Wilde, et al 2022, and this work).…”

Identification of chemosensory genes in the stingless bee Tetragonisca fiebrigi

“…A non-redundant coding sequence (CDS) database of the assembled transcripts was accomplished following the strategy used by Traverso et al . (2022) and Latorre-Estivalis et al . (2022) .…”