Characterization of odorant binding and chemosensory protein families in the kissing bug Triatoma infestans: comparative analysis among Heteroptera species

Abstract

Background: Plasticity in sensory perception and tolerance to xenobiotics contributes to insects' adaptive capacity and evolutionary success, by enabling them to cope with potentially toxic molecules from the environment or internal milieu. Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) have traditionally been studied in the context of chemoreception. However, accumulating evidence over the past few years indicates that these protein families can also sequester insecticide molecules. In doing so, the insecticide cannot reach its target site and can be more easily eliminated through the feces, complexed with these proteins. Thus, xenobiotic sequestration by OBPs and CSPs may lead to insecticide tolerance or even resistance. In the Southern Cone, the kissing bug Triatoma infestans is the main vector of Trypanosoma cruzi, the protozoan parasite that causes Chagas disease. Vectorial transmission of T. cruzi has not been interrupted in certain regions of Argentina, where several populations of T. infestans highly resistant to insecticides have been reported. Understanding the molecular mechanisms underlying resistance is crucial for designing effective vector control strategies. In this context, studying protein families involved in insecticide sequestration is essential.

Results: We manually corrected predicted gene models and identified new sequences of chemosensory and odorant-binding proteins in five Hemiptera species with different feeding habits. Using this information, we mined the raw genome sequence of T. infestans to identify and characterize their orthologs based on sequence conservation and phylogenetic relationships. In total, 26 chemosensory and 49 odorant-binding proteins were identified in the T. infestans genome. Phylogenetic analysis, tissue-specific expression, and molecular docking with major insecticides were performed to assess possible roles.

Conclusions: This work represents the first comprehensive genomic analysis of chemosensory and odorant-binding protein families across Hemiptera species, as well as the first characterization of these gene families in T. infestans using genomic data. It contributes to a better understanding of the molecular basis of chemoreception and insecticide resistance in T. infestans.

Keywords: Chemoreception; Insecticide; Insects; Kissing bugs; Xenobiotic sequestration.

Fig. 1

A) CSP and B) OBP sequences identified in the genomes of the species analyzed. Black bars indicate the number of complete sequences, and gray bars indicate the number of incomplete sequences. Abbreviations: Clec, C. lectularius; Hhal, H. halys; Nvir, Ne. viridula; Olae, O. laevigatus; Rpro, R. prolixus; Nlug, Ni. lugens; Tinf, T. infestans.

Fig. 2

SeqLogo of T. infestans CSP (A) and OBP (B) sequences. A) The cysteines at positions 59, 66, 85, and 88 in the alignment of CSP8 are conserved in the 24 complete CSP sequences identified in T. infestans. Partial sequences CSP22 and CSP26 were not included. B) The cysteines at positions 67, 169, 173, 224, 247, and 257 in the alignment of OBP1 are conserved in the 31 complete OBP sequences identified in T. infestans. Neither partial OBP sequences nor any minus-C OBP sequences were included.

Fig. 3

Phylogeny of the CSP family. See Additional files 1 and 5 for sequence IDs. A CSP from B. tabaci (AFJ342498.1) was used as an outgroup. Branch support values greater than 0.8 are indicated by gray circles

Fig. 4

Phylogeny of the OBP family. See Additional files 1 and 5 for sequence IDs. An OBP from B. tabaci (XP_018896211.1) was used as an outgroup. Branch support values greater than 0.8 are indicated by gray circles

Fig. 5

CSP expression levels represented as log10 (FPKM+1) in T. infestans. Each column represents a different library from the dataset. A) antennal and B) salivary gland transcriptomes. F: Fed, U: Unfed; A: Adult, N: Nymphal; C: Chile, P: Peru, B1: Bolivian F1, Bc: Bolivian colony, A: Argentina. Cluster analysis with dendrograms grouped proteins by similar expression patterns

Fig. 6

OBP expression levels represented as log10 (FPKM + 1) in T. infestans. Each column represents a different library from the dataset. A) antennal and B) salivary gland transcriptomes. F: Fed, U: Unfed; A: Adult, N: Nymphal; C: Chile, P: Perú, B1: Bolivian F1, Bc: Bolivian colony, A: Argentina. Cluster analysis with dendrograms grouped the proteins by similar expression patterns

Fig. 7

Docking of A) deltamethrin and B) malathion inside TinfCSP19. C Docking of fipronil inside TinfCSP10 (ribbon representation)

Fig. 8

Docking of A) deltamethrin and B) malathion inside TinfOBP45. C) Docking of fipronil inside TinfOBP16 (ribbon representation)