Adaptations in energy metabolism and gene family expansions revealed by comparative transcriptomics of three Chagas disease triatomine vectors

Abstract

BackgroundChagas disease is a parasitic infection caused by Trypanosoma cruzi. It is an important public health problem affecting around seven to eight million people in the Americas. A large number of hematophagous triatomine insect species, occupying diverse natural and human-modified ecological niches transmit this disease. Triatomines are long-living hemipterans that have evolved to explode different habitats to associate with their vertebrate hosts. Understanding the molecular basis of the extreme physiological conditions including starvation tolerance and longevity could provide insights for developing novel control strategies. We describe the normalized cDNA, full body transcriptome analysis of three main vectors in North, Central and South America, Triatoma pallidipennis, T. dimidiata and T. infestans.ResultsTwo-thirds of the de novo assembled transcriptomes map to the Rhodnius prolixus genome and proteome. A Triatoma expansion of the calycin family and two types of protease inhibitors, pacifastins and cystatins were identified. A high number of transcriptionally active class I transposable elements was documented in T. infestans, compared with T. dimidiata and T. pallidipennis. Sequence identity in Triatoma-R. prolixus 1:1 orthologs revealed high sequence divergence in four enzymes participating in gluconeogenesis, glycogen synthesis and the pentose phosphate pathway, indicating high evolutionary rates of these genes. Also, molecular evidence suggesting positive selection was found for several genes of the oxidative phosphorylation I, III and V complexes.ConclusionsProtease inhibitors and calycin-coding gene expansions provide insights into rapidly evolving processes of protease regulation and haematophagy. Higher evolutionary rates in enzymes that exert metabolic flux control towards anabolism and evidence for positive selection in oxidative phosphorylation complexes might represent genetic adaptations, possibly related to prolonged starvation, oxidative stress tolerance, longevity, and hematophagy and flight reduction. Overall, this work generated novel hypothesis related to biological adaptations to extreme physiological conditions and diverse ecological niches that sustain Chagas disease transmission.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4696-8) contains supplementary material, which is available to authorized users.

Nezara viridula (Hemiptera: Pentatomidae) transcriptomic analysis and neuropeptidomics

“…To estimate the proportion of the generated database that is homologous to R. prolixus (httpd://www.vectorbase.org/organisms/rhodnius-prolixus/cdc/rproc3;26), H. halys ( https://i5k.nal.usda.gov/Halyomorpha_halys ), and O. fasciatus ( https://data.nal.usda.gov/dataset/oncopeltus-fasciatus-genome-assembly-10 ) predicted proteomes, we used NCBI-BLASTX (–e 1.0E-05). Putative 1:1 orthologue identification among these datasets was done using the BLAST RBH strategy as described 80 . The orthologues shared by three or more species were calculated using a bash script to simplify this operation (bash script is provided in Supp.…”

Expansions and contractions in gene families of independently-evolved blood-feeding insects

“…Previously, several works explored the relationship between gene families expansions and hematophagy [10,20,37,40], but they usually focused only in one species/ group or few gene families and they did not employ a statistical approach to model the evolution of gene families. Two exceptions are the works of Neafsey et al (2015) [9] and Thomas et al (2020) [41].…”

“…Although several strategies to infer convergent molecular evolution are being developed and used [17], few works aimed to study the convergence of gain and loss in gene copies number across distinct lineages [16]. For example, in insects, the expansion of some gene families has been linked to blood-feeding behavior, since the expression of extra copies of genes would help in blood digestion [18][19][20][21].…”

Salivary and Intestinal Transcriptomes Reveal Differential Gene Expression in Starving, Fed and Trypanosoma cruzi-Infected Rhodnius neglectus

“…Driven by hunger, R. neglectus needs to search for a host to feed, which may explain the increased expression of the transcript for Csp-like (Figure 9A), a protein related to the ability to perceive chemical substances that are important for the insect, in feeding, reproduction, and survival, and has already been identified in several triatomine tissues (Ribeiro et al, 2014;Marchant et al, 2016;Martinez-Barnetche et al, 2018).…”