Abstract
Background Dinoponera quadriceps is a predatory giant ant that inhabits the Neotropical region and subdues its prey (insects) with stings that deliver a toxic cocktail of molecules. Human accidents occasionally occur and cause local pain and systemic symptoms. A comprehensive study of the D. quadriceps venom gland transcriptome is required to advance our knowledge about the toxin repertoire of the giant ant venom and to understand the physiopathological basis of Hymenoptera envenomation.ResultsWe conducted a transcriptome analysis of a cDNA library from the D. quadriceps venom gland with Sanger sequencing in combination with whole-transcriptome shotgun deep sequencing. From the cDNA library, a total of 420 independent clones were analyzed. Although the proportion of dinoponeratoxin isoform precursors was high, the first giant ant venom inhibitor cysteine-knot (ICK) toxin was found. The deep next generation sequencing yielded a total of 2,514,767 raw reads that were assembled into 18,546 contigs. A BLAST search of the assembled contigs against non-redundant and Swiss-Prot databases showed that 6,463 contigs corresponded to BLASTx hits and indicated an interesting diversity of transcripts related to venom gene expression. The majority of these venom-related sequences code for a major polypeptide core, which comprises venom allergens, lethal-like proteins and esterases, and a minor peptide framework composed of inter-specific structurally conserved cysteine-rich toxins. Both the cDNA library and deep sequencing yielded large proportions of contigs that showed no similarities with known sequences.ConclusionsTo our knowledge, this is the first report of the venom gland transcriptome of the New World giant ant D. quadriceps. The glandular venom system was dissected, and the toxin arsenal was revealed; this process brought to light novel sequences that included an ICK-folded toxins, allergen proteins, esterases (phospholipases and carboxylesterases), and lethal-like toxins. These findings contribute to the understanding of the ecology, behavior and venomics of hymenopterans.
Highlights
In recent years, the order Hymenoptera, which comprises numerous species of bees, wasps and ants, has received increasing attention because of their direct and indirect influences on human health, ecological balance, agriculture and the forestry economy
As summarized in figure 2, the comparison of translated sequences with non-redundant protein databanks using BlastX analysis allowed for the classification and identification the following clusters (Fig. 2-A): (1) proteins involved in general metabolism (56% of contigs and singlets; e.g., transferases, ATP synthase, dehydrogenases, ribosomal proteins, and cytocrome c); (2) venomlinked polypeptide gene sequences (15%) that highlighted the predominant expression of dinoponeratoxins, allergen peptides, and an inhibitor cysteine-knot (ICK) motif-containing toxin; (3) cDNA precursor sequences that yielded no hits (20%), and (4) ESTs that represented hypothetical proteins with unknown function (5%)
Comparisons of the amino acid and nucleotide sequences of the hypothetical proteins with a specific arthropod database revealed that the ESTs of D. quadriceps shared homology with polypeptides from scorpions and others ants, including H. saltator, S. invicta and S. saevissima (Fig. 2-B; Table S1)
Summary
The order Hymenoptera, which comprises numerous species of bees, wasps and ants, has received increasing attention because of their direct and indirect influences on human health, ecological balance, agriculture and the forestry economy. The importance of investigating hymenopterans is well-known; information from diverse studies has culminated with the establishment of a genome database This database maintains scientific information about one species of bee (Apis mellifera), two species of bumblebees (Bombus terrestris and B. impatiens), a parasitoid wasp (Nasonia vitripennis), and seven species of ants [1]. The seven ant species detailed in this database include the fungus-growing (leaf cutter) ants Acromyrmex echinatior and Atta cephalotes, the Florida carpenter ant Camponotus floridanus, Jerdon’s jumping ant Harpegnathos saltator, the Argentine ant Linepithema humile, the red harvester ant Pogonomyrmex barbatus, and the fire ant Solenopsis invicta (http:// hymenopteragenome.org/ant_genomes/). A comprehensive study of the D. quadriceps venom gland transcriptome is required to advance our knowledge about the toxin repertoire of the giant ant venom and to understand the physiopathological basis of Hymenoptera envenomation
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