Transcriptome analysis in venom gland of the predatory giant ant Dinoponera quadriceps: insights into the polypeptide toxin arsenal of hymenopterans

PLoS One. 2014 Jan 31;9(1):e87556. doi: 10.1371/journal.pone.0087556. eCollection 2014.

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.

Results: We 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.

Conclusions: To 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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ant Venoms / biosynthesis*
  • Ant Venoms / genetics
  • Ants / genetics
  • Ants / metabolism*
  • Gene Expression Profiling / methods
  • Gene Expression Regulation / physiology*
  • Humans
  • Insect Proteins / biosynthesis*
  • Insect Proteins / genetics
  • Transcriptome / physiology*

Substances

  • Ant Venoms
  • Insect Proteins

Grants and funding

The giant ant project was sponsored by the program for funding new research groups of The National Council for Scientific and Technological Development (CNPq), Ministry of Science and Technology, Federal Government of Brazil (program PRONEM/FUNCAP/CNPq, Ref. numbers PRN-0040-00067.01.00/10 and SPU 10582724-0). This study was partly supported by grants from the Science and Technology Development Fund of Macau, China (Ref. no. from 045/2007 to 078/2011/A3). GR-B and ARBPS are grateful to CNPq and the Coordination for the Improvement of Higher Education Personnel (CAPES) Program on Toxinology (Issued 2010), Ministry of Education of the Federal Government of Brazil for partial financial support for this work. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.