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Transcriptome analysis in venom gland of the predatory giant ant dinoponera quadriceps: Insights into the polypeptide toxin arsenal of hymenopterans
Alba F. C. Torres1; Chen Huang2; Cheong-Meng Chong2; Siu Wai Leung2; Álvaro R. B. Prieto-da-Silva3; Alexandre Havt4; Yves P. Quinet5; Alice M. C. Martins1; Simon M. Y. Lee2; Gandhi Rádis-Baptista6
2014-01-31
Source PublicationPLoS ONE
ISSN19326203
Volume9Issue:1
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. © 2014 Torres et al.

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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. © 2014 Torres et al.

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DOI10.1371/journal.pone.0087556
URLView the original
Indexed BySCIE
Language英語English
WOS Research AreaScience & Technology - Other Topics ; Science & Technology - Other Topics
WOS SubjectMultidisciplinary Sciences
WOS IDWOS:000330621900132
Scopus ID2-s2.0-84900345494
Fulltext Access
Citation statistics
Document TypeJournal article
CollectionDEPARTMENT OF PHARMACEUTICAL SCIENCES
Institute of Chinese Medical Sciences
THE STATE KEY LABORATORY OF QUALITY RESEARCH IN CHINESE MEDICINE (UNIVERSITY OF MACAU)
Corresponding AuthorAlice M. C. Martins
Affiliation1.Department of Clinical and Toxicological Analysis, Faculty of Pharmacy, Federal University of Ceara, Fortaleza, Ceara, Brazil
2.State Key Laboratory of Quality Research in Chinese Medicine and Institute of Chinese Medical Sciences, University of Macau, Macao, China
3.Laboratory of Genetics, Institute Butantan, Sao Paulo, Brazil
4.Department of Physiology and Pharmacology, Faculty of Medicine, Federal University of Ceara, Fortaleza, Ceara, Brazil
5.Laboratory of Entomology, State University of Ceara, Fortaleza, Ceara, Brazil
6.Laboratory of Biochemistry and Biotechnology, Institute for Marine Sciences, Federal University of Ceara
Recommended Citation
GB/T 7714
Alba F. C. Torres,Chen Huang,Cheong-Meng Chong,et al. Transcriptome analysis in venom gland of the predatory giant ant dinoponera quadriceps: Insights into the polypeptide toxin arsenal of hymenopterans[J]. PLoS ONE, 2014, 9(1).
APA Alba F. C. Torres., Chen Huang., Cheong-Meng Chong., Siu Wai Leung., Álvaro R. B. Prieto-da-Silva., Alexandre Havt., Yves P. Quinet., Alice M. C. Martins., Simon M. Y. Lee., & Gandhi Rádis-Baptista (2014). Transcriptome analysis in venom gland of the predatory giant ant dinoponera quadriceps: Insights into the polypeptide toxin arsenal of hymenopterans. PLoS ONE, 9(1).
MLA Alba F. C. Torres,et al."Transcriptome analysis in venom gland of the predatory giant ant dinoponera quadriceps: Insights into the polypeptide toxin arsenal of hymenopterans".PLoS ONE 9.1(2014).
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