Transcriptomic-Proteomic Correlation in the Predation-Evoked Venom of the Cone Snail, Conus imperialis.

Ai-Hua Jin,Paul Alewood,Mriga Dutt,Richard Lewis,Sébastien Dutertre,Alun Jones,Vincent Lavergne

doi:10.3390/md17030177

Abstract

Individual variation in animal venom has been linked to geographical location, feeding habit, season, size, and gender. Uniquely, cone snails possess the remarkable ability to change venom composition in response to predatory or defensive stimuli. To date, correlations between the venom gland transcriptome and proteome within and between individual cone snails have not been reported. In this study, we use 454 pyrosequencing and mass spectrometry to decipher the transcriptomes and proteomes of the venom gland and corresponding predation-evoked venom of two specimens of Conus imperialis. Transcriptomic analyses revealed 17 conotoxin gene superfamilies common to both animals, including 5 novel superfamilies and two novel cysteine frameworks. While highly expressed transcripts were common to both specimens, variation of moderately and weakly expressed precursor sequences was surprisingly diverse, with one specimen expressing two unique gene superfamilies and consistently producing more paralogs within each conotoxin gene superfamily. Using a quantitative labelling method, conotoxin variability was compared quantitatively, with highly expressed peptides showing a strong correlation between transcription and translation, whereas peptides expressed at lower levels showed a poor correlation. These results suggest that major transcripts are subject to stabilizing selection, while minor transcripts are subject to diversifying selection.

Highlights

Venom variation has been described for secretions produced by various venomous animals, such as cone snails [1], scorpions [2,3], snakes [4,5], spiders [6,7], fire ants [8], and parasitic wasps [9].The contributing factors leading to such variation comprise geographical location, feeding habits, season, size, and gender [7,10,11,12,13]
Using an integrated venomics approach, we revealed the occurrence of transcriptomic messiness and variable peptide processing in various cone snail species that may contribute to the venom variation [19]
After motif searching using parameters generated from the ConoServer database [21], a total of 267 unique conopeptide precursors were retrieved, including 96 from the specimen specimen 1 (S1) and 233 from specimen specimen 2 (S2), with 62 overlapping (Figure 1A and Supplementary Table S1)

Summary

Introduction

Venom variation has been described for secretions produced by various venomous animals, such as cone snails [1], scorpions [2,3], snakes [4,5], spiders [6,7], fire ants [8], and parasitic wasps [9].The contributing factors leading to such variation comprise geographical location, feeding habits, season, size, and gender [7,10,11,12,13]. Venom variation has been described for secretions produced by various venomous animals, such as cone snails [1], scorpions [2,3], snakes [4,5], spiders [6,7], fire ants [8], and parasitic wasps [9]. Cone snails are marine molluscs that produce complex venom to defend against predators and to capture prey [14]. The occurrence of individual variation of the dissected and injected venoms of cone snails has been well documented using proteomic approaches [15,16]. Further complexity was added when we discovered that cone snails possess a remarkable ability to inject venoms with differing components in response to predatory.

Methods

Results

Discussion

Conclusion