Abstract
BackgroundAnimal venoms attract enormous interest given their potential for pharmacological discovery and understanding the evolution of natural chemistries. Next-generation transcriptomics and proteomics provide unparalleled, but underexploited, capabilities for venom characterization. We combined multi-tissue RNA-Seq with mass spectrometry and bioinformatic analyses to determine venom gland specific transcripts and venom proteins from the Western black widow spider (Latrodectus hesperus) and investigated their evolution.ResultsWe estimated expression of 97,217 L. hesperus transcripts in venom glands relative to silk and cephalothorax tissues. We identified 695 venom gland specific transcripts (VSTs), many of which BLAST and GO term analyses indicate may function as toxins or their delivery agents. ~38% of VSTs had BLAST hits, including latrotoxins, inhibitor cystine knot toxins, CRISPs, hyaluronidases, chitinase, and proteases, and 59% of VSTs had predicted protein domains. Latrotoxins are venom toxins that cause massive neurotransmitter release from vertebrate or invertebrate neurons. We discovered ≥ 20 divergent latrotoxin paralogs expressed in L. hesperus venom glands, significantly increasing this biomedically important family. Mass spectrometry of L. hesperus venom identified 49 proteins from VSTs, 24 of which BLAST to toxins. Phylogenetic analyses showed venom gland specific gene family expansions and shifts in tissue expression.ConclusionsQuantitative expression analyses comparing multiple tissues are necessary to identify venom gland specific transcripts. We present a black widow venom specific exome that uncovers a trove of diverse toxins and associated proteins, suggesting a dynamic evolutionary history. This justifies a reevaluation of the functional activities of black widow venom in light of its emerging complexity.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-366) contains supplementary material, which is available to authorized users.
Highlights
Animal venoms attract enormous interest given their potential for pharmacological discovery and understanding the evolution of natural chemistries
We hereafter refer to this set of 695 sequences as venom gland specific transcripts (VSTs)
Of the VSTs, 266 (38.3%) had a significant (e-value ≤ 1e-5) BLASTx hit to the UniProt database, while 429 (61.7%) had no significant BLASTx hit to UniProt at this e-value cutoff (Additional file 1)
Summary
Animal venoms attract enormous interest given their potential for pharmacological discovery and understanding the evolution of natural chemistries. Venomous taxa have evolved many times within the metazoa [1], and occur in both vertebrates and invertebrates. The venoms these diverse taxa produce are chemically complex and play key roles in organismal ecology, functioning in both predation and defense. Molecules contributing to the toxicity of venom are the focus of sustained effort aimed at characterizing their physiological roles and biochemical action, given their potential in pharmacological and biomedical applications [2]. The venoms of some spiders have been extensively studied, largely due to the potential for isolating novel insecticidal toxins [7], and reasons of direct medical concern [10,11,12,13]. Past work has focused on a small fraction of total spider species, and much of the molecular diversity of spider venoms remains to be discovered
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