An economic dilemma between weapon systems may explain an arachno-atypical venom in wasp spiders (Argiope bruennichi)

Abstract

Spiders use venom to subdue their prey, but little is known about the diversity of venoms in different spider families. Given the limited data available for orb-weaver spiders (Araneidae) we selected the wasp spider Argiope bruennichi for detailed analysis. Our strategy combined a transcriptomics pipeline based on multiple assemblies with a dual proteomics workflow involving parallel mass spectrometry techniques and electrophoretic profiling. We found that the remarkably simple venom of A. bruennichi has an atypical composition compared to other spider venoms, prominently featuring members of the CAP superfamily and other, mostly high-molecular-weight proteins. We also detected a subset of potentially novel toxins similar to neuropeptides. We discuss the potential function of these proteins in the context of the unique hunting behavior of wasp spiders, which rely mostly on silk to trap their prey. We propose that the simplicity of the venom evolved to solve an economic dilemma between two competing yet metabolically expensive weapon systems. This study emphasizes the importance of cutting-edge methods to encompass smaller lineages of venomous species that have yet to be characterized in detail, allowing us to understand the biology of their venom systems and to mine this prolific resource for translational research.

Enlighting the toxinological dark matter of spider venom enzymes

“…CAPs isolated from snake venom are neurotoxic whereas those from hematophagous species are potentially hemotoxic [10], and little is known about spider venom CAPs. However, based on sequence similarity to Conus CAP proteins, they may represent a hitherto unrecognized lineage of proteases [30] and we therefore included them in our survey. One CAP has been described thus far from each of the families Barychelidae (Trittame), Lycosidae (Lycosa) and Ctenidae (Phoneutria).…”

“…The only exceptions are sphingomyelinase D enzymes from sicariid spiders and a few neurotoxin-processing enzymes involved in toxin maturation [25][26][27][28][29]. However, in some araneomorph spiders, enzymes may be the major venom components, implying they serve important biological functions [30,31]. This growing body of evidence suggests that spider venoms contain a vast resource of undiscovered enzymes that can be thought of as toxinological dark matter.…”