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 cysteine-rich secretory protein, antigen 5 and pathogenesis-related protein 1 (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 the lineages of smaller 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.
Highlights
Spiders are diverse and species-rich arthropods that have conquered most terrestrial habitats
Venom glands were dissected from 14 female A. bruennichi specimens, and the venom was extracted and set aside for proteomic analysis
This study demonstrated that helical arthropod-neuropeptide-derived (HAND) toxins are derived from hormones of the ion transport peptide/crustacean hyperglycemic hormone (ITP/CHH) family, which are ubiquitous and functionally diverse neuropeptides in arthropods
Summary
Spiders are diverse and species-rich arthropods that have conquered most terrestrial habitats. Spiders possess a unique biochemical toolbox that uses a combination of venom and silk to subdue prey, contributing to their evolutionary success [2] They represent one of the few orders of terrestrial animals in which almost all extant species feature a functional venom system and are considered as the most successful group of venomous animals [3]. Venoms are complex mixtures of low-molecular-weight compounds, peptides and proteins, which act as toxins by disrupting important physiological processes when injected into prey [5,6] They are used for defense, predation or competitor deterrence, but in all cases, they are physiologically expensive traits that have been optimized by strong selective pressure for specific functions. Several blockbuster drugs have been derived from venom components [7], but they were investigated as research tools, cosmetics, industrial enzymes or bioinsecticides [8,9,10,11]
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