An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (Argiope bruennichi)

Abstract

<jats:p>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.</jats:p>

A Spider Toxin Exemplifies the Promises and Pitfalls of Cell-Free Protein Production for Venom Biodiscovery

“…For the bottom-up analysis of USCTX, we employed a workflow that was established for the study of animal toxins in the past [ 39 , 40 ]. Briefly, excised gel pieces were destained in 25 mM of ammonium hydrogen carbonate containing 50% ( v / v ) acetonitrile and then dehydrated with 100% acetonitrile, reswelled in 50 mM of ammonium hydrogen carbonate, again dehydrated with 100% acetonitrile, and finally dried under vacuum.…”

The biology and evolution of spider venoms

“…For example, many spider venoms contain neprilysin metalloproteases and members of the CAP (cysteine‐rich secretory protein, antigen 5 and pathogenesis‐related 1) family, but their molecular role remains unclear (Undheim et al ., 2013; Kuhn‐Nentwig et al ., 2019; Langenegger et al ., 2019; Zobel‐Thropp et al ., 2019; Lüddecke et al ., 2020). Many spider venoms also contain disulfide isomerases, carboxypeptidases, and serine proteases, which may facilitate the post‐translational modification and maturation of toxins (Langenegger et al ., 2019).…”

“…Comparable effects are triggered by other C. salei venom components, including K + ions and the cytolytic peptide cupiennin 1a (Wullschleger et al ., 2005). This mechanism has been described as ‘neurotoxin merging’ and is also likely to play a role in other species that produce CSTX‐related peptides in their venom (Clémençon et al ., 2020; Lüddecke et al ., 2020).…”

Tiergifte als Quelle neuartiger Bioressourcen

“…Eine rezente Analyse des Gifts der Wespenspinne Argiope bruennichi zeigt, dass auch in Spinnengiften viel Neues zu entdecken ist [9]. Toxins evolved convergently in all major animal groups for predation, defense or competition.…”