The first venomous crustacean revealed by transcriptomics and functional morphology: remipede venom glands express a unique toxin cocktail dominated by enzymes and a neurotoxin

B.M. von Reumont, A. Blanke, S. Richter, F. Alvarez, C. Bleidorn, R.A. Jenner
Molecular biology and evolution 31(1), 48-58
Graphical abstract: 
Animal venoms have evolved many times. Venomous species are especially common in three of the four main groups of arthropods (Chelicerata, Myriapoda, Hexapoda), which together represent tens of thousands of species of venomous spiders, scorpions, centipedes and hymenopterans. Surprisingly, despite their great diversity of body plans there is no unambiguous evidence that any crustacean is venomous. We provide the first conclusive evidence that the aquatic, blind and cave-dwelling remipede crustaceans are venomous, and that venoms evolved in all four major arthropod groups. We produced a three-dimensional reconstruction of the venom delivery apparatus of the remipede Speleonectes tulumensis, showing that remipedes can inject venom in a controlled manner. A transcriptomic profile of its venom glands shows that they express a unique cocktail of transcripts coding for known venom toxins, including a diversity of enzymes and a probable paralytic neurotoxin very similar to one described from spider venom. We screened a transcriptomic library obtained from whole animals and identified a non-toxin paralogue of the remipede neurotoxin that is not expressed in the venom glands. This allowed us to reconstruct its probable evolutionary origin, and underlines the importance of incorporating data derived from non-venom gland tissue to elucidate the evolution of candidate venom proteins. This first glimpse into the venom of a crustacean and primitively aquatic arthropod reveals conspicuous differences from the venoms of other predatory arthropods such as centipedes, scorpions and spiders, and contributes valuable information for ultimately disentangling the many factors shaping the biology and evolution of venoms and venomous species.