Abstract
Cone snails use separately evolved venoms for prey capture and defence. While most use a harpoon for prey capture, the Gastridium clade that includes the well-studied Conus geographus and Conus tulipa, have developed a net hunting strategy to catch fish. This unique feeding behaviour requires secretion of “nirvana cabal” peptides to dampen the escape response of targeted fish allowing for their capture directly by mouth. However, the active components of the nirvana cabal remain poorly defined. In this study, we evaluated the behavioural effects of likely nirvana cabal peptides on the teleost model, Danio rerio (zebrafish). Surprisingly, the conantokins (NMDA receptor antagonists) and/or conopressins (vasopressin receptor agonists and antagonists) found in C. geographus and C. tulipa venom failed to produce a nirvana cabal-like effect in zebrafish. In contrast, low concentrations of the non-competitive adrenoceptor antagonist ρ-TIA found in C. tulipa venom (EC50 = 190 nM) dramatically reduced the escape response of zebrafish larvae when added directly to aquarium water. ρ-TIA inhibited the zebrafish α1-adrenoceptor, confirming ρ-TIA has the potential to reverse the known stimulating effects of norepinephrine on fish behaviour. ρ-TIA may act alone and not as part of a cabal, since it did not synergise with conopressins and/or conantokins. This study highlights the importance of using ecologically relevant animal behaviour models to decipher the complex neurobiology underlying the prey capture and defensive strategies of cone snails.
Highlights
Cone snails use separately evolved venoms for prey capture and defence
Venomic studies of C. geographus revealed the presence of non-paralytic conantokins, conopressins, contulakins and conoinsulins in the distal duct segment where the predatory-evoked venoms are secreted in this species[2,12,13,14]
Recent venomic studies of C. tulipa support a similar distribution, with conantokins dominant in the distal duct section, the α1-adrenoceptor (α1-AR) antagonist ρ-TIA and vasopressin receptor (VR) antagonist conopressin-T dominant in the proximal central duct, whereas conoinsulins were only detected at low levels in the C. tulipa transcriptome15. ρ-TIA is an allosteric antagonist of the mammalian α1-AR that binds to a well-characterized pharmacophore on the extracellular surface of this family A GPCR16,17
Summary
While most use a harpoon for prey capture, the Gastridium clade that includes the well-studied Conus geographus and Conus tulipa, have developed a net hunting strategy to catch fish. This unique feeding behaviour requires secretion of “nirvana cabal” peptides to dampen the escape response of targeted fish allowing for their capture directly by mouth. The Gastridium clade, including the well-studied Conus geographus and Conus tulipa, use a net hunting strategy where so called “nirvana cabal” peptides are secreted into the water to inhibit the escape response of teleost fish[7], allowing capture of large fish This study directly implicates ρ-TIA as an antagonist at the zebrafish α1-AR that may contribute to the nirvana cabal, allowing fish capture directly by mouth without harpooning
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