Molecular Tuning of Sea Anemone Stinging

Abstract

The judicious control of behavior in response to environmental cues is key to survival for all living creatures. We choose to study sensory transduction and behavior regulation in cnidarians like jellyfish and anemones because they present as an attractive system with decentralized nervous systems and a unique “all-or-nothing” stinging behavior. Cnidarians use specialized cells called nematocytes to shoot single-use, venom-covered barbs to envenomate prey or predators. How do different cnidarians control stinging for different purposes like predation versus defense? We previously showed that the anemone Nematostella vectensis uses a specialized voltage-gated calcium (CaV) channel to trigger stinging in response to synergistic prey-derived chemicals and touch (Weir et al., 2020). Here we use experiments and theory to reveal that stinging behavior is suited to distinct ecological niches. While the burrowing anemone Nematostella uses uniquely strong CaV inactivation for precise control of predatory stinging, the related anemone Exaiptasia diaphana, which inhabits exposed environments to support photosynthetic endosymbionts, stings indiscriminately for self-defense. Consistent with their indiscriminate stinging behavior, Exaiptasia nematocytes express a CaV splice variant that confers weak CaV inactivation. Chimeric analyses of jellyfish and anemone CaVs revealed that differences in inactivation are mediated by the CaVβ subunit N-terminus. These findings reveal a molecular control mechanism for cnidarian stinging and demonstrate how evolutionary tuning of ion channel structure suits distinct signal processing and behavior.