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Mol Biol Evol. 2019 May 27. pii: msz132. doi: 10.1093/molbev/msz132. [Epub ahead of print]

The birth and death of toxins with distinct functions: a case study in the sea anemone Nematostella.

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Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Israel.
Department of Biology, University of North Carolina at Charlotte, Charlotte, NC, USA.
Department of Toxicology and Pharmacology, Catholic University of Leuven, Leuven, Belgium.


The cnidarian Nematostella vectensis has become an established lab model, providing unique opportunities for venom evolution research. The Nematostella venom system is multimodal: involving both nematocytes and ectodermal gland cells, which produce a toxin mixture whose composition changes throughout the life cycle. Additionally, their modes of interaction with predators and prey vary between eggs, larvae, and adults, which is likely shaped by the dynamics of the venom system. Nv1 is a major component of adult venom, with activity against arthropods (through specific inhibition of sodium channel inactivation) and fish. Nv1 is encoded by a cluster of at least twelve nearly identical genes that were proposed to be undergoing concerted evolution. Surprisingly, we found that Nematostella venom includes several Nv1 paralogs escaping a pattern of general concerted evolution, despite belonging to the Nv1-like family. Here we show two of these new toxins, Nv4 and Nv5, are lethal for zebrafish larvae, but harmless to arthropods, unlike Nv1. Furthermore, unlike Nv1, the newly identified toxins are expressed in early life stages. Using transgenesis and immunostaining, we demonstrate that Nv4 and Nv5 are localized to ectodermal gland cells in larvae. The evolution of Nv4 and Nv5 can be described either as neofunctionalisation or subfunctionalisation. Additionally, the Nv1-like family includes several pseudogenes being an example of nonfunctionalisation and venom evolution through birth and death mechanism. Our findings reveal the evolutionary history for a toxin radiation and point towards the ecological function of the novel toxins constituting a complex cnidarian venom.


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