Abstract
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 12 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 neofunctionalization or as subfunctionalization. Additionally, the Nv1-like family includes several pseudogenes being an example of nonfunctionalization and venom evolution through birth-and-death mechanism. Our findings reveal the evolutionary history for a toxin radiation and point toward the ecological function of the novel toxins constituting a complex cnidarian venom.
Highlights
The starlet sea anemone Nematostella vectensis inhabits brackish lagoons along the east and west coasts of the United States and Canada (Hand and Uhlinger 1992; Darling et al 2005)
Our study shows that Nv4 and Nv5, to Nv1, are venom components produced by ectodermal gland cells
Because Nematostella does not feed until the primary polyp stage, toxins such as Nv4 and Nv5 produced only from egg to planula stages can be assumed to play purely a protective role
Summary
The starlet sea anemone Nematostella vectensis inhabits brackish lagoons along the east and west coasts of the United States and Canada (Hand and Uhlinger 1992; Darling et al 2005). During its complex life cycle, Nematostella goes through a mobile larval stage (planula) followed by metamorphosis into a sessile adult polyp. Embryos develop inside the egg package until they reach the planula stage ($3 days post fertilization [dpf]), start swimming, and leave the gelatinous package (Hand and Uhlinger 1992). Around 6 dpf, planulae begin metamorphosis into a primary polyps, distinguished by growing four tentacles around their mouth and settling down on the bottom of the pond. The toxin NvePtx protects eggs and planulae from fish predators, whereas Nv1 toxin is involved in both predation and defense in adults (Columbus-Shenkar et al 2018)
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