Ctenophores and parahoxozoans independently evolved complex and functionally diverse sets of voltage-gated K⁺channels

Abstract

The ctenophore speciesMnemiopsis leidyiis known to have a large set of voltage-gated K+channels, but little is known about the functional diversity of these channels or the evolutionary history of this gene family in other ctenophore species. Here, we searched the genomes of two additional ctenophore species,Beroe ovataandHormiphora californensis, for voltage-gated K+channels and functionally expressed a subset ofM. leidyichannels. We found that the last common ancestor of these three disparate ctenophore lineages probably had at least 33 voltage-gated K+channels. Two of these genes belong to the EAG family, and the remaining 31 belong to the Shaker family and form a single clade within the animal/choanoflagellate Shaker phylogeny. We additionally found evidence for 10 of these Shaker channels in a transcriptome of the early branching ctenophore lineageEuplokamis dunlapae, suggesting that the diversification of these channels was already underway early in ctenophore evolution. We functionally expressed 16MnemiopsisShakers and found that they encode a functionally diverse array of voltage-gated K+conductances with functional orthologs for many classic Shaker family subtypes found in cnidarians and bilaterians. Ctenophores therefore appear to have independently evolved much of the voltage-gated K+channel diversity that is shared between cnidarians and bilaterians.