Abstract
The genome of the cnidarian Nematostella vectensis (starlet sea anemone) provides a molecular genetic view into the first nervous systems, which appeared in a late common ancestor of cnidarians and bilaterians. Nematostella has a surprisingly large and diverse set of neuronal signaling genes including paralogs of most neuronal signaling molecules found in higher metazoans. Several ion channel gene families are highly expanded in the sea anemone, including three subfamilies of the Shaker K+ channel gene family: Shaker (Kv1), Shaw (Kv3) and Shal (Kv4). In order to better understand the physiological significance of these voltage-gated K+ channel expansions, we analyzed the function of 18 members of the 20 gene Shaker subfamily in Nematostella. Six of the Nematostella Shaker genes express functional homotetrameric K+ channels in vitro. These include functional orthologs of bilaterian Shakers and channels with an unusually high threshold for voltage activation. We identified 11 Nematostella Shaker genes with a distinct “silent” or “regulatory” phenotype; these encode subunits that function only in heteromeric channels and serve to further diversify Nematostella Shaker channel gating properties. Subunits with the regulatory phenotype have not previously been found in the Shaker subfamily, but have evolved independently in the Shab (Kv2) family in vertebrates and the Shal family in a cnidarian. Phylogenetic analysis indicates that regulatory subunits were present in ancestral cnidarians, but have continued to diversity at a high rate after the split between anthozoans and hydrozoans. Comparison of Shaker family gene complements from diverse metazoan species reveals frequent, large scale duplication has produced highly unique sets of Shaker channels in the major metazoan lineages.
Highlights
The classical view of cnidarian nervous system as a simple, diffuse nerve net has been eroded by recent anatomical and genetic findings
It was surprising that the cnidarians, which have traditionally been viewed as having simple nervous systems, had an extensive set of voltage-gated ion channel genes, including cnidarian-specific expansions in 5 of 14 ancestral K+ channel families [2,3]
A lone Shaker gene we identified in the genome of the basal chordate Strongylocentrotus purpuratus [34] (Table S1) was intronless, suggesting that chordate and most cnidarian Shaker genes may have evolved from a common intronless ancestor
Summary
The classical view of cnidarian nervous system as a simple, diffuse nerve net has been eroded by recent anatomical and genetic findings. Sequencing of the Nematostella vectensis (anthozoan) and Hydra magnipapillata (hydrozoan) genomes revealed that the molecular building blocks of the nervous system (including genes that regulate neuronal development, synapse formation and electrical signaling) are conserved between cnidarians and bilaterians [1,2]. The ion channel families shared between bilaterians and cnidarians were likely present in the first nervous systems and may represent a fundamental set of ion channels required for complex neuronal signaling. 43 of 46 ion channel families conserved across Bilateria, including all major classes of voltage-gated ion channels, are present in Nematostella [3]. It was surprising that the cnidarians, which have traditionally been viewed as having simple nervous systems, had an extensive set of voltage-gated ion channel genes, including cnidarian-specific expansions in 5 of 14 ancestral K+ channel families [2,3]. The large number of genes implies a high degree of diversity in the intrinsic electrical properties of cnidarian neurons and raises the question of why such diversity is needed in a comparatively simple nervous system
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