Multiple parallel expansions of bilaterian-like phototransduction gene families in the eyeless Anthozoa

Abstract

Opsin-mediated phototransduction cascades in photoreceptor cells are primarily responsible for light-mediated behaviors in animals. Although some visual cascades are well-studied, phototransduction mediated by non-visual opsins and in non-model animal lineages are poorly characterized. In the Cnidaria (jellyfish, corals, sea anemones etc.), the sister group to Bilateria (vertebrates, arthropods, mollusks etc.), limited evidence suggests some overlap with bilaterian phototransduction. This raises the question of whether phototransduction pathways arose a single time early in animal evolution or if light signaling cascades have evolved multiple times. These evolutionary patterns remain obscured because almost nothing is known about phototransduction in a major group within Cnidaria, the eyeless Anthozoa (corals, sea anemones, sea pens etc.). To better understand whether bilaterian-like phototransduction could be present in Anthozoa, we phylogenetically characterized 63 genes in 12 protein families known to be crucial in two types of bilaterian phototransduction in the sea anemone Nematostella vectensis. Using high quality genomic data from N. vectensis, we took a candidate gene approach to find phototransduction genes and characterize their expression in development and regeneration. We found that N. vectensis possesses the core suite of proteins for both r-opsin and c-opsin mediated phototransduction. In addition, several new gene subfamilies were identified, particularly in the G protein subunits and TRP channels, and many were anthozoan-specific. We identified a novel G protein subunit family, which we call GVI, and characterized its expression in N. vectensis with in situ hybridization. This expansion of phototransduction genes correlates with a large anthozoan-specific radiation in opsin number, suggesting possible coevolution of receptor and signaling diversity in Anthozoa. While further functional experiments on these genes are needed, our findings are in line with the hypothesis that the common ancestor of Eumetazoa had at least two related phototransduction cascades which then further diversified in each animal lineage.