Nematostella vectensisexemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia

Abstract

Background: Opsins are the primary proteins responsible for light detection in animals. Cnidarians (jellyfish, sea anemones, corals) have diverse visual systems that have evolved in parallel with bilaterians (squid, flies, fish) for hundreds of millions of years. Medusozoans (e.g. jellyfish, hydroids) have evolved eyes multiple times, each time independently incorporating distinct opsin orthologs. Anthozoans (e.g. corals, sea anemones,) have diverse light-mediated behaviors and, despite being eyeless, exhibit more extensive opsin duplications than medusozoans. To better understand the evolution of photosensitivity in animals without eyes we increased anthozoan representation in the phylogeny of animal opsins and investigated the large but poorly characterized opsin family in the sea anemoneNematostella vectensis. Results: We analyzed genomic and transcriptomic data from 16 species of cnidarians to generate a large opsin phylogeny (708 sequences) with the largest sampling of anthozoan sequences to date. We identified 29 opsins fromN. vectensis(NvOpsins) with high confidence, using transcriptomic and genomic datasets. We found that lineage-specific opsin duplications are common across Cnidaria, with anthozoan lineages exhibiting among the highest numbers of opsins in animals. To establish putative photosensory function of NvOpsins, we identified canonically conserved protein domains and amino acid sequences essential for opsin function in other animal species. We show high sequence diversity among NvOpsins at sites important for photoreception and transduction, suggesting potentially diverse functions. We further examined the spatiotemporal expression ofNvOpsinsand found both dynamic expression of opsins during embryonic development and sexually dimorphic opsin expression in adults. Conclusions: These data show that lineage-specific duplication and divergence has led to expansive diversity of opsins in eyeless cnidarians, suggesting opsins from these animals may exhibit novel biochemical functions. The variable expression patterns of opsins inN. vectensissuggest opsin gene duplications allowed for a radiation of unique sensory cell types with tissue- and stage-specific functions. This diffuse network of distinct sensory cell types could be an adaptive solution for varied sensory tasks experienced in distinct life history stages in anthozoans.

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

“…Mature N. vectensis adults have two germ layers and a mouth that is surrounded by up to sixteen tentacles (Layden et al, 2016). Rather than specialized organs like an eye, specialized cell types are dispersed throughout the animal, including opsin-expressing cells (Layden et al, 2016; McCulloch et al, 2023).…”

“…Though N. vectensis is eyeless, larval dispersal, adult locomotor activity, and sexual reproduction are all light-dependent (Layden et al, 2016; Tarrant et al, 2019). N. vectensis also has among the highest number of opsins found in animals, at 29 (McCulloch et al, 2023). Additionally, N. vectensis have opsins from three groups: cnidopsins, which are sister to bilaterian xenopsins, the A nthozoan S pecific O psins II (ASO-II) which are sister to canonical visual c-opsins, and the A nthozoan S pecific O psins I (ASO-I) which are sister to all other animal opsins (Fig.…”

“…Additionally, N. vectensis have opsins from three groups: cnidopsins, which are sister to bilaterian xenopsins, the A nthozoan S pecific O psins II (ASO-II) which are sister to canonical visual c-opsins, and the A nthozoan S pecific O psins I (ASO-I) which are sister to all other animal opsins (Fig. 1B) (McCulloch et al, 2023). In contrast, medusozoans only have one opsin class, the cnidopsins, which are not sister to c- or r-opsins, making it a challenge to compare these pathways without direct orthology (Fig.…”

“…1B) (Macias-Munõz et al, 2019; Suga et al, 2008). The anthozoan-specific opsin diversity could also be reflected in distinct signaling pathways present in the variety of opsin-expressing cell types in N. vectensis (McCulloch et al, 2023). Understanding the extent of conservation in phototransduction cascade proteins in N. vectensis could help us trace the origins of the phototransduction cascade in animals.…”

“…Cnidarian-specific groups are highlighted in blue. Tree adapted from McCulloch et al 2023. C) Schematic of the c-opsin phototransduction cascade and the proteins investigated in the current study.…”