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 anemoneNematostella vectensis. Using high quality genomic data fromN. vectensis, we took a candidate gene approach to find phototransduction genes and characterize their expression in development and regeneration. We found thatN. vectensispossesses 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 α subunit family, which we call GαVI, and characterized its expression inN. vectensiswith 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.

Larval swimming in the sea anemone Nematostella vectensis is sensitive to a broad light spectrum and exhibits a wavelength‐dependent behavioral switch

“…Medusozoa, the group including jellyfish and Hydra , have evolved eyes at least 8 times from eyeless forms (Picciani et al., 2018 ). Mostly correlational evidence suggests cnidarian eyes share some homology with bilaterian visual systems in their development, photoreceptor proteins (opsins), and phototransduction pathways (Gehring, 2005 ; Hansen et al., 2023 ; Koyanagi et al., 2008 ; Kozmik et al., 2008 , 2003 ). Some genetic links to light‐mediated behavior in non‐ocular light‐sensing have also been shown in Medusozoa.…”

“…Despite being eyeless, N. vectensis is typical among hexacorals in having among the most opsins of any animal, at 29 (McCulloch et al., 2023 ). The expression patterns of these opsins and the presence of genes involved in multiple bilaterian phototransduction pathways suggest a diversity of light‐mediated behavioral responses in N. vectensis (Hansen et al., 2023 ; McCulloch et al., 2023 ). For instance, some opsins are found only in adults and may be sexually dimorphic in expression levels, suggesting a role in reproduction, while others are only found in larval stages, suggesting a role in swimming and substrate finding in this species (McCulloch et al., 2023 ).…”

Larval swimming in the sea anemoneNematostella vectensisis sensitive to a broad light spectrum and exhibits a wavelength-dependent behavioral switch

“…Medusozoa, the group including jellyfish and Hydra, have evolved eyes at least 8 times from eyeless forms (Picciani et al, 2018). Mostly correlational evidence suggests cnidarian eyes share some homology with bilaterian visual systems in their development, photoreceptors (opsins), and phototransduction pathways (Gehring, 2005;Hansen et al, 2023;Koyanagi et al, 2008;Kozmik et al, 2008Kozmik et al, , 2003. Some genetic links to light behavior in non-ocular light sensing have also been shown in Medusozoa.…”

“…Despite no eye, N. vectensis is typical among hexacorals in having among the most opsins of any animal, at 29 (McCulloch et al, 2023). The expression patterns of these opsins and presence of genes involved in multiple bilaterian phototransduction pathways suggest a diversity of light-mediated behavioral responses in N. vectensis (Hansen et al, 2023; McCulloch et al, 2023). For instance, some opsins are found only in adults and may be sexually dimorphic in expression levels, suggesting a role in reproduction, while others are only found in larval stages, suggesting a role in swimming and substrate finding (McCulloch et al, 2023).…”