Shedding Light on Patterns of Unconventional Expression of Opsin Genes in Hydra vulgaris.

Abstract

Opsins are G-protein-coupled receptors often expressed in neuronal photoreceptor cells and used for light detection in most animals, including cnidarians like corals, jellyfish, and anemones. Opsins may also be expressed in non-neuronal cell types, where they may confer light sensitivity. For example, opsins might be involved in pre-neural phototaxis of larval box jellyfish. However, the overall extent of non-neuronal expression of opsins is not well understood, despite the potential for identifying additional light or opsin-mediated organismal functions. To investigate the prevalence of non-neuronal opsin expression in a cnidarian, we analyzed published data from Hydra vulgaris, a freshwater hydroid that responds to light despite lacking distinct photosensory structures such as eyes. We quantified opsin expression across Hydra cell types and states of cell differentiation using published single-cell RNA sequencing (scRNA-seq) data and assay for transposase-accessible chromatin sequencing data. We identified 45 opsin transcripts in Hydra expressed in neuronal and non-neuronal cell types, as well as across inferred states of cell differentiation. We found a wider diversity of opsin gene transcripts in neuronal cell types, predominantly in fully differentiated cells. In contrast, we detected fewer opsin transcripts in non-neuronal cell types, and they were expressed from stem cell to progenitor cell to fully differentiated cell state-all within the same inferred cell type. These opsin transcripts appear to be expressed at higher levels in ectodermal epithelial cells near the head organizer of Hydra (a key developmental patterning region) and share transcription factor binding motifs with development genes such as Six, Otx, Ptx, Rfx4, and Hxa. Overall, we outline an array of opsin gene transcripts, their expression, and open chromatin patterns across cell type diversity in Hydra, and highlight potential co-regulatory relationships that may pave the way for future work on unconventional roles for opsin genes in Hydra.