Minicollagen expression dynamics reveal a transcriptional program for cnidogenesis in the sea anemone Nematostella vectensis

Abstract

Cnidae are explosive harpoon-like organelles localized within stinging cells, or cnidocytes, of the phylum Cnidaria (jellyfish, hydroids, sea anemones, and corals). These unique Golgi-derived vesicular structures define the phylum and are prominent examples of an evolutionary cellular novelty. While recent studies have focused on the developmental specification and regulation of cnidocytes more broadly, less is understood about gene expression patterns, structural variations, and toxin repertoires within distinct cnidae subtypes. Here, we determine the transcriptional profile of two major cnidae subtypes in the sea anemone Nematostella vectensis, nematocytes and spirocytes, using the cnidae-specific structural family of proteins called minicollagens. We first define the in vivo expression patterns for three known and three uncharacterized minicollagen orthologs. We show that four minicollagens are broadly expressed throughout ectodermal cnidocytes in developing larvae and primary polyps while two others are restricted to tentacular cnidocytes. Leveraging whole adult scRNA-seq data and two novel transgenic reporter lines, we then demonstrate that the tentacle-restricted cnidocytes are developing spirocytes that are distinguished by expression of the minicollagen NvNcol5. To deepen our analysis of cnidocyte gene expression, we used a customized RNA-FACS-seq pipeline to determine global transcriptional differences between these two subtypes. This approach identified a suite of differentially expressed genes, illuminating spatial and temporal gene expression dynamics across both developing nematocytes and spirocytes. Altogether, our experiments provide fundamental and novel insights into the specialization of cnidarian stinging cells while establishing a rich set of resources for further investigation.