Unraveling a Receptor-Mediated Bioluminescence Signaling Pathway in Red Tide Algae

G protein-coupled receptors (GPCRs) are ubiquitous transmembrane proteins in multicellular life. Human vision, taste, and neuron activity are all mediated by GPCRs, and a large percentage of currently approved drugs target GPCRs. However, our understanding of GPCRs in single-celled eukaryotes is incomplete, and many of the components of GPCR signal transduction are underrepresented in protists. Previous works studying bioluminescent dinoflagellates-single-celled algae involved in coral reef endosymbiosis and toxic red tide blooms-implicate GPCRs in a signaling pathway for bioluminescence but have not elucidated the individual components comprising the pathway. Herein, we identified a novel GPCR in dinoflagellates-Bioluminescence-Inducing Receptor 1 (BIR1)-which plays a significant role in the signaling pathway for bioluminescence in red tide blooms in response to wave turbulence. Additionally, we identified a full endogenous G-protein complex and downstream effectors that are integral to known calcium signaling networks. Based on these identifications, we used knockdown and knockout techniques to demonstrate the integral role of BIR1 in bioluminescence and highlight its role in predator response and shear force-elicited GPCR signaling in red tide blooms. This advance opens avenues for red tide control and supports the existence of similar GPCR pathways involved in bloom toxicity dynamics.