Waves of light at the bottom of the ocean: insights into the luminous systems of three Pennatuloidea (Anthozoa)

Bioluminescence is the production of visible light by living organisms. It occurs through the oxidation of specific luciferin substrates catalyzed by luciferase enzymes. Auxiliary proteins such as fluorescent proteins and coelenterazine-binding proteins can modify the wavelength of the emitted light or stabilize reactive luciferin molecules, respectively. Additionally, calcium ions are crucial in the luminescence processes across various species. Despite many bioluminescent organisms, only a few systems have been fully studied, notably the Renilla genus among anthozoans, which uses a coelenterazine-dependent luciferase, calcium-dependent coelenterazine-binding protein, and green fluorescent protein. We investigated the bioluminescence of three sea pen species: Pennatula phosphorea, Funiculina quadrangularis , and Anthoptilum murrayi (Pennatuloidea, Anthozoa). Their light emission spectra reveal peaks at 510 nm, 513 nm, and 485 nm, respectively. We confirmed the coelenterazine-based reaction in all three species. Using transcriptome analyses, we identified luciferases, fluorescent proteins, and coelenterazine-binding transcripts for P. phosphorea and A. murrayi. Immunodetection confirmed luciferase expression in P. phosphorea and F. quadrangularis. We also expressed recombinant A. murrayi luciferase, confirming its activity. We underscore the role of calcium ions in bioluminescence, which is possibly associated with the mechanism of coelenterazine binding and substrate release. The study proposes a model for anthozoan bioluminescence, offering new avenues for futur ecological and functional research on these luminous organisms.