Biochemical characterization of diverse deep-sea anthozoan bioluminescence systems

Abstract

AbstractBioluminescence, light produced by living organisms, is a common trait in the ocean. In benthic ecosystems in the deep-sea, octocorals are some of the most abundant luminous animals. Among luminous sessile organisms, the shallow-water sea pansy Renilla has been well studied for its chemistry and molecular biology. Aside from Renilla, however, little is known about the bioluminescent mechanisms of other anthozoans, especially deep-sea corals. In this study, we investigated the characteristics of bioluminescence in deep-sea anthozoans. The bioluminescent capabilities of Heteropolypus, Kophobelemnon, Paragorgia, and a hormathiid anemone are newly described. Coelenterazine, a substrate for bioluminescent reactions, was detected in extracts from octocorals. Coelenterazine-dependent luciferase activity was found in all the anthozoans. Moreover, immunoreactivity against Renilla luciferase was detected in protein extracts from the families Isididae, Alcyoniidae, Umbellulidae, Funiculinidae, Kophobelemnidae and Protoptilidae, suggesting that all luminous octocorals may share a common biochemical mechanism, which utilizes coelenterazine and Renilla-type luciferase. Our results support the hypothesis that the last common ancestor of all the octocorals was bioluminescent, and that bioluminescence evolved a minimum of six times in Cnidaria. Future studies with robust phylogenies, wide taxon sampling, and comparative transcriptome analyses could reveal the patterns of evolution of bioluminescence in octocorals and anthozoans. Our study provides fundamental observations of deep-sea corals and experimental evidence of their coelenterazine-dependent luciferase systems.