Abstracts

The bioluminescence of brittle stars has long captivated scientists, and it’s not over yet! Previous research suggested that the luciferase enzyme of the brittle star Amphiura filiformis is homologous to the one of the sea pansy Renilla (Cnidaria). Surprisingly, these enzymes also share high sequence identity and structural similarity with haloalkane dehalogenases which are mostly microbial enzymes that cleave carbon-halogen bonds in diverse halogenated hydrocarbons. This suggests that ancestral non-luciferase enzymes were convergently co-opted into luciferases in cnidarians and echinoderms. Using chromosome-scale genome, extensive transcriptome analyses, immunodetections and in situ hybridisations, we identified multiple luciferase genes in the brittle star and studied their expression during development and arm regeneration. Our investigation revealed nine luciferase-like gene copies, with seven organised in two clusters of tandem duplicates and two existing as isolated copies. In echinoderms, the presence of multiple Renilla-type luciferase-like gene copies stands out as a notable example of lineage-specific evolution through tandem duplications followed by asymmetric divergence. Our analyses indicate that luciferase-like genes have undergone duplication events across all echinoderm lineages except for sea stars. These luciferase-like genes possibly encode diverse functions across bioluminescent and non-bioluminescent species. Further investigation revealed the presence of luciferase mRNAs and proteins in the light-emitting spines and central nervous system of adult brittle stars. The expression of luciferase peaked during the differentiation of spines during the regeneration process. This research provides valuable insights into the dynamic evolutionary processes that shape the functional repertoire of echinoderm genomes and drive the evolution of echinoderm bioluminescence.