Bioluminescence chemistry of fireworm Odontosyllis

Significance We report the identification and characterization of the small molecule aspects of the Odontosyllis undecimdonta bioluminescence system. The chemical structures of the 4 best-known marine luciferins are as diverse as their phylogenetic distribution. The unique structure of Odontosyllis luciferin provides a key insight into a completely novel chemical basis of bioluminescence. Odontosyllis oxyluciferin is the only green primary emitter described for any known bioluminescent marine organism. Together with Odontosyllis luciferase, our recent findings provide insight into the biochemistry and photochemistry of a new light-emitting system. Our studies represent a crucial step in the development of orthogonal luminescence-based analytical methods for a variety of applications, including live animal imaging and pharmaceutical development. Marine polychaetes Odontosyllis undecimdonta, commonly known as fireworms, emit bright blue-green bioluminescence. Until the recent identification of the Odontosyllis luciferase enzyme, little progress had been made toward characterizing the key components of this bioluminescence system. Here we present the biomolecular mechanisms of enzymatic (leading to light emission) and nonenzymatic (dark) oxidation pathways of newly described O. undecimdonta luciferin. Spectral studies, including 1D and 2D NMR spectroscopy, mass spectrometry, and X-ray diffraction, of isolated substances allowed us to characterize the luciferin as an unusual tricyclic sulfur-containing heterocycle. Odontosyllis luciferin does not share structural similarity with any other known luciferins. The structures of the Odontosyllis bioluminescent system’s low molecular weight components have enabled us to propose chemical transformation pathways for the enzymatic and nonspecific oxidation of luciferin.