Investigation of the Dinoflagellate Bioluminescence Mechanism: Chemically Initiated Electron Exchange Luminescence or Twisted Intramolecular Charge Transfer?

Ubiquitous in the world’s oceans, dinoflagellates are capable of fantastic displays of bright-blue bioluminescence. This luminosity is a consequence of the oxidation of an open-chain tetrapyrrole, dinoflagellate luciferin (LH2), by the enzyme dinoflagellate luciferase (LCF). While many other bioluminescence systems are well understood, the reaction mechanism of LCF remains enigmatic. A comprehensive density functional theory investigation was used to evaluate several competing mechanisms of LCF catalysis employing distinct excited-state luminophores. The results provide strong evidence in favor of a mechanism of dinoflagellate bioluminescence involving an excitedstate gem-diol(ate) intermediate. Analysis of the molecular orbitals relevant to the emission process indicates that catalysis from the E isomer of LH2 is likely to proceed via a chemically initiated electron-exchange luminescence reaction, whereas that from the Z isomer may involve the formation of a biologically unprecedented twisted intramolecular charge transfer state.