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

Abstract

AbstractUbiquitous 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 excited‐state 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.