Fire fly luciferin as antioxidant and light emitter: the evolution of insect bioluminescence

Insects are the main group with luminescent species among terrestrial animals. In this paper, we report that fire fly luciferin is endowed with antioxidant properties against oxidative and nitrosative stress. The luciferin reduces linoleate peroxidation in acellular tests and increases the viability of mammalian cells exposed to the oxidant tert-butyl hydroperoxide. Dehydrorhodamine-based tests indicate that fire fly luciferin also scavenges peroxynitrite, whereas parallel tests on cells showed a marked protection of cells subjected to the peroxynitrite generator SIN-1. Together, these results suggest that fire fly luciferin's antioxidant properties could help photocytes coping with the hyperoxidant conditions to which they are submitted during luminous emissions. These data could also suggest that the evolutionary foundation of the bioluminescent system could have been the luciferin, and not the luciferase, first serving as a scavenger of oxidants toxic to the cells, then as a light emitting substrate for luciferase precursors. Similarities with the evolutionary scenario proposed for marine bioluminescent organisms relying on coelenterazine suggest that the surprisingly high success rate observed in the independent emergence of bioluminescent animals could reflect the ease of transformation of antioxidant mechanisms into light-producing systems.