THE ORIGINS OF MARINE BIOLUMINESCENCE - TURNING OXYGEN DEFENSE-MECHANISMS INTO DEEP-SEA COMMUNICATION TOOLS

Bioluminescence, the emission of ecologically functional light by livi ng organisms, emerged independently on several occasions, yet the evol utionary origins of most bioluminescent systems remain obscure. We pro pose that the luminescent substrates of the luminous reactions (lucife rins) are the evolutionary core of most systems, while luciferases, th e enzymes catalysing the photogenic oxidation of the luciferin, serve to optimise the expression of the endogenous chemiluminescent properti es of the luciferin. Coelenterazine, a luciferin occurring in many mar ine bioluminescent groups, has strong antioxidative properties as it i s highly reactive with reactive oxygen species such as the superoxide anion or peroxides. We suggest that the primary function of coelentera zine was originally the detoxification of the deleterious oxygen deriv atives. The functional shift from its antioxidative to its light-emitt ing function might have occurred when the strength of selection for an tioxidative defence mechanisms decreased. This might have been made po ssible when marine organisms began colonising deeper layers of the oce ans, where exposure to oxidative stress is considerably reduced becaus e of reduced light irradiance and lower oxygen levels. A reduction in metabolic activity with increasing depth would also have decreased the endogenous production of reactive oxygen species. Therefore, in these organisms, mechanisms for harnessing the chemiluminescence of coelent erazine in specialised organs could have developed, while the benefici al antioxidative properties were maintained in other tissues. The full range of graded irradiance in the mesopelagic zone, where the majorit y of organisms are bioluminescent, would have provided a continuum for the selection and improvement of proto-bioluminescence. Although the requirement for oxygen or reactive oxygen species observed in biolumin escent systems reflects the high energy required to produce visible li ght, it may suggest that oxygen-detoxifying mechanisms provided excell ent foundations for the emergence of many bioluminescent systems.