The Evolution of Bioluminescent Oxygen Consumption as an Ancient Oxygen Detoxification Mechanism

Endogenous reductants such as hydrogen sulfide and alkylthiols provided free radical scavenging systems during the early evolution of life. The development of oxygenic photosynthesis spectacularly increased oxygen levels, and ancient life forms were obliged to develop additional antioxidative systems. We develop here the hypothesis of how ``prototypical' bioluminescent reactions had a plausible role as an ancient defense against oxygen toxicity through their ``futile' consumption of oxygen. As oxygen concentrations increased, sufficient light would have been emitted from such systems for detection by primitive photosensors, and evolutionary pressures could then act upon the light emitting characteristics of such systems independently of their use as futile consumers of oxygen. Finally, an example of survival of this ancient mechanism in present-day bioluminescent bacteria (in the Euprymna scolopes–Vibrio fischeri mutualism) is discussed. Once increasing ambient oxygen levels reached sufficiently high levels, the use of ``futile' oxygen consumption became too bioenergetically costly, so that from this time the evolution of bioluminescence via this role was made impossible, and other mechanisms must be developed to account for the evolution of bioluminescence by a wide range of organisms that patently occurred after this (e.g., by insects). Received: 25 May 2000 / Accepted: 14 November 2000