THE EVOLUTION OF BIOLUMINESCENCE IN BACTERIA

Abstract

Individuals of aerobic, saprophytic bacterial species, encountering a changing environment in which they were regularly exposed to periods of severe hypoxia, would have gained a major selective advantage in fatty acid metabolism if a mutation in a flavoprotein oxygenase permitted them to oxidize accumulated C8‐C18 aliphatic aldehydes to fatty acids at oxygen concentrations below which the cytochrome oxidase mediated electron transport pathway became inhibited. Such mutants, able to continue to metabolize exogenous lipid fatty acids under hypoxia, might have outproduced their wild type ancestors. Colonies of those mutants which utilized reduced flavin mononucleotide (FMNH2) as the flavin cofactor would have been luminous, owing to the fortuitous coincidence that the aldehyde oxygenation resulted in an enzyme‐flavin excited electronic state which emitted blue light with a high fluorescence yield. If this accidental “proto‐bioluminescence” were initially of sufficient brightness to have elicited phototactic responses in nearby motile organisms, increasing thereby detrital food sources or the potential for dispersal and colonization for the bacteria, a new and completely different selective advantage, that of bioluminescent signalling, would have arisen from the original metabolic function. This is the biochemical analog of Darwin's principle of functional change in structural continuity. It is proposed that bacterial luciferase, the FMNH2‐oxygenase in luminous bacteria, was such a mutation. The present ubiquitous distributions of luminous bacterial species in marine waters, on the surfaces of marine animals and as symbionts in the specialized light organs and digestive tracts of many fish species have resulted from subsequent environmental selection and optimization for this original proto‐bioluminescent reaction. By extension it is suggested whereas “protobioluminescence” arose in many species independently whenever metabolic oxygenation of a substrate resulted in an adventitiously efficient chemiluminescence, the function of bioluminescence arose only upon favorable interaction between the “proto‐bioluminescence” and its ecosystem.