5. The problem of the early evolution of bioluminescence systems
The origin of bioluminescence is regarded as a problematic aspect of Darwin’s theory of evolution (for recent discussions see Czyż & Węgrzyn 2001a, Labas et al. 2001). The problem is that the function of bioluminescence is generally believed to be directly associated with the visual behaviour of organisms. If this were true, there should be no benefit to organisms possessing weakly luminescent systems, i.e. emitting low amounts of light. Quite simply, for the development of an efficient system, there has to be positive environmental pressure to select individuals bearing more and more effective systems among population of organisms. However, if we consider that luminescence is advantageous to glowing organisms only when the emitted light is sufficiently intens to be visible, then the development of luminescence during evolution remains obscure, as it is hard to believe that early luminescent systems were as efficient as currently existing ones, or that they appeared suddenly in their present forms. Thus, early luminescence systems of low efficiency had to evolve in order to produce enzymes and substrates allowing highly efficient reactions that produce light easily detectable by the optic organs of other organisms. But how to imagine an evolutionary process based on the selection of organisms producing light more effectively than other individuals at a stage when the intensity of light emitted during bioluminescence was far below that capable of being seen by the naked eye? The question is, therefore, what was the evolutionary drive that led to the establishment of weakly luminescent systems and their further improvement?
Recent studies of the biological role of bacterial luminescence, discussed in the preceding section, have shed new light on the problem of the early evolution of luminescence systems. As described above, bioluminescence can stimulate DNA repair by activating the photoreactivation reaction (Czyż et al. 2000b). Moreover, this stimulation is effective even when luminescence is several hundred times less intense than that observed in wild-type V. harveyi, as demonstrated in experiments with E. coli cells bearing the luxCDABE operon and the luxR gene (Czyż et al. 2000b). Such E. coli cells produce light invisible to the naked eye, but this luminescence is of an intensity that is still sufficient to stimulate effective DNA repair. Therefore, it seems plausible that stimulation of DNA repair could have been an evolutionary drive for bacterial luminescence. When the light emission of the early luminescent bacteria was very weak, more luminescent cells could repair DNA more effectively. This mechanism could have operated even when the emitted light was still invisible to the naked eye. Thus, weakly luminescent bacteria might prevail in competition with cells producing light less effectively in environments endangered by mutagenic factors like UV irradiation.
Very recent results from our laboratory (Czyż & Węgrzyn, submitted) suggest that bioluminescence provides no advantage to bacteria under non-stress conditions. When wild-type luminescent bacteria (a wild-type V. harveyi strain) were cultured together with otherwise isogenic luxA mutants under standard laboratory conditions, the luxA mutants became absolutely predominant over wild-type cells in such mixed cultures. This predominance might be due to the consumption of a significant portion of cell energy for light emission by wild-type bacteria that resulted in their slower growth relative to dark mutants, thus luxA cells prevailed. However, when the mixed cultures were irradiated with UV light, luminescent bacteria dominated over dark mutants. This may well have been because wild-type cells were able to repair DNA more efficiently in the absence of external light and compete more effectively with the luxA mutants.
The results described above (Czyż & Węgrzyn, submitted) may support the hypothesis that stimulation of DNA repair could have been an early evolutionary drive of bacterial bioluminescence. This mechanism could have operated, especially at stages when the efficiency of luminescent systems was yet too weak to produce light detectable by the naked eye but good enough to stimulate photoreactivation. It should also be noted that a similar mechanism could govern another process stimulated by the activity of luciferase, i.e. the detoxification of deleterious oxygen derivatives (see the preceding section). Finally, one might speculate that after the appearance of improved luminescent systems capable of producing light sensed by animals, other evolutionary drives started to operate which led to the establishment of the symbiosis between luminescent bacteria and fish or cephalopods. Nevertheless, stimulation of DNA repair and detoxification of deleterious oxygen derivatives may still be important roles played by bioluminescence in present-day free-living bacteria.
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