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, 98 (20), 11148-51

Can Coelenterates Make Coelenterazine? Dietary Requirement for Luciferin in Cnidarian Bioluminescence

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Can Coelenterates Make Coelenterazine? Dietary Requirement for Luciferin in Cnidarian Bioluminescence

S H Haddock et al. Proc Natl Acad Sci U S A.

Abstract

In the calcium-activated photoprotein aequorin, light is produced by the oxidation of coelenterazine, the luciferin used by at least seven marine phyla. However, despite extensive research on photoproteins, there has been no evidence to indicate the origin of coelenterazine within the phylum Cnidaria. Here we report that the hydromedusa Aequorea victoria is unable to produce its own coelenterazine and is dependent on a dietary supply of this luciferin for bioluminescence. Although they contain functional apophotoproteins, medusae reared on a luciferin-free diet are unable to produce light unless provided with coelenterazine from an external source. This evidence regarding the origins of luciferin in Cnidaria has implications for the evolution of bioluminescence and for the extensive use of coelenterazine among marine organisms.

Figures

Figure 1
Figure 1
The hydromedusa Aequorea victoria. In bioluminescent specimens, light is produced by photoproteins and associated green-fluorescent protein localized around the bell margin (not shown). The photograph, taken under white light, shows the medusa in its natural state, but does not show luminescence or fluorescence.
Figure 2
Figure 2
Regeneration of extracted apophotoprotein from nonluminous Aequorea victoria. Extracts incubated with coelenterazine produced light upon the addition of Ca2+. The negative control consisted of extracts of aquarium-reared, nonluminous scyphomedusa Aurelia aurita, from which protoprotein could not be regenerated.
Figure 3
Figure 3
Induction of bioluminescence by feeding. (a) Feeding with natural prey induced luminescence only when the prey was originally bioluminescent, as with the hydromedusa Mitrocoma cellularia and the lobate ctenophore Bathocyroe fosteri. Nonluminous prey such as the cydippid ctenophore Hormiphora californensis did not cause nonluminous A. victoria to become bioluminescent. (b) A. victoria fed on the nonluminescent scyphomedusa Aurelia aurita became luminescent only if the prey had been injected with coelenterazine before feeding.
Figure 4
Figure 4
Mechanical stimulation of medusae after direct injection. (a) Nonluminescent A. victoria became luminescent upon injection of coelenterazine, but not after equal treatments of methanol, coelenteramide, or Cypridina-type luciferin alone (not shown). Nonluminous Aurelia aurita did not produce light under any treatments. (b) Captive-reared Eutonina indicans produced flashes upon stimulation after direct injection with coelenterazine but not with Cypridina-type (ostracod) luciferin.
Figure 5
Figure 5
Light production could be stimulated soon after injection of coelenterazine into nonluminous A. victoria and persisted for several days. Data show integrated light from periodic trials of an individual medusa.

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