Luciferase a light source for the silica-based optical waveguides (spicules) in the demosponge Suberites domuncula

Abstract

Two classes of sponges (animal phylum Porifera) possess a siliceous skeleton which is composed of spicules. Studying the optical fiber-mechanical properties of large spicules from hexactinellid sponges (> 5 cm) it was demonstrated that they are effective light-collecting optical fibers. Here, we report that the demosponge Suberites domuncula is provided with a biosensor system composed of the (organic) light producing luciferase and the (inorganic) light transducing silica spicules. The light transmission feature of these smaller spicules (200 microm) has been demonstrated and the ability of sponge tissue to generate light has been proven. Screening for a luciferase gene in S. domuncula was successful; the recombinant luciferase was prepared and shown to be bioactive. The luciferase protein is abundantly present in the close neighborhood of the spicules. The expression of the luciferase gene is under the control of light.

A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence

“…and A. filiformis ; figure 6). Recently, similar cases were described for the sponge Suberites domuncula and for the squid Watasenia scintillans , in which firefly-type luciferases were demonstrated to be involved in light emission [71,72] (figure 6). Luciferases could be co-opted from other genes with other functions and share high similarity with these primary genes, as was shown in the case of insect bioluminescence in which luciferases evolved from acyl-CoA ligases [39].…”

Flashing light in sponges through their siliceous fiber network: A new strategy of “neuronal transmission” in animals

“…Following the completion of the molecular biology studies we had unequivocally demonstrated the presence of the gene encoding luciferase [25] and we also reported on the existence of a gene for the luciferin-regenerating enzyme. Furthermore, after demonstrating for the first time both the property of the demosponge spicules to act as optical waveguides and the capacity of the animals to produce light in crude extracts, we showed that the recombinant luciferase was bioactive and caused bioluminescence activity in vitro.…”

“…In order to identify the luciferase in S. domuncula our EST database was screened with the main focus on the presence of polypeptides comprising the characteristic domains for metazoan luciferase [25], e.g., the acetyl-coenzyme A (acyl-CoA) synthetase region and the luciferinbinding site residues. This database, which comprises 30000 ESTs, can be considered to cover most of the genes in sponges.…”

“…Sequence comparison of the S. domuncula luciferase cDNA was performed and the highest sequence similarity was found to be the luciferase protein from P. pyralis [25] (Figure 4(c)). Lower similarities to the 4-coumarate-CoA ligases and the acetyl CoA synthetases were observed, with only 36% similarity (19% identity) to the acetyl CoA synthetase from Saccharomyces cerevisiae.…”

“…More specifically, the expression of the S. domuncula cryptochrome gene after light exposure (the light source within the spectral range of 330900 and 700 1100 nm) [29] is primarily restricted to the surface zone of the animal, suggesting that the photoactivated protein is compartmentalized in the cortex (the outer tissue layer). Similarly, the expression of poriferan luciferase is lightadapted [25].…”