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

Abstract

Sponges (phylum Porifera) represent a successful animal taxon that evolved prior to the Ediacaran-Cambrian boundary (542 million years ago). They have developed an almost complete array of cell- and tissue-based interaction systems necessary for the establishment of a functional, multicellular body. However, a network of neurons, one cell/tissue-communication system is missing in sponges. This fact is puzzling and enigmatic, because these animals possess receptors known to be involved in the nervous system in evolutionary younger animal phyla. As an example, the metabotropic glutamate/GABA-like receptor has been identified and cloned by us. Recently, we have identified a novel light transmission/light responsive system in sponges that is based on their skeletal elements, the siliceous glass fibers, termed spicules. Two classes of sponges, the Hexactinellida and the Demospongiae, possess a siliceous skeleton that is composed of spicules. Studying the large spicules from hexactinellid sponges (>5 cm) revealed that these spicules are effective light-collecting optical fibers. Now we can report that the demosponge, Suberites domuncula, has a biosensor system consisting of the (organic) light producing luciferase and the (inorganic) light transducing silica spicules. The light transmission features of these smaller spicules (200 μm) has been demonstrated and the ability of the sponge tissue to generate light had been proven. Screening for a luciferase gene in S. domuncula was successful. In the next step, we searched for a protein potentially involved in light reception. Such a protein was identified, cloned and recombinantly expressed from S. domuncula. The protein sequence displays two domains characteristic of a cryptochrome, the N-terminal photolyase-related region and the C-terminal FAD-binding domain. The experimental data indicate that sponges may employ a network of luciferase-like proteins, a spicular system and a cryptochrome as the light source, optical waveguide and photosensor, respectively. Finally, we have identified a potential transcription factor involved in the control of the expression of luciferase and cryptochrome, a SOX-related protein. We assume that a flashing light signaling circuit exists, which may control the retinoic acid-induced differentiation of stem cells into pulsating and contracting sponge cells, and into pinacocytes and myocytes. Such a “nervous”-like signal transduction system has not been previously described.