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

WANG XiaoHong 0 1 FAN XingTao 1 SCHRDER Heinz C 0 MLLER Werner E G 0 0 ERC Advanced Grant Research Group at the Institute for Physiological Chemistry, University Medical Center of the Johannes Gutenberg University , Mainz D-55099, Germany 1 National Research Center for Geoanalysis, Chinese Academy of Geological Sciences , Beijing 100037, China 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 m) 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. - In living organisms 4 major groups of biominerals exist: (1) iron compounds which are primarily restricted to prokaryotes; (2) calcium phosphates found in metazoans; (3) calcium carbonates used by prokaryotes, protozoans, plants, fungi and metazoans; and (4) amorphous silica present in sponges and diatoms. It is surprising that the occurrence of silica as a major skeletal element is restricted to particular unicellular organisms and to sponges (Demospongiae and Hexactinellida). Since the transition from Protozoa to Metazoa dates back to 600 to 1000 million years ago, it has been proposed that the oxygen level, temperature and seawater chemistry played a major role in the evolution from Protozoa to Metazoa [1,2]. In particular, it is postulated that during the period of the appearance of sponges the ocean The Author(s) 2012. This article is published with open access at Springerlink.com was richer in sodium carbonate than in sodium chloride, and that such a soda ocean had probably a pH >9. Under such conditions the concentration of silica, the dioxide form of silicon, in seawater was presumably higher than it is today. Even though these animals, the sponges, comprise the simplest body plan [3], their biomineral structure formation is already highly complex and poorly understood. Like in triploblasts, the diploblastic Porifera skeleton formation also has a pronounced effect on morphogenesis. As an example, if animals grow under unfavorable conditions that do not allow the formation of inorganic deposits (silica or calcium biominerals), the growth of the specimens is heavily suppressed. Silica is the major constituent of sponge spicules in the classes of Demospongiae and Hexactinellida [4,5]. The spicules of these sponges are composed of hydrated, amorphous and non-crystalline silica. The secretion of spicules occurs in Demospongiae in specialized cells, the sclerocytes, in which silica is deposited around an organic filament. If the formation of siliceous spicules is inhibited, the sponge body collapses. The synthesis of spicules is a rapid process with 100 m long megascleres forming within 40 h. Recent studies revealed that the dominant enzyme that catalyzes the formation of monomeric to polymeric silica is silicatein, an enzyme that belongs to the cathepsin subfamily [6,7]. The formation of siliceous spicules in sponges is genetically controlled, and in turn, also the processes ruling morphogenesis [8]. The skeletal framework of the sponges is highly ordered, as clearly observed in the examples of the demosponge Lubomirskia baicalensis [9] and the hexactinellid Monorhaphis chuni [5]. Most siliceous sponges are composed of longer megascleres, >10 m in length, and shorter microscleres (<10 m). 1 Spicule network in sponges: a unique nervous system? Sponges are devoid of a nervous system. We have proposed that the biological function of the siliceous spicules is to act as optical fibers that may substitute for a nerve system [10]. For our initial studies, the hexactinellid sponge species Hyalonema sieboldi was selected, which is characterized by extremely long spicules that form the stalk of the animals. Subsequently, the same function was also proposed for the hexactinellid M. chuni [11]. The first surprising result was that light transmitted through the spicules was cut-off below 600 nm and above 1310 nm, in a similar manner to a combined high/low pass filter [10,11]. From comprehensive studies of luminous genera, which includes organisms that are able to emit light through their bioluminescent systems, it is known that most pelagic deep-sea organisms emit light with emission spectra maxima around 480 nm, whereas those which are terrestrial or live in freshwater produce light with longer wavelengths. Bioluminescence, a widespread phenomenon in nature, is a process in which two molecules of an organism react by the emission of light. 2 Light production in dark aquatic environments Luminous bacteria occur frequently in the aquatic/marine environment and are found as planktonic forms and in symbioses with fish, squid and other organisms [12,13] (Figure 1(a)). In a classic experiment, f (...truncated)