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Flashing Light in Sponges Through Their Siliceous Fiber Network: a New Strategy of “Neuronal Transmission” in Animals

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Flashing Light in Sponges Through Their Siliceous Fiber Network: a New Strategy of “Neuronal Transmission” in Animals View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Springer - Publisher Connector Article SPECIAL TOPIC September 2012 Vol.57 No.25: 33003311 Omics in Marine Biotechnology doi: 10.1007/s11434-012-5241-9 SPECIAL TOPICS: Flashing light in sponges through their siliceous fiber network: A new strategy of “neuronal transmission” in animals WANG XiaoHong1,2*, FAN XingTao1, SCHRÖDER Heinz C2 & MÜLLER Werner E G2* 1 National Research Center for Geoanalysis, Chinese Academy of Geological Sciences, Beijing 100037, China; 2 ERC Advanced Grant Research Group at the Institute for Physiological Chemistry, University Medical Center of the Johannes Gutenberg University, Mainz D-55099, Germany Received November 7, 2011; accepted April 20, 2012; published online July 11, 2012 Sponges (phylum Porifera) represent a successful animal taxon that evolved prior to the Ediacaran-Cambrian boundary (542 mil- lion 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 miss- ing 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 gener- ate light had been proven. Screening for a luciferase gene in S. domuncula was successful. In the next step, we searched for a pro- tein 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 identi- fied a potential transcription factor involved in the control of the expression of luciferase and cryptochrome, a SOX-related pro- tein. 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. sponges, Suberites domuncula, “nervous”-like signal system, light transmission, siliceous spicules, luciferase, cryptochrome Citation: Wang X H, Fan X T, Schröder H C, et al. Flashing light in sponges through their siliceous fiber network: A new strategy of “neuronal transmission” in animals. Chin Sci Bull, 2012, 57: 33003311, doi: 10.1007/s11434-012-5241-9 In living organisms 4 major groups of biominerals exist: (1) silica as a major skeletal element is restricted to particular iron compounds which are primarily restricted to prokary- unicellular organisms and to sponges (Demospongiae and otes; (2) calcium phosphates found in metazoans; (3) cal- Hexactinellida). Since the transition from Protozoa to Met- cium carbonates used by prokaryotes, protozoans, plants, azoa dates back to 600 to 1000 million years ago, it has fungi and metazoans; and (4) amorphous silica present in been proposed that the oxygen level, temperature and sea- sponges and diatoms. It is surprising that the occurrence of water chemistry played a major role in the evolution from Protozoa to Metazoa [1,2]. In particular, it is postulated that *Corresponding authors (email: [email protected]; [email protected]) during the period of the appearance of sponges the ocean © The Author(s) 2012. This article is published with open access at Springerlink.com csb.scichina.com www.springer.com/scp Wang X H, et al. Chin Sci Bull September (2012) Vol.57 No.25 3301 was richer in sodium carbonate than in sodium chloride, and molecules of an organism react by the emission of light. that such a “soda ocean” had probably a pH >9. Under such conditions the concentration of silica, the dioxide form of 2 Light production in dark aquatic silicon, in seawater was presumably higher than it is today. Even though these animals, the sponges, comprise the environments simplest body plan [3], their biomineral structure formation is already highly complex and poorly understood. Like in Luminous bacteria occur frequently in the aquatic/marine triploblasts, the diploblastic Porifera skeleton formation also environment and are found as planktonic forms and in sym- has a pronounced effect on morphogenesis. As an example, bioses with fish, squid and other organisms [12,13] (Figure if animals grow under unfavorable conditions that do not 1(a)). In a classic experiment, fish kept for 1 to 2 d in the allow the formation of inorganic deposits (silica or calcium open are shown to have been settled by bacteria. Colonies biominerals), the growth of the specimens is heavily sup- of luminous bacteria start to grow and can be photographed pressed. Silica is the major constituent of sponge spicules in to show the production of their own light (Figure 1(a)). This the classes of Demospongiae and Hexactinellida [4,5]. The visible light is made by living organisms, and hence this spicules of these sponges are composed of hydrated, amor- light quality was termed as bioluminescence. On land this phous and non-crystalline silica. The secretion of spicules phenomenon is rarely seen, with fireflies representing the occurs in Demospongiae in specialized cells, the sclerocytes, best-known terrestrial example of living light. In contrast, in in which silica is deposited around an organic filament. If the ocean bioluminescence is very common in pro- and eu- the formation of siliceous spicules is inhibited, the sponge karyotic organisms ranging in sizes from microns to meters, body collapses. The synthesis of spicules is a rapid process and from autotrophs, herbivores to carnivores. Biolumines- with 100 μm long megascleres forming within 40 h. Recent cence as a form of chemiluminescence is well known, studies revealed that the dominant enzyme that catalyzes the where the reaction chemicals are produced by living organ- formation of monomeric to polymeric silica is silicatein, an isms. The names assigned to these organic chemicals are enzyme that belongs to the cathepsin subfamily [6,7]. The luciferin for the substrate and luciferase for the enzyme. formation of siliceous spicules in sponges is genetically Bioluminescence light allows these organisms to passively controlled, and in turn, also the processes ruling morpho- attract or actively repel commensalic organisms. However, genesis [8]. The skeletal framework of the sponges is highly it has never been proposed that light is also a signal con- ordered, as clearly observed in the examples of the ductor within an organism. In the ocean, blue light can pen- demosponge Lubomirskia baicalensis [9] and the hexacti- etrate deepest (Figure 1(c)) and the relief area can be re- nellid Monorhaphis chuni [5]. Most siliceous sponges are solved on the basis of different intensities of a blue color. If composed of longer megascleres, >10 μm in length, and the same area is photographed with a flash, a bright scale of shorter microscleres (<10 μm). colors becomes visible (Figure 1(d)). By checking adaptation of organisms in the dark, two light qualities are distinguished: bioluminescence and bio- 1 Spicule network in sponges: a unique nervous fluorescence. This can be strikingly seen in animals that live system? in absolute darkness, e.g., in caves. The “grottenolm”, the hypogean salamander Proteus anguinus, is an example who Sponges are devoid of a nervous system. We have proposed lives in the Adriatic karst caves and is blind. However, after that the biological function of the siliceous spicules is to act illumination with a daylight flash the biofluorescent signals as optical fibers that may substitute for a nerve system [10]. arising from the pigment (hemoglobin) of the almost trans- For our initial studies, the hexactinellid sponge species Hy- parent reptile become apparent (Figure 1(b)). The fluores- alonema sieboldi was selected, which is characterized by cence of animals under these conditions has no function for extremely long spicules that form the stalk of the animals. the behavior of the animals in the dark [14]. A different Subsequently, the same function was also proposed for the function of this bio-phenomenon can be attributed to the hexactinellid M. chuni [11]. The first surprising result was biofluorescence seen in other aquatic organisms. In corals that light transmitted through the spicules was cut-off
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