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Formation of Giant Spicules in the Deep-Sea Hexactinellid Monorhaphis Chuni (Schulze 1904): Electron-Microscopic and Biochemical Studies

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Formation of Giant Spicules in the Deep-Sea Hexactinellid Monorhaphis Chuni (Schulze 1904): Electron-Microscopic and Biochemical Studies Cell Tissue Res (2007) 329:363–378 DOI 10.1007/s00441-007-0402-x REGULAR ARTICLE Formation of giant spicules in the deep-sea hexactinellid Monorhaphis chuni (Schulze 1904): electron-microscopic and biochemical studies Werner E. G. Müller & Carsten Eckert & Klaus Kropf & Xiaohong Wang & Ute Schloßmacher & Christopf Seckert & Stephan E. Wolf & Wolfgang Tremel & Heinz C. Schröder Received: 25 November 2006 /Accepted: 19 February 2007 / Published online: 4 April 2007 # Springer-Verlag 2007 Abstract The siliceous sponge Monorhaphis chuni (Hexa- spicules; it harbors the axial filament and is surrounded by ctinellida) synthesizes the largest biosilica structures on an axial cylinder (100–150 μm) of electron-dense homo- earth (3 m). Scanning electron microscopy has shown that geneous silica. During dissolution of the spicules with these spicules are regularly composed of concentrically hydrofluoric acid, the axial filament is first released arranged lamellae (width: 3–10 μm). Between 400 and 600 followed by the release of a proteinaceous tubule. Two lamellae have been counted in one giant basal spicule. An major proteins (150 kDa and 35 kDa) have been visualized, axial canal (diameter: ~2 μm) is located in the center of the together with a 24-kDa protein that cross-reacts with antibodies against silicatein. The spicules are surrounded by a collagen net, and the existence of a hexactinellidan Carsten Eckert was previously with the Museum für Naturkunde, collagen gene has been demonstrated by cloning it from Invalidenstrasse 43, 10115 Berlin, Germany. Aphrocallistes vastus. During the axial growth of the The collagen sequence from Aphrocallistes vastus reported here, viz., spicules, silicatein or the silicatein-related protein is [COL_APHRO] APHVACOL (accession number AM411124), has been deposited in the EMBL/GenBank data base. proposed to become associated with the surface of the spicules and to be finally internalized through the apical This work was supported by grants from the European Commission, opening to associate with the axial filament. Based on the the Deutsche Forschungsgemeinschaft, the Bundesministerium für Bildung und Forschung Germany (project: Center of Excellence data gathered here, we suggest that, in the Hexactinellida, BIOTECmarin), the National Natural Science Foundation of China the growth of the spicules is mediated by silicatein or by a (grant no. 50402023), and the International Human Frontier Science silicatein-related protein, with the orientation of biosilica Program. deposition being controlled by lectin and collagen. * : : : : W. E. G. Müller: ( ) C. Eckert K. Kropf U. Schloßmacher C. Seckert H. C. Schröder Keywords Spicules . Silica formation . Silicatein-related Institut für Physiologische Chemie, Abteilung Angewandte . Molekularbiologie, Universität Mainz, protein Hexactinellida Monorhaphis chuni (Porifera) Duesbergweg 6, 55099 Mainz, Germany e-mail: [email protected] Introduction URL: http://www.biotecmarin.de/ The phylum Porifera (sponges) has been subdivided into X. Wang three classes, viz., the Hexactinellida, Demospongiae, and National Research Center for Geoanalysis, 26 Baiwanzhuang Dajie, Calcarea, whereby the first two taxa comprise individuals 100037 Beijing, China with a siliceous skeleton composed of spicules, and : members of the last-mentioned taxon have calcareous S. E. Wolf W. Tremel (calcium carbonate) skeletal elements. Based on molecular Institut für Anorganische Chemie, Universität Mainz, Duesbergweg 10–14, biological (Kruse et al. 1997) and geological (Reitner and 55099 Mainz, Germany Wörheide 2002) studies, the Hexactinellida taxon has been 364 Cell Tissue Res (2007) 329:363–378 established as the oldest, having evolved between Neo- two subclasses: the Hexasterophora and Amphidiscophora proterozoic glaciations (720–585 Ma), sometimes referred (for a review, see Reiswig 2006). In the latter subclass, to as “snowball” Earth (for a review, see Corsetti et al. amphidiscs are the (main) microscleres and never fuse. One 2006). During this period, a cycle of silicate weathering and member of this subclass is the family Monorhaphididae, carbonate precipitation, prior to or simultaneously with the which includes three described species: Monorhaphis glaciations, has been proposed to have resulted in the chuni, M. dives, and M. intermedia. Since the discovery dissolution of surface rocks composed of insoluble silicates of these sponges during the first German deep-sea (CaSiO3). Subsequently, soluble calcium carbonate (CaCO3) expedition (RV “Valdivia”) and the first descriptions of and soluble silica (SiO2) was formed by reaction with these animals by Chun (1900) and Schulze (1904), only atmospheric CO2 (Walker et al. 1981). In consequence, the little additional information has been added regarding the level of dissolved silicic acid in seawater increased providing form and construction of their skeletal systems. Nothing has the inorganic starting material for the formation of siliceous been published concerning the synthesis of their giant spicules. Physical and chemical analyses have revealed that spicules. Worldwide, M. chuni has been documented only the siliceous skeletons of the two siliceous sponge classes are at a few sampling sites (Tabachnick 2002), suggesting a composed of amorphous silica with a water content of distribution in the deep sea in the Indian Ocean and in the around 10% (Sandford 2003). Analysis of infrared spectra West Pacific. One outstanding feature of Monorhaphis is its have shown a distinct difference between the two taxa of anchoring spicule, which can reach lengths of up to 3 m between 1,080 and 1,100 cm−1 suggesting a different with a maximum diameter of 8.5 mm (Schulze 1904). M. molecular configuration involving the Si-O-Si linkage chuni thus produces the largest biosilica structure known on (Sandford 2003). Other than silicic acid, only small Earth. Polished cross sections confirm the existence of up amounts of trace elements (<3%) are found in the spicules. to 500 highly regular concentric rings that are arranged During the past few years, some aspects of the mechanism around a 150-μm-thick less-structured core (Schulze 1904). of spicule formation in Demospongiae have been clarified. In the middle of this core, a square axial channel with a Work mainly with Tethya aurantium (Shimizu et al. 1998; proteinaceous filament of approximately 2 μm in thickness Cha et al. 1999)andSuberites domuncula (Krasko et al. is visible running through the entire spicule from one end to 2000) has established that, in contrast to silica deposition in the other. The concentric rings around this core have nearly other organisms (e.g., in diatoms), biosilica formation in constant thickness in all samples, but this thickness varies sponges is mediated enzymatically via the enzyme among sampling locations; for example, from the Somalia silicatein. Silicatein forms the axial filament of the basin, silica strata are 8–10 μm in thickness, whereas those spicules from which the growth of the spicules starts from the Madagascar basin are 3–5 μm thick. intracellularly (Shimizu et al. 1998;Mülleretal.2003, Recently, Aizenberg et al. (2005) have published a 2005;WangandWang2006). Although marine sponges detailed structural analysis of the spicule formation in the contain two isoforms of silicatein at least, freshwater hexactinellid Euplectella.Theyhavedemonstratedstructural sponges contain up to five silicatein isoforms, indicating hierarchies of spicule synthesis starting from the nanometer- the more complex formation and organization of the sized particles of silica to the final mature spicules. The spicules in these animals (Müller et al. 2006). In S. composition of the proteins that are associated with and domuncula, and probably also in other Demospongiae, found within the spicules has not been described. In a recent spicule formation starts intracellularly. After reaching a study, Ehrlich et al. (2005) dissolved the basal spicules of the size of approximately 6–8 μm, the macroscleres (spicules hexactinellid Hyalonema sieboldi in 2.5 M NaOH at 30°C for of >10 μm) are extruded from the cells (sclerocytes) and 14 days and were able to show that the abundant structural completed extracellularly, where they may reach lengths of protein associated with the spicules was probably collagen over 100 μm (Müller et al. 2005). In the extracellular with an Mr of around 130 kDa. However, whether degradation space, both the final longitudinal size and the final of the collagen fibrils occurred during the dissolution of silica thickness of the spicules are reached by appositional with NaOH remained unclear. In continuation of these studies, growth (Müller et al. 2006). These processes are mediated we have analyzed the protein composition of the spicule- by silicatein and controlled by galectin, which acts as an associated protein(s) in the spicules of M. chuni and M. organic matrix for the attachment of silicatein molecules intermedia; the results are presented here. (Schröder et al. 2006). Collagen probably provides the We present a microscopic analysis of the spicules from M. structural groove along which the galectin-silicatein chuni with major emphasis on the giant spicules (giant basal strings are guided, thus allowing the formation of the spicules or basalia: 1 m) and also the large comitalia intricately architectured spicules (Eckert et al. 2006). (~60 mm). This is followed by an examination of the organic The monophyletic group of Hexactinellida is, according components of these spicules,
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