Sponge spicules as blueprints for the biofabrication of inorganic–organic composites and biomaterials
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While most forms of multicellular life have developed a calcium-based skeleton, a few specialized organisms complement their body plan with silica. However, of all recent animals, only sponges (phylum Porifera) are able to polymerize silica enzymatically mediated in order to generate massive siliceous skeletal elements (spicules) during a unique reaction, at ambient temperature and pressure. During this biomineralization process (i.e., biosilicification) hydrated, amorphous silica is deposited within highly specialized sponge cells, ultimately resulting in structures that range in size from micrometers to meters. Spicules lend structural stability to the sponge body, deter predators, and transmit light similar to optic fibers. This peculiar phenomenon has been comprehensively studied in recent years and in several approaches, the molecular background was explored to create tools that might be employed for novel bioinspired biotechnological and biomedical applications. Thus, it was discovered that spiculogenesis is mediated by the enzyme silicatein and starts intracellularly. The resulting silica nanoparticles fuse and subsequently form concentric lamellar layers around a central protein filament, consisting of silicatein and the scaffold protein silintaphin-1. Once the growing spicule is extruded into the extracellular space, it obtains final size and shape. Again, this process is mediated by silicatein and silintaphin-1, in combination with other molecules such as galectin and collagen. The molecular toolbox generated so far allows the fabrication of novel micro- and nanostructured composites, contributing to the economical and sustainable synthesis of biomaterials with unique characteristics. In this context, first bioinspired approaches implement recombinant silicatein and silintaphin-1 for applications in the field of biomedicine (biosilica-mediated regeneration of tooth and bone defects) or micro-optics (in vitro synthesis of light waveguides) with promising results.
KeywordsBiosilica Silicatein Silintaphin-1 Biomaterials Porifera Sponges Biomedicine Biotechnology
Sponges are aquatic, sessile, multicellular organisms with a Bauplan that appears simple at a first glance and lacks similarities to any other living organism. Therefore, during early studies, it was difficult to determine morphological characters that would conclusively allow to group sponges into either one of two kingdoms of multicellular life: Metazoa or Plantae. In an early attempt to reconcile different views, sponges had been classified as “Zoophyta” (Donati 1753) or “Thierpflanzen” (Pallas 1787). Later on, the discovery of significant morphological similarities on the cellular level, i.e., between a highly differentiated poriferan cell type (choanocytes) and unicellular flagellate eukaryotes (choanoflagellates), established a close relationship between the phyla Porifera and Choanozoa (Afzelius 1961; Salvini-Plawen 1978). Recently, phylogenomic analyses also confirmed a significant evolutionary relatedness to the Placozoa. This phylum consists of only one species, which is even simpler in structure than any poriferan species (Blackstone 2009). However, whether Placozoa are highly simplified eumetazoans or a sister taxon to all other metazoans remains controversial until today. It was Grant who first grouped sponges into a common taxon, termed “phylum Porifera” (Grant 1833), initially comprising only sessile marine animals with a soft and spongy (amorphously shaped) body. However, with the discovery of glass sponges (class Hexactinellida; Schmidt 1870), this definition was broadened to include “most strongly individualized, radially symmetrical” entities (Hyman 1940). Finally, after comprehensive isolation, cloning, and phylogenetic analyses of many poriferan genes, it became obvious that the phylum Porifera comprises three classes—Hexactinellida, Demospongiae, and Calcarea—and forms the basis of the metazoan kingdom (Müller 1995). A few years later, it could be clarified that Hexactinellida (glass sponges), Demospongiae (silicate/spongin sponges), and Calcarea (calcareous sponges) are monophyletic and closely related to the common ancestor of all metazoans, the Urmetazoa (Müller 2001).
Sponges appeared during the Neoproterozoic, the geologic period from 1,000 to 542 Ma (reviewed in Müller et al. 2007c). Fossil records indicate that during this period, also other multicellular animals existed, which, however, became extinct (Knoll and Carroll 1999), especially during the Varanger–Marinoan ice ages (605 to 585 Ma). Two major reasons contributed to the evolutionary success of the poriferan taxon: (a) symbiosis with microorganisms and (b) presence of hard skeletons (Müller et al. 2007c). The maintenance of symbiotic relationships with unicellular organisms allowed sponges to survive adverse environmental conditions because the autotrophic microbial symbionts represented rich organic carbon sources. On the other hand, the development of skeletal elements facilitated an increase in size, a common metazoan phyletic trend also known as Cope’s rule (Nicol 1966): Since changes in body size affect almost every aspect of life (Schmidt-Nielsen 1984), two strategies have been developed in animals to circumvent any constraints (reviewed in Page 2007), first by acquisition of a hydrostatic skeleton, as it is known from the “worm”-like phyla of the Ediacara and pre-Ediacara Eon (Xiao and Kaufman 2006), or second by acquisition of rigid solid skeletal elements (Alexander et al. 1979; Biewener 2005), as they were realized in Neoproterozoic siliceous sponges (see Müller et al. 2007c).
During animal evolution, biomolecules (e.g., secondary metabolites) and biomaterials (e.g., biominerals) were selected for higher biological efficiency and superior physical properties. Scheuer (1987) and Baker and Murphy (1981) were pioneers in exploiting secondary metabolites for biomedical applications. They conclusively outlined strategies to discover and apply such compounds for biomedical use, resulting in the development of 9-β-d-arabinofuranosyladenosine (ara-A) as a first active pharmaceutical ingredient (Müller et al. 1977). On the other hand, the fundament for the biotechnological exploitation of biominerals has been laid by Lowenstam and Weiner (1989), who introduced the conceptual framework for understanding the formation of inorganic deposits within organisms. In this context, the fundamental importance of organic macromolecules during biomineralization was highlighted.
In contrast, for initiation and maintenance of biomineral formation, bioseeds and/or organic surfaces and matrices are required; for these reactions, inorganic [e.g., phosphate] or organic precursors [β-glycerophosphate] are used as donors. Weiner and Dove (2003) distinguished two categories of mineralization: (a) biologically induced mineralization and (b) biologically controlled mineralization. (a) During the seed phase of biologically induced mineralization processes, organic polymers allow controlled nucleation and crystal growth. For example, marine snow (three-dimensional organic/mineral meshwork; Leppard 1999) and coccoliths/coccospheres (calcitic remains of coccolithophorids [single-celled algae]) have mineralization activity. The latter one has recently been implied in the formation of ferromanganese crusts in the deep sea (Wang and Müller 2009a, b; Fig. 2B). These particles/aggregates act as bioseeds and mediate deposition of inorganic materials from an environment that contains the inorganic precursors at nonsaturated conditions. (b) Biologically controlled mineralization describes a process that is guided along bioseeds and organic matrices (organic guiding macromolecules; Fig. 2C). These biomolecules control initiation and growth of biominerals, morphology, and speed of the mineralization process. Biominerals represent genuine composite materials, formed from the inorganic “polymer”/mineral and the organic component (protein, polysaccharide, glycoprotein). These organic molecules function as bioseeds (during seed phase) and also as scaffold during the subsequent growth phase. This widely occurring process takes place within the living system (e.g., mammalian teeth or bone formation) or extracellularly (e.g., foraminiferan CaCO3 shells; see Lowenstam and Weiner 1989).
A special form of biologically controlled mineralization (i.e., enzymatically controlled; Fig. 2D) has been described for the biosilicification process in siliceous sponges (see Müller et al. 2007d). In these animals (Demospongiae and Hexactinellida), the enzyme silicatein is catalytically involved in the formation of biosilica (Cha et al. 1999; Müller et al. 2005; 2007d), concurrently serving as organic scaffold for the inorganic polysilicate mineral product (Müller et al. 2008a; Wang et al. 2008). Hence, it acts as both bioseed and organic matrix. Since then, learning from sponges and mastering nature’s concept of forming siliceous skeletal elements inspired many strategies that aim to biofabricate minerals with exquisite and distinguished (bio)chemical and (bio)physical properties (Mayer 2005). Additionally, the discovery of organic molecules that are implicated in the formation of inorganic polymers caused a paradigm shift in biomaterials science and technology. While silicatein might facilitate the synthesis of new biomaterials (e.g., for dental applications or tissue engineering), an additional protein, silintaphin-1, provides the products of the silicatein-mediated reactions with defined morphologies.
Silicatein-based spicule formation
The biogenic basis of spicule formation and the turnover of silica in spicules have already been depicted by Duncan (1881). He formulated “The spicule which has lived, has to decay, and may live again in another form”. However, it took until 1999 until Cha et al. discovered that the main constituent of the proteinaceous filament within the axial canal of spicules is an enzyme, subsequently termed silicatein, which might be involved in biosilica formation. Soon after having identified this anabolic enzyme, also the corresponding catabolic enzyme (silicase) was discovered (Schröder et al. 2003). The identification of a biosilica degrading enzyme supported the view that the siliceous components in spicules are under metabolic turnover (Eckert et al. 2006). Studies on the metabolism of spicules on the cellular level became possible after the introduction of a poriferan cell culture system, primmorphs (Imsiecke et al. 1995; Custódio et al. 1998). Already the first contribution on that topic resolved that spicule formation starts intracellularly in “J” sclerocytes, by formation of an initial organic axial filament, around which the inorganic silica mantel is deposited. This result had later been corroborated by application of more advanced immunochemical and electron microscopy techniques (Müller et al. 2007e).
The difficult accessibility of hexactinellids, which live primarily in depths of more than 300 m, generally results in a very poor sampling. Accordingly, only recently the first hexactinellid silicatein (Crateromorpha meyeri) could be identified and characterized (Müller et al. 2008c). This molecule shares high similarity to the demosponge sequences (expect value of 8e−58) and contains the same catalytic triad amino acids. However, striking in the C. meyeri sequence is a second Ser-rich cluster, which is located between the second and the third aa of the catalytic triad. Strong binding of the protein to the spicule silica surface has been attributed to this cluster (Müller et al. 2008a).
The posttranslational modifications of silicatein have been found to be essential for the enzyme activity with respect to (a) association with other structural and functional molecules within the tissue and (b) self-association/self-assembly. For those studies, silicatein had been isolated from spicules in the absence of HF, but in the presence of a glycerol-based buffer. Following this rationale, it could be demonstrated that silicatein exists not only in the axial canal but also in the extraspicular and extracellular space (Müller et al. 2005; Schröder et al. 2006). The enzymatic reaction mechanism of silicatein had been proposed by Cha et al. (1999); the detailed properties of the reaction kinetics have been specified experimentally (Müller et al. 2008b).
- (a)Intracellular phase (initial growth): It could be demonstrated that silicic acid is actively taken up by cells [sclerocytes] via the Na+/HCO 3 − [Si(OH)4] cotransporter (Schröder et al. 2004). In parallel, mature silicatein is synthesized/processed and subsequently deposited together with silicic acid in special organelles of the sclerocytes, the silicasomes. Within silicasomes axial filaments are formed around which silica is subsequently deposited enzymatically (Fig. 4A, B). After formation of a first layer (or a few layers), juvenile spicules are released into the extracellular space, where they grow in length and diameter by appositional layering of silica lamellae (Müller et al. 2005; Fig. 4C). There, spicules obtain their final shape, e.g., S. domuncula tylostyles are characterized by a terminal globular swelling (Fig. 4D, E).
Extracellular phase (consecutive appositional growth): Silicatein is present in an enzymatically active form in the extracellular space (Müller et al. 2005). There, silicatein molecules are organized to larger entities as demonstrated by immunogold electron microscopic analysis. These molecules are arranged along filamentous strings, which are organized concentrically to the spicule surface (Schröder et al. 2006; Fig. 4C) and consist of the protein galectin that oligomerizes in the presence of Ca2+. Within this organic cylinder that enfolds the growing spicule, the siliceous mantel grows stepwise, by appositional layering of lamellae. Not only centrifugal growth (“thickening”) but also axial growth (“elongation”) of spicules is driven by extraspicular silicatein. Thus, the accumulation of silicatein at the tip of growing spicules can be visualized immunochemically by transmission electron microscopy (TEM) analyses (Fig. 4B). In the extracellular space, both axial and radial growth of the spicules is driven by silicatein that surrounds the surface of the already existing silica lamellae (Fig. 4C-a–C-d). In hexactinellids, appositionally layered silica lamellae can reach 1,000 in number (Wang et al. 2009). However, in demosponges, the individual lamellae fuse and form a “solid” siliceous shell, which surrounds the axial filament (Fig. 4C-e).
- (c)Extracellular phase (final morphogenesis): So far, the processes described above do not explain the species-specific shaping of spicules. This final step of spiculogenesis (i.e., morphogenesis) still remains mysterious. However, since spicules of both demosponges (e.g., S. domuncula, Eckert et al. 2006) and hexactinellids (e.g., M. chuni, Müller et al. 2008d) are surrounded or even embedded into a fibrous network of collagen and other proteins (see below), it is safe to assume that these molecules (released by specialized sponge cells) provide a scaffold within which the galectin-containing strings are organized (Fig. 5). Data suggest that the galectin-containing strings are organized by collagen fibers to net-like structures (Schröder et al. 2006). Those fibers that are released by the specialized cells, the collencytes, provide the organized platform for the morphogenesis of the spicules. The longitudinal growth of the spicules can be explained by the assumption that at the tips of the spicules, the galectin/silicatein complexes are incorporated into deposited biosilica under formation and elongation of the axial canal.
Silica deposition in spicules
A comprehensive summary of the physical and chemical analyses of poriferan siliceous spicules has been given by Sandford (2003). It is summarized that in both classes of siliceous sponges, the inorganic matrix is almost indistinguishable and comprises amorphous opal, which contains traces of other elements. Weaver et al. (2003) conclusively demonstrated that in spicules of the demosponge T. aurantium, silica nanoparticles, with a mean diameter of 75 nm, are arranged along alternating layers. This pattern had been exposed after etching of spicular cross sections. It was concluded that the annular layering may be related to variations in the degree of silica condensation, rather than variability in the inclusion of organics. Nevertheless, a proteinaceous coat, immunoreacting with silicatein antibodies, can be released by HF treatment from spicules S. domuncula (Fig. 3). Similarly, the exact localization of proteins within the lamellar organization of hexactinellid spicule remains to be determined. While Woesz et al. (2006) provided evidence by Raman spectroscopy for the existence of proteins between siliceous layers (organic interlayers in M. chuni), high resolution scanning electron microscopy (HR-SEM) and biochemical determinations suggest that proteins are localized within the silica depositions (Müller et al. 2008d). Nonetheless, the unusual combination of mechanical properties, such as strength, stiffness, and toughness observed in hexactinellid spicules, is based on the proteinaceous components enfolded within (Mayer 2005).
The silicatein interactor silintaphin-1
In order to obtain the molecular tools required to enzymatically generate composite materials with defined characteristics, a comprehensive screening program was started for proteins that mediate in combination with silicatein spiculogenesis. By application of a yeast two-hybrid system, a poriferan (S. domuncula) cDNA library was successfully screened for a silicatein-binding protein involved in spiculogenesis. Thus, a first strong silicatein interactor was identified and subsequently termed silintaphin-1 (Wiens et al. 2009). The existence of this 42.5-kDa silicatein interactor (386 aa) is restricted to sponges. Since it shows no sequence similarities to any other known proteins, silintaphin-1 probably represents the prototypic member of a new family. However, the protein reveals significant similarities along a stretch of ca. 110 aa to the pleckstrin homology (PH) domain, a common protein interaction domain that occurs in many unrelated proteins. PH domains usually form a structure that can serve as scaffold for presenting different types of binding sites (Lemmon and Ferguson 2000; Lemmon 2004). In silintaphin-1, the PH domain likely facilitates binding to silicatein and consequently assists assembly of the axial filament. Furthermore, it is flanked on both sides by several nearly identical aa sequence repeats rich in Pro and charged/polar residues (Glu, Asp, Thr). This combination of repeated sequence composition and ligand-binding domain is also found in titin (connectin), a filamentous protein of sarcomers with unique elastic properties and distinct bending rigidities (Trombitas et al. 1998). In analogy, silintaphin-1 hence might convey a similar elasticity and flexibility required during spiculogenesis.
Silintaphin-1 expression was observed to be significantly upregulated in regenerating S. domuncula tissue that requires profound synthesis of spicules and/or reorganization of the skeletal elements. Furthermore, the expression was also susceptible to the silicon concentration in the surrounding aquatic medium, indicating that silintaphin-1 is tightly interwoven in the pathways of poriferan silicon metabolism and spiculogenesis.
Subsequently, antibodies were raised against the poriferan protein, to elucidate its localization in sponge tissue. In situ detection of silicatein with labeled antibodies was already performed earlier, confirming the presence of the enzyme in axial filaments (Müller et al. 2005). However, recent analyses by confocal laser scanning microscopy conclusively demonstrated the almost exclusive colocalization of silintaphin-1 (fluorescein isothiocyanate-labeled antibodies; Fig. 8D) and silicatein (Cy3-labeled antibodies; Fig. 8E) within both a substantial layer surrounding spicules and the axial filament (Fig. 8F; merge). Interestingly, within the axial filament silintaphin-1 forms a core structure that is enfolded by silicatein. The general colocalization with silicatein suggests that silintaphin-1 contributes not only to the filament formation but also to the determination of the final spicular morphology.
Biomedical/biotechnological application of silicatein and silintaphin-1
First attempts to evaluate the biomedical application of silicatein/biosilica for treatment of bone/tooth defects and dental care are promising. Thus, during a reaction of silicatein with the substrate sodium metasilicate, nanoscale biosilica layers (50–150 nm) were formed on dental (pig teeth; Fig. 10C, D) and bone hydroxyapatite (rat femurs; Fig. 10E, F; HR-SEM). This data pave the way for biomedical approaches that aim, e.g., to generate protective biosilica layers on teeth (reducing the risk of bacterial induced caries/cavities) or to regenerate bone tissue via biosilica-stimulated activity of mineralizing cells (resulting in an increased deposition of hydroxyapatite).
In poriferan cells, spiculogenesis is initiated by the synthesis of the axial filament around which silica nanoparticles assemble to form a compact concentric layer. In a further biomimetic approach, this process was reconstructed in vitro. For that purpose, amorphous silica nanoparticles (diameter 20 nm) were coincubated with refolded recombinant silicatein (1 h, RT). Fourier transform infra-red spectroscopy with attenuated total reflectance (FT-IR ATR) and immunoblot analyses confirmed the adsorption of the enzyme onto the nanoparticles’ surfaces even after several washing steps, indicative of the significant binding capacity of silicatein to amorphous silica. Subsequent incubation of the silica/protein complexes with native silintaphin-1 resulted in the formation of structures with spicular to rod-like morphology (200–400 nm in width, >2 μm in length), thus revealing the cross-linking capacities of silintaphin-1 (Fig. 11B). This visual inspection by TEM was corroborated by FT-IR ATR and Western blot analyses that demonstrated a strong interaction of silintaphin-1 with adsorbed silicatein (Wiens et al., in preparation). In controls, lacking silintaphin-1, no assembly of nanoparticles was observed.
In a variation of this experiment, the silica nanoparticles were exchanged by γ-Fe2O3 nanocrystals (diameter 8–10 nm) that had been surface-functionalized with the reactive polymer poly(pentafluorophenyl acrylate) and chemisorbed Ni2+-NTA to facilitate binding of recombinant, His-tagged silicatein (Tahir et al. 2006; Wiens et al. 2009). Neither functionalized (carrying silicatein) nor unmodified did the particles assemble to regular structures. However, coincubation of functionalized silicatein-binding γ-Fe2O3 nanocrystals with silintaphin-1 resulted once more in the formation of rod-like structures with clear-cut edges (Fig. 11C).
During the aforementioned experimental variations, inorganic nanoparticulate carriers were employed to immobilize silicatein. In an alternative approach, nanoparticles were omitted. Instead, equimolar concentrations of silintaphin-1 and silicatein were coincubated for 30 min (RT) to induce protein–protein interaction. Then, the titania alkoxide precursor titanium bis-(ammonium-lactato)-dihydroxide was added (100 μM) for 1 h (RT). This monomeric alkoxide precursor was recently employed to generate nanostructured biotitania during a reaction that was mediated by surface-immobilized silicatein (Tahir et al. 2005). In this alternative approach, the combination of silicatein and silintaphin-1 not only induced the formation of titania nanoparticles but also resulted in their assembly to spicular structures, resembling those composed of silica or γ-Fe2O3 in size and shape (Fig. 11D). Consequently, silintaphin-1 forms the basis for in vitro synthesis of tailored materials since it facilitates (a) the generation of polymer products without prior surface immobilization of silicatein and (b) the assembly of nanoparticles (including enzymatic nanoparticulate products) to ordered structures.
Natural sponge spicules can act as optical glass fibers that transmit light with high efficiency (Müller et al 2006), as initially described by Cattaneo-Vietti et al. (1996). In addition, transmission of light is very selective since only wavelengths between 615 and 1,310 nm can pass through the spicules (sharp high- and low-pass filters). Spicules comprise a high refractive index core, a surrounding low-refractive-index cylindrical tube, and an outer portion with a progressively increasing refractive index. These optical characteristics of spicules are complemented by surprising mechanical properties based on the composite structure, lamellar architecture, and presence of dopants. Thus, spicules revealed enhanced fracture toughness (Sundar et al 2003; Aizenberg et al. 2004). Accordingly, it is tempting to employ the directed assembly of silica nanoparticles by the combined action of silicatein and silintaphin-1 to fabricate light-guiding micro- and nanostructured composites that represent an economical alternative to industrial glass fibers currently used in micro-optical approaches.
This work was supported by grants from the German Bundesministerium für Bildung und Forschung (project “Center of Excellence BIOTECmarin”), the International Human Frontier Science Program, the European Commission (project no. 031541—Biomineralization for lithography and microelectronics (BIO-LITHO)), the consortium BiomaTiCS at the Universitätsmedizin of the Johannes Gutenberg-Universität Mainz, and the International S & T Cooperation Program of China (grant no. 2008DFA00980).
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