Sponge spicules as blueprints for the biofabrication of inorganic–organic composites and biomaterials

Werner E. G. Mller 0 1 2 3 4 Xiaohong Wang 0 1 2 3 4 Fu-Zhai Cui 0 1 2 3 4 Klaus Peter Jochum 0 1 2 3 4 Wolfgang Tremel 0 1 2 3 4 Joachim Bill 0 1 2 3 4 Heinz C. Schrder 0 1 2 3 4 Filipe Natalio 0 1 2 3 4 Ute Schlomacher 0 1 2 3 4 Matthias Wiens 0 1 2 3 4 0 F.-Z. Cui Department of Materials Science and Engineering, State Key laboratory of New Ceramics and Fine Processing, Tsinghua University , 100084 Beijing, China 1 X. Wang National Research Center for Geoanalysis , 26 Baiwanzhuang Dajie, 100037 Beijing, China 2 J. Bill Materials Synthesis and Microstructure Design, Max-Planck-Institute for Metals Research , Heisenbergstr. 3, 70569 Stuttgart, Germany 3 W. Tremel Institute for Inorganic and Analytical Chemistry, Johannes Gutenberg University , Duesbergweg 10-14, 55099 Mainz, Germany 4 K. P. Jochum Max Planck Institute for Chemistry , J.J. Becherweg 27, 55128 Mainz, Germany 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. 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 Calcareaand forms the basis of the metazoan kingdom (Mller 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 (Mller 2001). Sponges appeared during the Neoproterozoic, the geologic period from 1,000 to 542 Ma (reviewed in Mller 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 VarangerMarinoan 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 (Mller 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 Copes 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 wormlike 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 Mller et al. 2007c). Skeletal elements (spicules) of siliceous sponges, Hexactinellida and Demospongiae, are composed of amorphous opal (SiO2 nH2O). They already existed in pre-Ediacaran sponges and represent a general and basic morphological character until today (Xiao et al. 2000). It is easily conceivable why the animals integrated silicon instead of calcium as the fundamental element for their inorganic skeleton, since the Neoproterozoic oceans were rich in silicic acid and continuously replenished by products of the silicate weathering-carbonate precipitation cycle (Walker 2003). Sponges a (...truncated)