Structure and composition of calcareous sponge spicules: A review and comparison to structurally related biominerals

Since the early 19th century, the skeletons of calcareous sponges (Porifera: Calcarea) with their mineralized spicules have been investigated for their morphologies, structures, and mineralogical and organic compositions. These biomineral spicules, up to about 10 mm in size, with one to four rays called actines, have various specific shapes and consist mainly of magnesium-calcite: in only one case has an additional phase of stabilized amorphous CaCO3 (ACC) been discovered. The spicules are invariably covered by a thin organic sheath and display a number of intriguing properties. Despite their complex morphologies and rounded surfaces without flat crystal faces they behave largely as single crystal individuals of calcite, and to some degree crystallographic orientation is related to morphology. Despite their single-crystalline nature, most spicules show nearly isotropic fracture behaviour, not typical for calcite crystals, indicating enhanced fracture resistance. These unusual morphological and mechanical properties are the result of their mechanism of growth. Each spicule is formed by specialized cells (sclerocytes) that supply mineral ions or particles associated by organic macromolecules to extracellular cavities, where assembly and crystallization in alignment with an initial seed crystal (nucleus) takes place. As a result of discontinuous mineral deposition, cross-sections of larger spicules display concentric layering that mantles a central calcitic rod. On a smaller scale, the entire spicule displays a 'nano-cluster' structure with crystallographically aligned and putatively semicoherent crystal domains as well as a dispersed organic matrix intercalated between domain boundaries. This ultrastructure dissipates mechanical stress and deflects propagating fractures. Additionally, this nano-cluster construction, probably induced by intercalated organic substances, enables the formation of complex crystal morphologies independent of crystal faces. In this review, the current knowledge about the structure, composition, and formation of calcareous sponge spicules is summarised and discussed. Comparisons of calcareous sponge spicules with the amorphous silica spicules of sponges of the classes Hexactinellida and Demospongiae, as well as with calcitic skeletal elements of echinoderms are drawn. Despite the variety of poriferan spicule mineralogy and the distant phylogenetic relationship between sponges and echinoderms, all of these biominerals share similarities regarding their nano-scale construction. Furthermore, echinoderm skeletal elements resemble calcareous sponge spicules in that they represent magnesium-bearing calcite single-crystals with extremely complex morphologies.