Molecular biology of demosponge axial filaments and their roles in biosilicification

Abstract

For hundreds of years, the skeletal elements of marine and freshwater sponges have intrigued investigators with a diverse array of remarkably complex morphologies. Early studies of demosponge monaxonal megascleres revealed the presence of a central organic axial filament running their entire length. Until recently, however, the precise function of these axial filaments was largely unknown. The spicules from the temperate Eastern Pacific demosponge, Tethya aurantia, comprise approximately 75% of the dry weight of this species, facilitating the large-scale isolation and purification of the biosilica-associated proteins. Silicateins, the most abundant proteins comprising the axial filaments of these spicules, prove to be members of a well-known superfamily of proteolytic and hydrolytic enzymes and can be easily collected after silica demineralization with hydrofluoric acid. Consistent with these findings, the intact filaments are more than simple, passive templates; in vitro, they actively catalyze and spatially direct the hydrolysis and polycondensation of silicon alkoxides to yield silica at neutral pH and low temperature. Catalytic activity also is exhibited by the monomeric subunits obtained by disaggregation of the protein filaments and those produced from recombinant DNA templates cloned in bacteria. These proteins also can be used to direct the polymerization of organosilicon polymers (silicones) from the corresponding organically functionalized silicon alkoxides. Based on these observations, the silicateins are currently being used as models for the design of biomimetic agents with unique catalytic and structure-directing properties. The presence of axial filaments in a diversity of spicule types and the evolutionary implications of these findings are also discussed.

Biological glass fibers: Correlation between optical and structural properties

“…The low-temperature formation of silica in organisms, as an alternative to the hightemperature technological process (24), is a subject of extensive studies (25)(26)(27)(28)(29)(30)(31)(32). It has been shown that proteinaceous axial filaments isolated from the Eastern Pacific demosponge Tethya aurantia and their constituent proteins, silicateins (extracted from the filaments or produced from recombinant DNA templates) were effective in the in vitro induction of hydrolysis and polycondensation of silicon alkoxides to yield silica at ambient temperature and pressure and neutral pH (25,26,(30)(31)(32). Previous work investigating the mechanisms of silicification in diatoms suggested that the formation of silica nanoparticles is directed by specific polycationic peptides, silaffins (27)(28)(29).…”

Co-expression and Functional Interaction of Silicatein with Galectin

“…Major progress in understanding the biochemical mechanism of spicule formation in Demospongiae came from the discovery that silica deposition in T. aurantium is catalyzed by the enzyme silicatein (10,11); silicatein exists in the axial filament around which the first layer(s) of biosilica are formed. The axial filament had been isolated by hydrogen fluoride (HF), 2 which dissolves the biosilica of the spicules.…”

Magnetic resonance imaging of the siliceous skeleton of the demosponge Lubomirskia baicalensis

“…The center of these spicules is formed by an axial canal which contains an axial Wlament (Kaluzhnaya et al, 2005a) composed of silicatein (Kaluzhnaya et al, 2005b), the enzyme that is involved in the polymerization of silica (Cha et al, 1999;Krasko et al, 2000). An earlier study with the sponge Tethya aurantium (Weaver and Morse, 2003) reported that bifurcation of the axial Wlament precisely results in an unusual dichotomous morphology of the spicules. In L. baicalensis the degree of unusually formed spicules is high; often biaxonic (with biaxial Wlaments) or even polyaxonic (polyaxial Wlaments) spicules are found.…”