Shaping highly regular glass architectures: A lesson from nature

Abstract

Demospongiae is a class of marine sponges that mineralize skeletal elements, the glass spicules, made of amorphous silica. The spicules exhibit a diversity of highly regular three-dimensional branched morphologies that are a paradigm example of symmetry in biological systems. Current glass shaping technology requires treatment at high temperatures. In this context, the mechanism by which glass architectures are formed by living organisms remains a mystery. We uncover the principles of spicule morphogenesis. During spicule formation, the process of silica deposition is templated by an organic filament. It is composed of enzymatically active proteins arranged in a mesoscopic hexagonal crystal-like structure. In analogy to synthetic inorganic nanocrystals that show high spatial regularity, we demonstrate that the branching of the filament follows specific crystallographic directions of the protein lattice. In correlation with the symmetry of the lattice, filament branching determines the highly regular morphology of the spicules on the macroscale.

Fig. 1. The morphology of demosponge spicules and their inner axial filaments as revealed by scanning electron microscopy.

(A) Megascleres from the demosponge T. aurantium. Scale bar, 100 μm. Inset: Cross section of the spicule obtained by focused ion beam (FIB). Scale bar, 1 μm. (B) Megasclere from the demosponge S. ponderosus. Scale bar, 100 μm. Inset: Cross sections of the main shaft of the spicule obtained by FIB. Scale bar, 1 μm. Note: Some spicule tips were broken during sample preparation and appear to be flat. (C to E) Microscleres from the demosponge G. cydonium at different maturation levels, from a fully mature spicule to an immature one, respectively. Scale bars, 10 μm (C), 10 μm (D), and 1 μm (E).

Fig. 2. 3D morphology of demosponge spicules and their inner axial filaments as revealed by synchrotron microtomography and nanotomography.

A 3D reconstruction was obtained from the spicule, spicule plus the internal axial filament (red), and the filament alone in the demosponges (A to C) T. aurantium, (D to F) S. ponderosus, and (G to I) G. cydonium, respectively.

Fig. 3. X-ray diffraction analysis of protein crystals comprising the axial filaments of demosponge spicules.

(A) X-ray diffraction pattern acquired from the strongyloxea from the demosponge T. aurantium. The pattern was obtained by accumulating the diffraction data while rotating the spicule around its long axis within an angular interval of 70°, the rotation axis being perpendicular to the incident beam. (B) X-ray diffraction pattern acquired from the main shaft of the dichotriaene from the demosponge S. ponderosus. The pattern was obtained by accumulating the diffraction data while rotating the spicule around the long axis of its main shaft within an angular interval of 70°, the rotation axis being perpendicular to the incident beam. (C) X-ray diffraction pattern acquired from a mature sterraster from the demosponge G. cydonium. The pattern was obtained by raster-scanning the entire spicule with the incident beam perpendicular to the rastering plane.

Fig. 4. Proposed model of the morphogenesis of a dichotriaene in S. ponderosus.

(A) Angles between the different branches in the dichotriaene extracted from the x-ray microtomography reconstruction. (B) Three-dimensional model of the axial filament in dichotriaene and the Miller indices of the leading crystallographic planes in the branches, which were deduced from the crystal structure of the filament and the measured angles between branches. The numerical values are the angles between branches calculated with the aid of the lattice parameters of the mesoscopic protein crystal comprising the axial filament.