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Structure-Function Relationships in Biomineralized Composites: Analysis of the Architectural Complexities of Sponge Skeletal Systems

  • Author(s): Weaver, James C.
  • et al.
Abstract

The Porifera represent an ancient metazoan lineage with a fossil record that dates back more than half a billion years, and during their evolution since the mid to late Proterozoic, have presumably changed very little, maintaining their characteristically simple body plans. Although they lack the physiological complexities of many of the higher metazoa, sponges are well known for their ability to synthesize a wide range of intricately architectured siliceous skeletal elements, the formation of which in many instances far exceeds modern engineering capabilities. Because of their high precision fabrication, species-specific nanoscale structural attributes, fracture-resistant mechanical properties, and rapid rates of biosynthesis, siliceous sponge spicules have attracted a great deal of attention in recent years as model systems for the analysis of biosilicate nanofabrication.

Contained within the core of each siliceous skeletal element is a proteinaceous axial scaffold that is critically responsible for establishing spicule symmetry. Silicateins, the most abundant proteins comprising the axial filaments of demosponges, prove to be members of a well-known superfamily of proteolytic and hydrolytic enzymes and can be easily collected after silica dissolution 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. TEM and XRD analyses of these catalytic organic scaffolds from both demosponges and hexactinellids reveal that their constituent proteins exhibit highly regular ordering, and biochemical and structural analyses have provided new insight into the factors regulating their observed packing geometries and resulting spicule symmetry.

Because of their unusually large size and remarkable flexibility, spicules from the predominantly deep-sea hexactinellid sponges have provided a great deal of insight into new design strategies for more fracture resistant composite materials. In addition to their remarkable mechanical properties, the hexactinellids are also well known for the ability to form extremely complex hierarchically ordered robust skeletal networks from their constituent spicules. The design principles learned from these analyses as well as new techniques for investigating the synthesis mechanisms of sponge spicules in vivo are discussed in detail.

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