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The Unique Invention of the Siliceous Sponges: Their Enzymatically Made Bio-Silica Skeleton

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Molecular Biomineralization

Abstract

Sponges are sessile filter feeders that, among the metazoans, evolved first on Earth. In the two classes of the siliceous sponges (the Demospongiae and the Hexactinellida), the complex filigreed body is stabilized by an inorganic skeleton composed of amorphous silica providing them a distinct body shape and plan. It is proposed that the key innovation that allowed the earliest metazoans to form larger specimens was the enzyme silicatein. This enzyme is crucial for the formation of the siliceous skeleton. The first sponge fossils with body preservation were dated back prior to the “Precambrian-Cambrian” boundary [Vendian (610–545 Ma)/Ediacaran (542–580 Ma)]. A further molecule required for the formation of a hard skeleton was collagen, fibrous organic filaments that need oxygen for their formation. Silicatein forming the spicules and collagen shaping their morphology are the two organic components that control the appositional growth of these skeletal elements. This process starts in both demosponges and hexactinellids intracellularly and is completed extracellularly where the spicules may reach sizes of up to 3 m. While the basic strategy of their formation is identical in both sponge classes, it differs on a substructural level. In Hexactinellida, the initial silica layers remain separated, those layers bio-fuse (bio-sinter) together in demosponges. In some sponge taxa, e.g., the freshwater sponges from the Lake Baikal, the individual spicules are embedded in an organic matrix that is composed of the DUF protein. This protein comprises clustered stretches of amino acid sequences composed of pronounced hydrophobic segments, each spanning around 35 aa. We concluded with the remark of Thompson (1942) highlighting that “the sponge-spicule is a typical illustration of the theory of ‘bio-crystallisation’ to form ‘biocrystals’ ein Mittelding between an inorganic crystal and an organic secretion.” Moreover, the understanding of the enzymatic formation of the spicules conferred sponge biosilica a considerable economical actuality as a prime raw material of this millennium.

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Acknowledgments

This work was supported by grants from the German Bundesministerium für Bildung und Forschung (project “Center of Excellence BIOTECmarin”), the International Human Frontier Science Program, the European Commission (project no. 031541 – BIO-LITHO [biomineralization for lithography and microelectronics]), the Basic Scientific Research Program in China (Grant No. 200607CSJ-05), and the International S & T Cooperation Program of China (Grant No. 2008DFA00980).

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Müller, W.E.G. et al. (2011). The Unique Invention of the Siliceous Sponges: Their Enzymatically Made Bio-Silica Skeleton. In: Müller, W. (eds) Molecular Biomineralization. Progress in Molecular and Subcellular Biology(), vol 52. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21230-7_9

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