Glassin, a histidine-rich protein from the siliceous skeletal system of the marine sponge Euplectella , directs silica polycondensation

Abstract

The hexactinellids are a diverse group of predominantly deep sea sponges that synthesize elaborate fibrous skeletal systems of amorphous hydrated silica. As a representative example, members of the genus Euplectella have proved to be useful model systems for investigating structure-function relationships in these hierarchically ordered siliceous network-like composites. Despite recent advances in understanding the mechanistic origins of damage tolerance in these complex skeletal systems, the details of their synthesis have remained largely unexplored. Here, we describe a previously unidentified protein, named "glassin," the main constituent in the water-soluble fraction of the demineralized skeletal elements of Euplectella. When combined with silicic acid solutions, glassin rapidly accelerates silica polycondensation over a pH range of 6-8. Glassin is characterized by high histidine content, and cDNA sequence analysis reveals that glassin shares no significant similarity with any other known proteins. The deduced amino acid sequence reveals that glassin consists of two similar histidine-rich domains and a connecting domain. Each of the histidine-rich domains is composed of three segments: an amino-terminal histidine and aspartic acid-rich sequence, a proline-rich sequence in the middle, and a histidine and threonine-rich sequence at the carboxyl terminus. Histidine always forms HX or HHX repeats, in which most of X positions are occupied by glycine, aspartic acid, or threonine. Recombinant glassin reproduces the silica precipitation activity observed in the native proteins. The highly modular composition of glassin, composed of imidazole, acidic, and hydroxyl residues, favors silica polycondensation and provides insights into the molecular mechanisms of skeletal formation in hexactinellid sponges.T he hexactinellids are a circumglobal group of predominantly deep sea sponges. Exhibiting a diverse array of morphologies, the skeletal systems of hexactinellids, which are composed of amorphous hydrated silica (the other silica-forming sponge class is the Demospongiae), range in structural complexity from loose aggregations of individual skeletal elements (spicules) to complex, hierarchically ordered lattices. Hexactinellids have evolved the ability to colonize either rocky substrates or soft sediments and exhibit remarkable skeletal modifications to accomplish these feats (1). For example, the sediment-dwelling hexactinellids produce bundles of long fibrillar anchor spicules that form robust holdfast structures. These anchor spicules exhibit surprising flexibility and damage tolerance and have served as useful model systems for investigating high performance silica-based organic-inorganic biological composites (2-4). In one representative genus, Euplectella (Fig. 1), the constituent spicules are assembled into a highly regular cylindrical lattice that exhibits multiple levels of structural hierarchy spanning from the nanoscale to the macroscale. The lattice is composed of two interpenetrating grid-like networks of no...

Siliplant1 (Slp1) protein precipitates silica in sorghum silica cells

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“…Silicification is widespread among living beings from unicellular microbes to highly evolved multicellular organisms (Perry, 2003). Several bio-silica associated proteins have been reported, for example, silaffins (Kröger et al ., 1999; Poulsen & Kröger, 2004), silacidins (Wenzl et al ., 2008) and silicanin-1 (Kotzsch et al ., 2017) from diatoms; and silicateins (Shimizu et al ., 1998) and glassin (Shimizu et al ., 2015) from sponges. Among plants, a short peptide derived from an inducible proline-rich protein precipitates silica in vitro .…”

The Evolution of Silicon Transport in Eukaryotes

“…It should be noted that under this hypothesis, Si transport has ancient and deep origins and may be ancestral in eukaryotes; however, biosilicification is not. From molecular comparisons of silica polymerization mechanisms, it does appear that biosilicification has arisen independently in multiple different lineages (Sumper and Kroger 2004; Matsunaga et al 2007; Gong et al 2010; Shimizu et al 2015; Durak et al 2016). …”

Exploration of Genes Associated with Sponge Silicon Biomineralization in the Whole Genome Sequence of the Hexactinellid Euplectella curvistellata

“…The accession number FR748156). Our attempt to isolate silicatein from the silica skeleton of the E. aspergillum and E. curvistellata was unsuccessful, but instead we discovered glassin as a protein directing acceleration of silica polycondensation (Shimizu et al 2015). Sequences encoding silicatein have not identified from the transcriptome analysis of Aphrocallistes vastus by Riesgo et al (2015).…”