Mineralization of the metre-long biosilica structures of glass sponges is templated on hydroxylated collagen

Ehrlich, Hermann; Deutzmann, Rainer; Brunner, Eike; Cappellini, Enrico; Koon, Hannah; Solazzo, Caroline; Yang, Yingzi; Ashford, David A.; Thomas‐Oates, Jane; Lubeck, Markus; Baessmann, Carsten; Langrock, Tobias; Hoffmann, Ralf; Wörheide, Gert; Reitner, Joachim; Simon, Paul; Tsurkan, Mikhail V.; Ereskovsky, Alexander; Kurek, Denis V.; Bazhenov, Vasilii V.; Hunoldt, S.; Mertig, Michael; Vyalikh, D. V.; Молодцов, С. Л.; Kummer, K.; Worch, H.; Smetacek, Victor; Collins, Matthew J.

doi:10.1038/nchem.899

Cited by 149 publications

(142 citation statements)

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“…NEXAFS experiments, performed at the carbon K edge, provided evidence that the contribution of carbon is mainly owing to the organic part of the holdfast ( figure 3). Moreover, the carbon K-edge spectrum of this sponge holdfast showed all the typical absorption features of chitin and not those of spongin (figure 3), or collagen, as was the case for spicules of the hexactinellid Hyalonema sieboldi in previous studies by our team [30]. Both chitin and collagen spectra exhibited a strong peak at approximately 288 eV that is associated with the C 1s !…”

Section: (B) Identification Of Chitin Within Holdfast Of Lubomirskia mentioning

confidence: 85%

“…Recently, NEXAFS technique has been successfully applied to determine key differences between electronic properties related to the light adsorption by polysaccharides and proteins, even within diverse biominerals [28][29][30]. We used NEXAFS spectroscopy to explore site-specific electronic properties of L. baicalensis cleaned holdfast samples (measured on 500 Â 500 mm areas) in order to gain insight into the nature of the organic components.…”

Section: (B) Identification Of Chitin Within Holdfast Of Lubomirskia mentioning

confidence: 99%

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First report on chitinous holdfast in sponges (Porifera)

et al. 2013

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A holdfast is a root-or basal plate-like structure of principal importance that anchors aquatic sessile organisms, including sponges, to hard substrates. There is to date little information about the nature and origin of sponges' holdfasts in both marine and freshwater environments. This work, to our knowledge, demonstrates for the first time that chitin is an important structural component within holdfasts of the endemic freshwater demosponge Lubomirskia baicalensis. Using a variety of techniques (near-edge X-ray absorption fine structure, Raman, electrospray ionization mas spectrometry, Morgan-Elson assay and Calcofluor White staining), we show that chitin from the sponge holdfast is much closer to a-chitin than to b-chitin. Most of the three-dimensional fibrous skeleton of this sponge consists of spicule-containing proteinaceous spongin. Intriguingly, the chitinous holdfast is not spongin-based, and is ontogenetically the oldest part of the sponge body. Sequencing revealed the presence of four previously undescribed genes encoding chitin synthases in the L. baicalensis sponge. This discovery of chitin within freshwater sponge holdfasts highlights the novel and specific functions of this biopolymer within these ancient sessile invertebrates.

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Section: (B) Identification Of Chitin Within Holdfast Of Lubomirskia mentioning

confidence: 85%

Section: (B) Identification Of Chitin Within Holdfast Of Lubomirskia mentioning

confidence: 99%

First report on chitinous holdfast in sponges (Porifera)

et al. 2013

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“…protection, [72]), so once a foreign SIT gene was incorporated into the genome it would confer a strong selective advantage for that organism. Several common biomolecules, such as collagen [73], glycoproteins [69], polyamines [2] and proteases [74] are known to have the capacity to direct silica polymerization. It may be the case that many taxa possess the capacity for silicification but lack the means to concentrate sufficient silicon for polymerization to occur.…”

Section: (F ) Evolutionary Implications For Biosilicificationmentioning

confidence: 99%

A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates

et al. 2013

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Biosilicification is widespread across the eukaryotes and requires concentration of silicon in intracellular vesicles. Knowledge of the molecular mechanisms underlying this process remains limited, with unrelated silicontransporting proteins found in the eukaryotic clades previously studied. Here, we report the identification of silicon transporter (SIT)-type genes from the siliceous loricate choanoflagellates Stephanoeca diplocostata and Diaphanoeca grandis. Until now, the SIT gene family has been identified only in diatoms and other siliceous stramenopiles, which are distantly related to choanoflagellates among the eukaryotes. This is the first evidence of similarity between SITs from different eukaryotic supergroups. Phylogenetic analysis indicates that choanoflagellate and stramenopile SITs form distinct monophyletic groups. The absence of putative SIT genes in any other eukaryotic groups, including non-siliceous choanoflagellates, leads us to propose that SIT genes underwent a lateral gene transfer event between stramenopiles and loricate choanoflagellates. We suggest that the incorporation of a foreign SIT gene into the stramenopile or choanoflagellate genome resulted in a major metabolic change: the acquisition of biomineralized silica structures. This hypothesis implies that biosilicification has evolved multiple times independently in the eukaryotes, and paves the way for a better understanding of the biochemical basis of silicon transport through identification of conserved sequence motifs.

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“…contained collagen, celluloselike filaments, hexosamine-containing organics, and proteins containing relatively large amounts of aspartic acid, glutamic acid, glycine and histidine. Ehrlich et al (25) isolated a fibrous material from the anchoring spicules of the hexactinellid sponge Hyalonema sieboldi, and demonstrated that the material was composed of collagen with an unusual glycine-(3-hydroxyproline)-(4-hydroxyproline) motif, which in vitro, exhibited silica polycondensation and templating activities. Ehrlich and Worch (26) also reported chitin in hexactinellid sponges including Farrea occa and E. aspergillum as an organic component of their silicious skeletal systems.…”

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

Shimizu

Amano

Bari

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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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...

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Mineralization of the metre-long biosilica structures of glass sponges is templated on hydroxylated collagen

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Cited by 149 publications

References 19 publications

First report on chitinous holdfast in sponges (Porifera)

First report on chitinous holdfast in sponges (Porifera)

A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates

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

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