Unifying Design Strategies in Demosponge and Hexactinellid Skeletal Systems

Weaver, James C.; Milliron, Garrett; Allen, Peter M.; Miserez, Ali; Rawal, Aditya; Garay, Javier; Thurner, Philipp J.; Seto, Jong; Mayzel, Boaz; Friesen, Larry Jon; Chmelka, Bradley F.; Fratzl, Peter; Aizenberg, Joanna; Dauphin, Yannicke; Kisailus, David; Morse, Daniel E.

doi:10.1080/00218460903417917

Cited by 42 publications

(42 citation statements)

References 27 publications

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“…Considering that our model is an idealization and that it is not constructed with the goal of capturing the failure process, we do not expect this interpretation to be accurate. We believe that the silica cylinders will fail progressively, as was observed in spicules from related species (25,32,37). In traditional engineering design, the specific strength of loadbearing structural elements is increased by varying their external geometry.…”

Section: Discussionmentioning

confidence: 77%

“…Although the precise mechanical properties of the compliant organic interlayers have yet to be fully characterized, we incorporate their potential contributing effect into our model by assuming that σ 33 can be discontinuous across adjacent silica cylinders. The assumption that the interlayers are compliant compared with the silica cylinders is supported through recent mechanical characterization of spicules from Monorhaphis chuni (31,32), which is closely related to E. aspergillum, contains a similar bulk chemical composition (25), and is similarly laminated.…”

Section: Significancementioning

confidence: 99%

“…Through the detailed analysis of these complex skeletal materials, useful design lessons can be extracted that can be used to guide the synthesis of synthetic constructs with novel performance metrics (16)(17)(18)(19)(20). The complex and mechanically robust cage-like skeletal system of the hexactinellid sponge Euplectella aspergillum has proved to be a particularly useful model system for investigating structure-function relationships in hierarchically ordered biological composites (21)(22)(23)(24)(25). The sponge is anchored to the sea floor by thousands of anchor spicules (long, hair-like skeletal elements), each of which measures ca.…”

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confidence: 99%

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New functional insights into the internal architecture of the laminated anchor spicules of Euplectella aspergillum

Monn

Weaver

Zhang

et al. 2015

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

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To adapt to a wide range of physically demanding environmental conditions, biological systems have evolved a diverse variety of robust skeletal architectures. One such example, Euplectella aspergillum, is a sediment-dwelling marine sponge that is anchored into the sea floor by a flexible holdfast apparatus consisting of thousands of anchor spicules (long, hair-like glassy fibers). Each spicule is covered with recurved barbs and has an internal architecture consisting of a solid core of silica surrounded by an assembly of coaxial silica cylinders, each of which is separated by a thin organic layer. The thickness of each silica cylinder progressively decreases from the spicule's core to its periphery, which we hypothesize is an adaptation for redistributing internal stresses, thus increasing the overall strength of each spicule. To evaluate this hypothesis, we created a spicule structural mechanics model, in which we fixed the radii of the silica cylinders such that the force transmitted from the surface barbs to the remainder of the skeletal system was maximized. Compared with measurements of these parameters in the native sponge spicules, our modeling results correlate remarkably well, highlighting the beneficial nature of this elastically heterogeneous lamellar design strategy. The structural principles obtained from this study thus provide potential design insights for the fabrication of high-strength beams for load-bearing applications through the modification of their internal architecture, rather than their external geometry. structure-property relationship | structural biomaterial | biocomposite | variational analysis B iological structural materials such as nacre, tooth, bone, and fish scales (1-9) often exhibit remarkable mechanical properties, which can be directly attributed to their unique structure and composition (10)(11)(12)(13)(14)(15). Through the detailed analysis of these complex skeletal materials, useful design lessons can be extracted that can be used to guide the synthesis of synthetic constructs with novel performance metrics (16)(17)(18)(19)(20). The complex and mechanically robust cage-like skeletal system of the hexactinellid sponge Euplectella aspergillum has proved to be a particularly useful model system for investigating structure-function relationships in hierarchically ordered biological composites (21-25). The sponge is anchored to the sea floor by thousands of anchor spicules (long, hair-like skeletal elements), each of which measures ca. 50 μm in diameter and up to 10 cm in length ( Fig. 1 A and B). The distal end of each anchor spicule is capped with a terminal crown-like structure and is covered with a series of recurved barbs that secure the sponge into the soft sediments of the sea floor (Fig. 1C). The proximal regions of these spicules are in turn bundled together and cemented to the main vertical struts of the skeletal lattice.These spicules contain an elastically heterogeneous, lamellar internal structure and are composed of amorphous hydrated silica. Surrounding a thin ...

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Section: Discussionmentioning

confidence: 77%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

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New functional insights into the internal architecture of the laminated anchor spicules of Euplectella aspergillum

Monn

Weaver

Zhang

et al. 2015

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

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“…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.…”

mentioning

confidence: 99%

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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“…The total length of spicules in demosponge typically does not exceed a few millimetres due to the mechanisms behind its formation. Indeed, dimensions are limited by the size of the cells involved in the secretion of the axial filament (Uriz et al 2000;Weaver et al 2010). Demosponges and hexactinellids can be differentiated based on their meglasclere terminations and number of axes of symmetry, with demosponges having monaxons and tetraxons, and hexactinellids having monaxons and triaxons (Uriz et al 2003;Uriz 2006).…”

Section: Spicule Morphologymentioning

confidence: 99%

Analysis of silicatein gene expression and spicule formation in the demosponge Amphimedon queenslandica

Gauthier¹

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The skeletal elements in most sponges are siliceous spicules. These are fabricated into species-specific sizes and shapes. Demosponges, in particular, have specialised cells called sclerocytes that possess the unique ability to synthesise biosilica and these spicules.Underlying the diversity of demosponge spicules morphology is a conserved protein, called silicatein. This thesis aims to investigate the process of spiculogenesis in the different developmental stages of the demosponge Amphimedon queenslandica, and the evolution and developmental expression of the silicatein gene family in relation to spicule formation.A. queenslandica is the only sponge species to have its genome fully sequenced, assembled and annotated, and currently is one of the best models to study sponge development (Srivastava et al. 2010). This species broods embryos year-round, facilitating the access to Conservation of gene structure and exon length in silicatein and cathepsin L genes suggests that these genes have preserved an ancestral gene structure common to both gene families in both marine and freshwater sponges.Using in situ hybridisation, I demonstrated that silicatein genes are expressed during A. queenslandica early embryonic development, with genes being expressed exclusively in sclerocytes. Analysis of gene expression levels through embryogenesis and metamorphosis, using RNA-Seq performed on a pool of same stage individuals, revealed that all silicatein-like genes are differentially expressed throughout development, and the expression of silicatein genes occurs prior to spicule formation. However, some silicatein-like gene expression levels and spicule number do not appear to be tightly correlated.

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Unifying Design Strategies in Demosponge and Hexactinellid Skeletal Systems

Cited by 42 publications

References 27 publications

New functional insights into the internal architecture of the laminated anchor spicules of Euplectella aspergillum

New functional insights into the internal architecture of the laminated anchor spicules of Euplectella aspergillum

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

Analysis of silicatein gene expression and spicule formation in the demosponge Amphimedon queenslandica

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