Effects of Laminate Architecture on Fracture Resistance of Sponge Biosilica: Lessons from Nature

Miserez, Ali; Weaver, James C.; Thurner, Philipp J.; Aizenberg, Joanna; Dauphin, Yannicke; Fratzl, Peter; Morse, Daniel E.; Zok, Frank W.

doi:10.1002/adfm.200701135

Cited by 151 publications

(127 citation statements)

References 24 publications

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“…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: 80%

“…An alternate mechanics model based on the idea of controlling flaws has been put forward to explain the trend of decreasing thicknesses in the spicule's internal structure (32). In this alternate model σ 33 is assumed to vary affinely over Ω and the load capacity is maximized by varying the cylinder thicknesses subject to the constraint that each cylinder's strength be greater than the maximum value of σ 33 over its cross-section.…”

Section: Discussionmentioning

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: Significancementioning

confidence: 80%

Section: Discussionmentioning

confidence: 99%

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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“…While optimized hardness and modulus are important for maximizing impact forces during prey knocking, an additional biomechanical requirement is a fracture resistance in the impact region that is high enough to prevent permanent microdamage to the appendages. Since the microscopic size of the impact region (o100 mm) precludes the usage of standard fracture toughness specimens, as has, for instance, been done for other biominerals such as conch shells 43 or bone 44 (even 'miniaturized' samples with sizes in the mm range are orders of magnitude larger than the dactyl appendages' impact regions), fracture toughness was assessed by indentation fracture 22 . The method is deemed suitable as a comparative assessment of the fracture resistance.…”

Section: Discussionmentioning

confidence: 99%

“…Fracture toughness values were evaluated using a methodology we previously developed for sponge biosilica 22 . A sharp cubecorner tip was selected for these experiments because of its ability to induce cracking at external loads one to two orders of magnitude lower than the Berkovich geometry.…”

Section: Microstructural Features and Preferred Fibre Orientationmentioning

confidence: 99%

Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages

et al. 2014

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Stomatopods are shallow-water crustaceans that employ powerful dactyl appendages to hunt their prey. Deployed at high velocities, these hammer-like clubs or spear-like devices are able to inflict substantial impact forces. Here we demonstrate that dactyl impact surfaces consist of a finely-tuned mineral gradient, with fluorapatite substituting amorphous apatite towards the outer surface. Raman spectroscopy measurements show that calcium sulphate, previously not reported in mechanically active biotools, is co-localized with fluorapatite. Ab initio computations suggest that fluorapatite/calcium sulphate interfaces provide binding stability and promote the disordered-to-ordered transition of fluorapatite. Nanomechanical measurements show that fluorapatite crystalline orientation correlates with an anisotropic stiffness response and indicate significant differences in the fracture tolerance between the two types of appendages. Our findings shed new light on the crystallochemical and microstructural strategies allowing these intriguing biotools to optimize impact forces, providing physicochemical information that could be translated towards the synthesis of impact-resistant functional materials and coatings.

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“…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)(3)(4). In one representative genus, Euplectella (Fig.…”

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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Effects of Laminate Architecture on Fracture Resistance of Sponge Biosilica: Lessons from Nature

Cited by 151 publications

References 24 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

Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages

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

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