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

Abstract

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 ...

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

“…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.…”

A new structure-property connection in the skeletal elements of the marine sponge Tethya aurantia that guards against buckling instability

“…However, spicules also possess a proteinaceous scaffold within their silica3637. In some related species this protein forms distinct layers, which may affect the deformation and failure behavior of the spicules13353839. While T. aurantia ’s Sxa do not contain separate layers of protein and silica, the influence of any underlying protein scaffold on their elastic behavior is unknown.…”

“…Only a small amount of attention has been devoted to other equally important mechanical properties, such as strength, stiffness, and buckling resistance131415. Buckling is the phenomenon in which a slender, structural element that is subjected to an increasing axial compressive force abruptly starts to deform laterally when the force’s magnitude reaches a critical value.…”

Optical Properties of Nanostructured Silica Structures From Marine Organisms

“…Strongyloxea spicules have a strong Young's modulus of 72 GPa, which might be explained by the gathering of spicules into bundles to increase mechanical properties. It was also proposed that structure-property connection is also related to buckling resistance, and spicule's tapering structures can be considered as an optimal form for this purpose (Monn et al, 2015;Monn and Kesari, 2017). Overall, spicules have been shown to present remarkable mechanical properties in different axes as buckling resistance and toughness enhancement.…”

“…The overall density of the silica wall also affects the overall sinking rate of diatoms, and help the cells in escaping from predators and parasites, avoiding high light intensity, or finding new resource areas (Raven and Waite, 2004). The silica spicules provide support and defense to marine sponges (Burns and Ilan, 2003;Rohde and Schupp, 2011), correspond to an import feature that can serve as anchoring structure to hold on the sea floor (Ehrlich et al, 2010b;Monn et al, 2015;Monn and Kesari, 2017). However, the exact roles and properties of such silica structures for light perception, UV protection or signal transduction has been rarely investigated in vivo.…”