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Many natural silks produced by spiders and insects are unique materials in their exceptional toughness and tensile strength, while being lightweight and biodegradable–properties that are currently unparalleled in synthetic materials. Myriad approaches have been attempted to prepare artificial silks from recombinant spider silk spidroins but have each failed to achieve the advantageous properties of the natural material. This is because of an incomplete understanding of the in vivo spidroin-to-fiber spinning process and, particularly, because of a lack of knowledge of the true morphological nature of spidroin nanostructures in the precursor dope solution and the mechanisms by which these nanostructures transform into micrometer-scale silk fibers. Herein we determine the physical form of the natural spidroin precursor nanostructures stored within spider glands that seed the formation of their silks and reveal the fundamental structural transformations that occur during the initial stages of extrusion en route to fiber formation. Using a combination of solution phase diffusion NMR and cryogenic transmission electron microscopy (cryo-TEM), we reveal direct evidence that the concentrated spidroin proteins are stored in the silk glands of black widow spiders as complex, hierarchical nanoassemblies (∼300 nm diameter) that are composed of micellar subdomains, substructures that themselves are engaged in the initial nanoscale transformations that occur in response to shear. We find that the established micelle theory of silk fiber precursor storage is incomplete and that the first steps toward liquid crystalline organization during silk spinning involve the fibrillization of nanoscale hierarchical micelle subdomains.
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The Importance of a Filament-like Structure in Aerial Dispersal and the Rarefaction Effect of Air Molecules on a Nanoscale Fiber: Detailed Physics in Spiders’ Ballooning
Synopsis Many flying insects utilize a membranous structure for flight, which is known as a “wing.” However, some spiders use silk fibers for their aerial dispersal. It is well known that spiders can disperse over hundreds of kilometers and rise several kilometers above the ground in this way. However, little is known about the ballooning mechanisms of spiders, owing to the lack of quantitative data. Recently, Cho et al. discovered previously unknown information on the types and physical properties of spiders’ ballooning silks. According to the data, a crab spider weighing 20 mg spins 50–60 ballooning silks simultaneously, which are about 200 nm thick and 3.22 m long for their flight. Based on these physical dimensions of ballooning silks, the significance of these filament-like structures is explained by a theoretical analysis reviewing the fluid-dynamics of an anisotropic particle (like a filament or a high-slender body). (1) The filament-like structure is materially efficient geometry to produce (or harvest, in the case of passive flight) fluid-dynamic force in a low Reynolds number flow regime. (2) Multiple nanoscale fibers are the result of the physical characteristics of a thin fiber, the drag of which is proportional to its length but not to its diameter. Because of this nonlinear characteristic of a fiber, spinning multiple thin ballooning fibers is, for spiders, a better way to produce drag forces than spinning a single thick spider silk, because spiders can maximize their drag on the ballooning fibers using the same amount of silk dope. (3) The mean thickness of fibers, 200 nm, is constrained by the mechanical strength of the ballooning fibers and the rarefaction effect of air molecules on a nanoscale fiber, because the slip condition on a fiber could predominate if the thickness of the fiber becomes thinner than 100 nm.
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- Award ID(s):
- 1930744
- PAR ID:
- 10206553
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 60
- Issue:
- 4
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 864 to 875
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icaa063
