Reversibly labile, sclerotization-induced elastic properties in a keratin analog from marine snails: whelk egg capsule biopolymer (WECB)

Rapoport, H Scott; Shadwick, Robert E.

doi:10.1242/jeb.02613

Cited by 29 publications

(39 citation statements)

References 24 publications

(36 reference statements)

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“…The stress-strain data acquired during in situ tensile testing did not vary between individual samples and are in agreement with previously published findings on the material [2,5,20]. An example of a stress versus true strain curve can be seen in figure 1b.…”

Section: Mechanical Characterizationsupporting

confidence: 90%

“…As observed in previous static WAXD measurements on WEC material [5], unloaded strips of capsule wall material exhibit peaks with a D-spacing of approximately 0.53 nm along both the meridian and equator (figure 2a). These peaks correspond to the axial periodicity along coiled-coil a-helices [11] and suggest that this material has a-helical fibres oriented orthogonally as previously observed [2,5,20]. On straining the capsule material uniaxially from 0 to 5 per cent, true strain does not change these diffraction patterns appreciably.…”

Section: In Situ Wide Angle X-ray Diffractionsupporting

confidence: 72%

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Pseudoelastic behaviour of a natural material is achieved via reversible changes in protein backbone conformation

Harrington

Wasko

Mašić

et al. 2012

J. R. Soc. Interface.

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The egg capsules of marine prosobranch gastropods, commonly know as whelks, function as a protective encapsulant for whelk embryos in wave-swept marine environments. The proteinaceous sheets comprising the wall of whelk egg capsules (WEC) exhibit long-range reversible extensibility with a hysteresis of up to 50 per cent, previously suggested to result from reversible changes in the structure of the constituent protein building blocks. Here, we further investigate the structural changes of the WEC biopolymer at various hierarchical levels using several different time-resolved in situ approaches. We find strong evidence in these biological polymers for a strain-induced reversible transition from an ordered conformational phase to a largely disordered one that leads to the characteristic reversible hysteretic behaviour, which is reminiscent of the pseudoelastic behaviour in some metallic alloys. On the basis of these results, we generate a simple numerical model incorporating a worm-like chain equation to explain the phase transition behaviour of the WEC at the molecular level.

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Section: Mechanical Characterizationsupporting

confidence: 90%

Section: In Situ Wide Angle X-ray Diffractionsupporting

confidence: 72%

Pseudoelastic behaviour of a natural material is achieved via reversible changes in protein backbone conformation

Harrington

Wasko

Mašić

et al. 2012

J. R. Soc. Interface.

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“…This might be the situation for N. lamellosa. The capsules of N. lamellosa are tough structures (Rapoport and Shadwick 2002;Rapoport and Shadwick 2007), and studies of other species suggest that capsules protect individuals from predators (Pechenik 1999); however, the two species of predators used in our experiment can consume capsules and their contents (personal observation). In addition, N. lamellosa do not eat .…”

Section: Discussionmentioning

confidence: 77%

“…This species forms breeding aggregations from November to April, and lays encapsulated eggs on rocks in the mid-low intertidal zone (Strathmann 1987). Each capsule contains about 20 embryos (Spight and Emlen 1976), and is encased in a tough, thin, proteinaceous capsule that looks like a little American-style football with biomechanical properties similar to keratin (Rapoport and Shadwick 2002;Rapoport and Shadwick 2007). Unlike several related species, there are no reports of nurse eggs or intra-capsule cannibalism for N. lamellosa.…”

Section: Methodsmentioning

confidence: 99%

Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail

2010

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Predator-induced hatching plasticity has been demonstrated in many species of amphibians. However, animals from other clades (e.g., marine species of molluscs and annelids) also place their embryos in capsules or gelatinous masses and might also exhibit hatching plasticity to predators. To date there is no evidence of predator-induced hatching plasticity from any marine species or a major clade of bilateria animals, the Lophotrochozoa. We studied predator-induced hatching plasticity of Nucella lamellosa, a carnivorous marine snail that deposits embryos in capsules. We used two experiments to investigate the effects of two types of predator, crabs and isopods, on developing embryos. In the first experiment, we quantified proportion of hatched embryos from capsules through time exposed to water-borne chemicals of crabs and isopods. Crabs delayed time-to-hatching, and the effects of predators were additive. In the second experiment, we quantified proportion of hatched embryos from capsules through time, developmental stage, and size of embryos in capsules exposed to water-borne chemicals of crabs and conspecifics. With this experiment, we wanted to answer: (1) whether a delay in hatching corresponded to embryos developing slower, and (2) whether the general products of metabolic waste from organisms can delay hatching. We unexpectedly observed that adult conspecific snails accelerated hatching but not developmental rate-the few past studies on the effects of conspecifics have all demonstrated that conspecifics delay time-to-hatching and rate of development. The results were also inconsistent with metabolic waste in general causing a delay in hatching, although the effect of conspecifics does weaken this inference. This study demonstrates that predators delay time-to-hatching in a marine mollusc, and suggests that predator-induced hatching plasticity is widespread among animals and likely evolved multiple times within the bilateria. In addition, conspecifics accelerated time-to-hatching in a marine mollusc, which suggests that conspecifics, like predators, might commonly influence when embryos hatch.

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“…In all cases, the essential feature was that an extensible polymer provided hidden length, and there was a high density of weaker sacrificial bonds to provide energy dissipation. This general pattern has been seen in a number of solid biomaterials as well, with examples such as nacreous gastropod shell (Smith et al, 1999b), bone (Fantner et al, 2005), whelk egg capsule (Rapoport and Shadwick, 2007;Miserez et al, 2009), mussel byssus (Harrington et al, 2009;Krauss et al, 2013) and caddisfly silk (Ashton et al, 2013;Ashton and Stewart, 2015).…”

Section: Discussionmentioning

confidence: 79%

Double network gels and the toughness of terrestrial slug glue

Wilks

Rabice

Garbacz

et al. 2015

Journal of Experimental Biology

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The terrestrial slug Arion subfuscus produces a defensive secretion that is sticky and tough, despite being a dilute gel. It is unusual in having high stiffness for a gel, yet retaining the high extensibility typical of mucus. In tensile tests, it sustains an average peak stress of 101 kPa, and fails at an average strain of 9.5. This gives the gel toughness; it requires much greater strain energy to fracture than most gels. This toughness may arise from a double-network type mechanism. In this mechanism, two separate, interpenetrating networks of polymers with different properties combine to give toughness that can be several orders of magnitude greater than either network individually. Native gel electrophoresis suggests that A. subfuscus glue consists of two networks: a network of negatively charged proteins ranging in M r from 40×10 3 to 220×10 3 that can be dissociated by hydroxylamine and a network of heparan sulfate-like proteoglycans. The two networks are not tightly linked, though proteins of M r 40×10 3 and 165×10 3 may associate with the carbohydrates. Targeted disruption of either network separately, using enzymatic hydrolysis, disulfide bond breakage or imine bond disruption completely disrupted the glue, resulting in no measurable toughness. Thus, the two networks separately provide little toughness, but together they work synergistically to create a tough material, as predicted in the double-network mechanism.

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Reversibly labile, sclerotization-induced elastic properties in a keratin analog from marine snails: whelk egg capsule biopolymer (WECB)

Cited by 29 publications

References 24 publications

Pseudoelastic behaviour of a natural material is achieved via reversible changes in protein backbone conformation

Pseudoelastic behaviour of a natural material is achieved via reversible changes in protein backbone conformation

Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail

Double network gels and the toughness of terrestrial slug glue

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