Direct Solvation of Glycoproteins by Salts in Spider Silk Glues Enhances Adhesion and Helps To Explain the Evolution of Modern Spider Orb Webs

Abstract

The evolutionary origin of modern viscid silk orb webs from ancient cribellate silk ancestors is associated with a 95% increase in diversity of orb-weaving spiders, and their dominance as predators of flying insects, yet the transition's mechanistic basis is an evolutionary puzzle. Ancient cribellate silk is a dry adhesive that functions through van der Waals interactions. Viscid threads adhere more effectively than cribellate threads because of the high extensibility of their axial silk fibers, recruitment of multiple glue droplets, and firm adhesion of the viscid glue droplets. Viscid silk's extensibility is permitted by the glue's high water content, so that organic and inorganic salts present in viscid glue droplets play an essential role in contributing to adhesion by sequestering the atmospheric water that plasticizes the axial silk fibers. Here, we provide direct molecular and macro-scale evidence to show that salts also cause adhesion by directly solvating the glycoproteins, regardless of water content, thus imparting viscoelasticity and allowing the glue droplets to establish good contact. This "dual role" of salts, plasticizing the axial silk indirectly through water sequestration and directly solvating the glycoproteins, provides a crucial link to the evolutionary transition from cribellate silk to viscid silk. In addition, salts also provide a simple mechanism for adhering even at the extremes of relative humidity, a feat eluding most synthetic adhesives.

Diet-induced covariation between architectural and physicochemical plasticity in an extended phenotype

“…Spiral thread stickiness, however, was not significantly affected by feeding treatment so the second possibility seems the most likely. A greater concentration of HPO 4 but lower concentration of KNO 3 in the spiral glues of the webs of spiders fed adult crickets is somewhat difficult to explain, primarily because so little is known about the costs, benefits and functional significance of these salts within orb web gluey silks (Sahni et al, 2014a). A tentative explanation is that because nitrates are needed for other body functions (Frost et al, 2005) KNO 3 becomes more sparingly used as more spiral threads, and consequently more gluey silk, are deposited (Opell et al, 2013).…”

“…The salts induce cohesive forces that cause the aggregate silk to coalesce along the flagelliform thread into droplets that resemble beads on a string (Sahni et al, 2014b;Opell et al, 2015). The salts also facilitate water uptake from the environment into the droplets (Vollrath et al, 1990;Sahni et al, 2010Sahni et al, , 2011Townley and Tillinghast, 2013), which keeps the droplets hydrated, and thus solvates the glycoproteins (Sahni et al, 2011(Sahni et al, , 2014a.…”

Humidity-mediated changes in an orb spider's glycoprotein adhesive impact prey retention time

“…Over the course of a day, the volumes of these hygroscopic droplets change as they respond to changes in environmental humidity (Townley et al, 1991;Opell et al, 2013). Although the allocation of absorbed atmospheric water has not been fully studied, some of it solvates the glycoprotein, ensuring its interaction with a surface, some of it hydrates the glycoprotein core, reducing its viscosity, and some of it probably increases flagelliform fiber extensibility (Sahni et al, 2011(Sahni et al, , 2014Opell et al, 2011Opell et al, , 2013Amarpuri et al, 2015).…”

Ubiquitous distribution of salts and proteins in spider glue enhances spider silk adhesion

“…Salts found in the glue droplet are hygroscopic and are hypothesized to absorb and retain atmospheric water in the glue droplet41113. Recently, Solid-State NMR investigations showed that the salts directly facilitate adhesion by solvating the glycoproteins15.…”

“…However, both models are based on optical and physical measurements, and lack chemical evidence of heterogeneity in structure. Moreover, the recent finding that salts facilitate protein mobility at a molecular level15 suggests an alternative model where both salts and proteins are distributed ubiquitously throughout the glue droplet.…”