Diffusive Dynamic Modes of Recombinant Squid Ring Teeth Proteins by Neutron Spectroscopy

Abstract

Stimuli-responsive structural proteins are emerging as promising biocompatible materials for a wide range of biological and nonbiological applications. To understand the physical properties of structural proteins and to replicate their performance in biosynthetic systems, there is a need to understand the molecular mechanisms and relationships that regulate their structure, dynamics, and properties.Here, we study the dynamics of a recombinant squid-inspired protein from Loligo vulgaris (Lv18) by elastic and quasielastic neutron scattering (QENS) to understand the connection between nanostructure, chain dynamics, and mechanical properties. Lv18 is a semicrystalline structural protein, which is plasticized by water above its glass transition temperature at 35 °C. Elastic scans revealed an increased protein chain mobility upon hydration, superimposed dynamic processes, and a decrease in dynamic transition temperatures. Further analysis by QENS revealed that while dry Lv18 protein dynamics are dominated by localized methyl group rotations, hydrated Lv18 dynamics are dominated by the confined diffusion of flexible chains within a β-sheet nanocrystalline network (8 Å of confinement radius). Our findings establish a relationship between the segment block architecture of Lv18, the diffusive motions within the protein structure, and the mechanical properties of recombinant squid proteins, which will advance the molecular design of novel high-performance protein-inspired materials with tailored dynamics and mechanical properties.

Functional Chemical Motor Coatings for Modular Powering of Self-Propelled Particles

“…In addition, the nanocrystalline protein network is also dependent on temperature as it has a glass transition temperature in hydrated conditions of 40–45 °C. At this temperature, the material exhibits a glass transition where the amorphous chains of the polymer (i.e., amorphous strands connecting the β-sheet nanocrystals) are free to rotate and diffuse within the matrix and lead to a transition into a rubbery soft material, above 45 °C. , As expected, these changes in the protein network dynamics have an effect on the fuel release on SRT/HFIP motor systems and their activity lifetime. Above the glass transition temperature (rubbery state), the protein network is loose enough so that the fuel can diffuse out quickly, resulting in short activity lifetimes with increasing temperatures (Figure S5).…”

“…Squid sucker ring teeth (SRT) proteins are high-strength structural proteins found in teeth-like structures in the suction cups of squid species. 26 These proteins have a repetitive diblock amino acid sequence alternating throughout the peptide chain, with crystal-forming blocks that self-assemble into β-sheet nanostructures. 27,28 The β-sheet nanocrystals provide strong mechanical properties and stability underwater to the teethed appendages (∼GPa range modulus) by acting as reversible hydrogen-bonded cross-links in the protein network.…”

“…Squid sucker ring teeth (SRT) proteins are high-strength structural proteins found in teeth-like structures in the suction cups of squid species . These proteins have a repetitive diblock amino acid sequence alternating throughout the peptide chain, with crystal-forming blocks that self-assemble into β-sheet nanostructures. , The β-sheet nanocrystals provide strong mechanical properties and stability underwater to the teethed appendages (∼GPa range modulus) by acting as reversible hydrogen-bonded cross-links in the protein network. The dynamic nanocrystal cross-links enable fine control over the network structure, topology, and kinetics, achieving physical properties (mechanical, optical, thermal, and so forth) that often surpass their synthetic polymer analogs. , Due to their outstanding properties, SRT proteins and their biosynthetic derivatives have been recently used to develop soft actuators and self-propelled microrobots, achieving biodegradable functional robotic materials composed solely of proteins .…”

Adaptive Magnetoactive Soft Composites for Modular and Reconfigurable Actuators

“…The plasticization of the protein network increases the mobility of the chains in the amorphous phase, allowing for enhanced diffusion dynamics. [ 26 ] This not only results in the softening of the network (as measured by a decrease in modulus) but also in the emergence of healing properties. The protein network is stabilized by β‐sheet nanocrystals as reversible physical crosslinks; however, these nanostructures cannot reform in the glassy state as the chains have limited mobility and are kinetically trapped.…”

“…[18] Complementing the alanine-rich blocks, glycine-rich segments connect the β-sheet nanocrystals within the network, constituting the amorphous phase of the semicrystalline structure and providing the material with shape-memory properties. [25,26] While SRT proteins have been explored in soft small-scale devices, [27][28][29] they present an excellent materials platform for the reconfigurable programming of modular magnetic actuators due to their dynamic structure and reversible properties.…”