Chemo-mechanical-microstructural coupling in the tarsus exoskeleton of the scorpion Scorpio palmatus

• Published in: Acta biomaterialia Vol. 160; no. C; pp. 176 - 186
• Main Authors: Zhang, Haolu, Kellersztein, Israel, Freychet, Guillaume, Zhernenkov, Mikhail, Daniel Wagner, H., Greer, Julia R.
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01.04.2023; Elsevier
• Subjects: Animals; Ankle; Arthropod exoskeleton; Biomaterials; Chitin - chemistry; Exoskeleton Device; Mechanical properties; Proteins; Scorpions; Synchrotron radiation; Mechanical properties; Arthropod exoskeleton; Synchrotron radiation; Biomaterials
• ISSN: 1742-7061; 1878-7568
• DOI: 10.1016/j.actbio.2023.01.038

The multiscale structure of biomaterials enables their exceptional mechanical robustness, yet the impact of each constituent at their relevant length scale remains elusive. We used SAXD analysis to expose the intact chitin-fiber architecture within the exoskeleton on a scorpion's claw, revealing varying orientations, including Bouligand and unidirectional regions different from other arthropod species. We uncovered the contribution of individual components’ constituent behavior to its mechanical properties from the micro- to the nanoscale. At the microscale, in-situ micromechanical experiments were used to determine site-specific stiffness, strength, and failure of the biocomposite due to fiber orientation, while metal-crosslinking of proteins is characterized via fluorescence maps. At the constituent level, combined with FEA simulations, we uncovered the behavior of fiber-matrix deformation with fiber diameter <53.7 nm and protein modulus in the range 1.4–11 MPa. The unveiled microstructure-mechanics relationship sheds light on the evolved structural functionalities and constituents' interactions within the scorpion cuticle. The pincer exoskeleton is a fundamental part of the scorpion's body due to its multifunctionality. Precise structural and compositional analysis within the hierarchy is paramount to understand the fundamentals of the mechanical properties of the composite exoskeleton. Here, we expose the intact chitin-fiber architecture of the pincer exoskeleton using nondestructive analysis. In-situ mechanical characterization was performed at nanometer levels within the exoskeleton hierarchy, which complemented with simulations, uncovered the elastic modulus of the protein matrix. Our findings confirm the presence and distribution of metal ions and their role as reinforcements in the protein matrix via ligand coordinate bonds. In future work, these findings can be of great potential to inspire the design of composite materials. [Display omitted]