A Core Structural Protein That Builds the Locust Mandible with a Mechanical Gradient.

Abstract

Natural materials, such as locust mandibles and squid beaks, define significant mechanical gradients that have been attributed to the chemical gradients of their specialized structural proteins (SPs). However, the mechanism by which SPs form chemical gradients in these materials remains unknown. In this study, a highly abundant histidine-rich structural protein (<i>Lm</i>MHSP) was identified in the mandible of a migratory locust (<i>Locusta migratoria</i>). <i>Lm</i>MHSP was proven by both <i>in vivo</i> and <i>in vitro</i> evidence to act as a core building block of the mandible with a variety of synergistic functions including chitin binding, matrix formation via liquid-liquid phase separation, chemical cross-linking, and metal coordination. Furthermore, we found that the SP gradient in the locust mandible stems from the chitin-binding activity of <i>Lm</i>MHSP and different microstructures of chitin scaffolds in different regions. These findings advance our understanding of the formation mechanisms of natural biomaterials and have implications for the fabrication of biomimetic materials.