UC Santa Barbara

The eggcase of swell sharks ranks among the toughest permeable membranes known. It possesses an intricate, hierarchically ordered structure that is designed to protect delicate embryos from the external environment while enabling respiratory and metabolic exchange, achieving a tactical balance between conflicting properties — porosity and toughness.

A central concept that is not well understood is how its structural adaptations play a role in its mechanical properties. Structural analyses revealed three distinct hierarchical architectural adaptations to enhance eggcase survival: Bouligand-like organization, a non-cylindrical fibril geometry, and a nanolattice architecture. Using electron microscopy and in-situ small angle X-ray scattering during mechanical testing, we elucidated a stepwise cumulative deformation mechanism in the eggcase with indications of lattice-governed deformation mechanisms.  Key to the distinctive and enabling nanoarchitecture is a pH-driven assembly process of liquid crystalline collagenous proteins. However, the enabling molecular structure of the eggcase-forming proteins has long eluded identification due to its highly crosslinked nature and consequent insolubility. By leveraging RNA-sequencing and proteomic techniques, we discovered a new cohort of proteins, purseins, in the swell shark gland transcriptome. Characteristic of purseins is a series of contiguous domains comprising a collagenous midblock flanked by domains typically associated with the complement of innate immunity and network-forming collagens, type VIII and X. Structurally homologous proteins were also identified in the genome of other egg-producing cartilaginous fishes, suggesting a conserved molecular strategy across species including the whale shark and the elephant shark.