Mechanical adaptation of brachiopod shells via hydration-induced structural changes

Johannes Ihli,Luca Pasquini,Sabine Rosenfeldt,Esther H R Tsai,Giuseppe Falini,Mirko Holler,David G Reid,Fabio Nudelman,Melinda J Duer,Thomas S Glen,Klaus Wakonig,Thomas Kress,Eugénia Delacou,Maggie Cusack,Jim Buckman,Anna S Schenk

doi:10.1038/s41467-021-25613-4

Abstract

The function-optimized properties of biominerals arise from the hierarchical organization of primary building blocks. Alteration of properties in response to environmental stresses generally involves time-intensive processes of resorption and reprecipitation of mineral in the underlying organic scaffold. Here, we report that the load-bearing shells of the brachiopod Discinisca tenuis are an exception to this process. These shells can dynamically modulate their mechanical properties in response to a change in environment, switching from hard and stiff when dry to malleable when hydrated within minutes. Using ptychographic X-ray tomography, electron microscopy and spectroscopy, we describe their hierarchical structure and composition as a function of hydration to understand the structural motifs that generate this adaptability. Key is a complementary set of structural modifications, starting with the swelling of an organic matrix on the micron level via nanocrystal reorganization and ending in an intercalation process on the molecular level in response to hydration.

Highlights

The function-optimized properties of biominerals arise from the hierarchical organization of primary building blocks
A further advantage of a hierarchical structure is that it endows the organism with an additional level of constructional control, where the basic building blocks can be assembled into different structural motifs of different mechanical properties[8]
We report that the load-bearing shells of the brachiopod Discinisca tenuis[11] are able to dynamically modulate their mechanical properties in response to a change in the environment without the need for remodeling via resorption and regeneration of the tissue, i.e., they switch from hard and stiff when dry to malleable when hydrated within minutes

Summary

Introduction

The function-optimized properties of biominerals arise from the hierarchical organization of primary building blocks. These tomograms allow a structural evaluation of the shell and provide information such as local variations in swelling behavior and the hydration degree of specific components in the sample, e.g., organic- and mineral-rich regions.

Results

Conclusion