Heat-mediated micro- and nano-pore evolution in sea urchin biominerals

Biomineralized structures with intricate shapes and morphologies, such as sea urchin skeletal elements, grow via the deposition of hydrated amorphous calcium carbonate (ACC) particles that subsequently crystallizes into single-crystalline calcite. This process is accompanied by volume changes due to density differences between the initial and final mineral state as well as variations in hydration levels. For this reason, the presence of macroporosity in synthetic systems was shown to be pivotal in the formation of large single crystals through ACC precursors. However, the role of macroporosity down to nanoporosity in the formation of biogenic minerals remains unknown. Here, we investigate the micro- and nano-porosity as well as the evolution of internal interfaces in the spines and test plates of Paracentrotus lividus sea urchins during the heat-mediated crystallization of remnant ACC and the destruction of intracrystalline organic molecules, using SEM, FIB-SEM, and in situ heating synchrotron SAXS measurements. We show the presence of nanopores likely filled with hydrated organics and visualize the evolution of nano- to micro-pores induced by heating, which may serve to accommodate the volume changes between amorphous and crystalline phases. The obtained results analyzed using thermodynamical considerations suggest that the growth in size of the nanopores is controlled by Ostwald ripening and is well described in the framework of classical pore coarsening theories. The extracted activation energies manifest that nanopore coarsening in the test plates is governed by surface diffusion, whereas in the spines by bulk diffusion. We suggest that such striking differences in diffusion mechanisms are caused by dissimilar levels of macroporosity and distributions of nano- and micro-internal interfaces in pristine biominerals