Halochromic Amorphous Calcium Carbonate Crystallization Inspired by Biomineral Pigmentation in Sea Urchins

Marine life fascinates by its ability of producing a large variety of multifunctional biomineralized structures that often exhibit striking colors. For example, the wide range of hues observed in calcium carbonate (CaCO₃)-based biominerals of sea urchins is due to the occlusion of small organic pigment molecules (polyhydroxy-1,4-naphthoquinone molecules, PHNQs) within their skeletal elements. Synthesized by sea urchins, PHNQs are bio-active secondary metabolites responsible for the red colors displayed by the immune red-spherule cells as well as for the green and purple hues observed in the biomineralized spines. The latter are known to form through amorphous CaCO₃ (ACC) precursors. Biomineralization and pigmentation processes are two intertwined metabolic pathways, however the role of secondary metabolites, such as organic pigment molecules, on ACC formation and crystallization mechanisms remains unexplored. Therefore, inspired by the growth of pigmented calcite in sea urchins occurring through ACC precursors and in the presence of PHNQs, we co-precipitated ACC with naphthazarin (NZ) (an analogue to PHNQ) and studied its crystallization mechanisms in solution. Our results show that NZ produces intense colored hybrid pigments but has little effect on ACC structure and stability against crystallization while it promotes calcite formation after ACC crystallization and tends to stabilize the vaterite phase before its conversion into calcite. In addition, NZ, which is red at acidic pH and blue before ACC precipitation, leads to a lavender blue ACC powder that further crystallizes in solution into a violet blue calcite powder. We propose that these remarkable changes in color are due to successive OH deprotonations of NZ driven by pH variations imposed by ACC precipitation and crystallization likely during a dissolution/reprecipitation mechanism. Thus, by controlling the speciation of NZ in solution and capturing its partial deprotonation state within amorphous and then crystalline hybrid pigments, we evidence an halochromic ACC crystallization pathway that could unveil color changes during the pigmentation of CaCO₃-biominerals formed through amorphous phases. Blue colors that mostly originate from structural color in nature, can thus be obtained by tweaking red pigments using pH shift, a strategy already recognized in some plants.