Inorganic Ions Regulate Amorphous-To-Crystal Shape Preservation in Biomineralization COMMENTARY Jeffrey D

COMMENTARY Inorganic ions regulate amorphous-to-crystal shape preservation in biomineralization COMMENTARY Jeffrey D. Rimera,1 Calcified minerals in biogenic materials often play a utilitarian role, such as structural supports in bone, teeth, and shells, where the crystals are arranged in well-ordered arrays (1, 2). The ability of organisms to produce single crystalline scaffolds and hierarchical architectures with unique features, such as bent or spheroidal shapes, has long fascinated scientists. The mechanisms of biomineral nucleation and growth are complex and not fully understood, while the ability to mimic these processes in vitro has proven challenging. Much attention has been given to studying the skeletal sections of sea urchins and other organisms (e.g., mol- lusks, echinoderms, calcisponges, and corals) that con- tain curved surfaces and various convoluted shapes (3). From numerous studies of these materials, which are predominantly composed of calcium carbonate minerals, it has become evident that crystallization originates from the initial formation of amorphous calcium carbonate (ACC) (4, 5). The pathways by which Fig. 1. Illustration of the shape-preserving amorphous-to-crystalline ACC transforms into crystalline CaCO3 polymorphs transformation in magnesium-containing precursors of calcium carbonate, which has been a topic of ongoing investigation, although is one of the most abundant near-surface biominerals and a structural component many fundamental details remain elusive. In PNAS, Liu of sea urchin spicules and coccolith exoskeletons (both depicted in the blueprint et al. (6) report the time-resolved evolution of ACC to as bioinspired designs). This in vitro process involves two-step nucleation wherein the spheroidal morphology of amorphous calcium carbonate (ACC) is maintained + crystalline calcium carbonate using in situ transmission throughout crystallization of Mg-calcite. The role of Mg2 ions is generally electron microscopy to show that the presence of in- twofold: These additives inhibit nucleation in the solution phase, and they also organic ions leads to the direct transformation of the bring excess water into the precursors to facilitate solute rearrangement within amorphous phase to calcite, all the while preserving the solid phase, thus allowing calcite to retain the original shape of the amorphous particles. the morphology of the original precursor. ACC has become a recognized and frequently investigated form of calcium carbonate owing to its Navrotsky and coworkers (9) who showed that the importance in biomineralization. Six additional crystal- amorphous-to-crystalline transition occurs in the fol- line forms of calcium carbonate (1) include calcite, ara- lowing order (energetically downhill): ACC (more meta- gonite, vaterite, monohydrocalcite, calcium carbonate stable hydrated) → ACC (less metastable hydrated) → hexahydrate (ikaite), and the most recently discovered ACC (anhydrous) → vaterite → aragonite → calcite. · hemihydrate (CaCO3 1/2H2O) (7). ACC is structurally Chemical analysis of ACC phases extracted from complex (i.e., not a single mineral phase) with varying biominerals also reveals the presence of inorganic ions, + degrees of hydration. For example, in sea urchin larval such as Mg2 (4, 10, 11), and organic macromolecules spicules it has been shown that crystallization involves that can facilitate the stabilization of transient ACC three distinct stages: an initial (short-lived) hydrated phases (8, 12). ACC phase, an intermediate (transient) dehydrated In PNAS, Liu et al. (6) elegantly show that the pres- + form of ACC, and finally crystalline calcite (8). This ence of Mg2 ions alters the ACC-to-calcite transition sequence is consistent with thermodynamic data from pathway in a concentration-dependent manner. While aDepartment of Chemical and Biomolecular Engineering, University of Houston, Houston, TX 77204 Author contributions: J.D.R. wrote the paper. The author declares no competing interest. Published under the PNAS license. See companion article 10.1073/pnas.1914813117. 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1922923117 PNAS Latest Articles | 1of3 Downloaded by guest on October 1, 2021 + it has been known that Mg2 incorporation in ACC leads to in- their disorder-to-order transition, resulting in faceted cubes, anal- creased water content (13), Liu et al. confirm this using molecu- ogous to the morphology of calcite in the absence of inorganic lar dynamics to show that the presence of hydrogen-bonded additives, as reported in PNAS. The unique observation by Liu 2− 2+ networks between H2OandCO3 allow for more rapid ion et al. may reflect the ability of Mg ions to act as inhibitors of rearrangements in ACC (14). Introduction of these unstable sites calcification, either on the surfaces of growing crystals (18) or by putatively enables the direct transformation of ACC into calcite their incorporation in calcite leading to defects that increase min- wherein nucleation occurs within the amorphous precursor. This eral solubility (19). process is in stark contrast to calcite nucleation in solution involving ACC has been observed as a precursor to aragonite [55,56], a the dissolution–reprecipitation of amorphous precursors. Liu et al. polymorph of calcite; however, the role of amorphous phases in + suggest that the presence of Mg2 ions in solution inhibit this path- natural systems extends beyond ACC to diverse materials such as way by decreasing the supersaturation with respect to calcite. This, silica in plants and animals (opal), the skeletons of single-celled in turn, allows more time for ACC phases to directly transform into organisms (diatoms), or multicellular tissues (sponges) (1, 20, 21). Mg-calcite by virtue of the incorporated structured water. This pro- Additional examples include magnetite formed from a disordered cess is illustrated in Fig. 1 where the spherical shape of ACC parti- ferrihydrite precursor (22) and the amorphous calcium phosphate + cles infused with Mg2 ions is preserved throughout calcite (ACP) phase detected in the fins of zebrafish (23). Indeed, there is nucleation and growth. During this process, water is expelled from increasing in vivo and in vitro evidence that ACP in collagen matri- the ACC phase during concomitant densification without any no- ces plays an important role in bone formation (24, 25). Analogous ticeable change in particle morphology. Given the presence of to ACC, it is hypothesized that ACP acts as a transient (precursor) + Mg2 ions in numerous biominerals, it is conceivable that this phase during the growth of hydroxyapatite. This further highlights pathway may offer an explanation for the mechanism by which the important role of direct amorphous-to-crystalline transfor- organisms produce exquisite structures where the ACC phases mations in many natural and biological processes. Studies such function as “molds” to preserve shape during mineralization. as those by Liu et al. provide insights into the mechanisms of The nucleation of calcite in (or on) the amorphous solid is biomineralization. Moreover, the discovery of controlled transfor- characteristic of a two-step process that was first observed for mation of amorphous phases to crystals has practical implications proteins (15) but has since become a ubiquitous mechanism in in the manufacturing of new materials. For instance, Tang and the field of crystallization. The physical state of amorphous pre- coworkers (26) previously demonstrated the ability to mold calcite cursors can be quite diverse, ranging from liquid-like droplets into shapes (e.g., stars) and patterned arrays from cross-linked and clusters to gels or nanoparticles. The impact of amorphous ionic oligomers using organic additives. The ability to accomplish species in crystallization is increasingly more evident given the similar processes in ACC using magnesium, an inexpensive earth- significant increase in literature citations emphasizing their roles abundant resource, holds considerable promise for designing facile, as precursors for nucleation as well as growth units during crystal- efficient methods to tailor single crystalline materials with unprec- lization by particle attachment, which both fall under the moniker edented morphologies that cannot be easily achieved through of nonclassical pathways (16). There are additional examples, such conventional routes. as zeolites (nanoporous aluminosilicates) (17), where amorphous Acknowledgments gel-like precursors undergo direct transformation to crystals; J.D.R. acknowledges funding from the Welch Foundation (Award E-1794). however, unlike the evolution of Mg-ACC precursors, the spher- Additional support has been provided by the National Science Foundation (Award ical morphology of zeolite amorphous gels is not preserved during DMR-1710354) and the National Institutes of Health (Award 1R21AI126215-01). 1 L. Addadi, S. Raz, S. Weiner, Taking advantage of disorder: Amorphous calcium carbonate and its roles in biomineralization. Adv. Mater. 15, 959–970 (2003). 2 K. Simkiss, K. Wilbur, Biomineralization, Cell Biology, and Mineral Deposition (Academic Press, New York, 1989). 3 Y. Politi, T. Arad, E. Klein, S. Weiner, L. Addadi, Sea urchin spine calcite forms via a transient amorphous calcium carbonate phase. Science 306, 1161–1164 (2004). 4 L. B. Gower, Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 108, 4551–4627 (2008). 5 S. Weiner, Y. Levi-Kalisman, S. Raz, L. Addadi,

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