Molecular Dynamics of Ion Hydration in the Presence of Small Carboxylated Molecules and Implications for Calcification

Abstract

The aspartate-rich macromolecules found at nucleation sites of calcifying organisms are widely implicated in regulating biomineral formation. Anecdotal evidence suggests that their ability to influence the onset of nucleation and composition of calcified structures may arise from effects on ion hydration. This study investigates the interactions of acidic amino acids and dipeptides with hydrated cations using molecular dynamics. By monitoring the hydration states of Mg2+, Ca2+, and Sr2+ during their approach to negatively charged molecules, we show that carboxylate moieties of Asp promote dehydration of Ca2+ and Sr2+. A contact ion pair (CIP) is not required to disrupt cation hydration, and we demonstrate that reductions and rearrangements of first shell water can begin at ion-Asp separation distances as large as approximately 4.9 A for Ca2+ and approximately 5.1 A for Sr2+. CIP formation between Ca2+ and Sr2+ and carboxylate groups decreases the total first shell coordination number from an average of 8.0 and 8.4 in bulk water to 7.5 and 8.0, respectively. The energy barrier to physically replacing waters about Ca2+ with carboxylate oxygen atoms is small (approximately 2 kcal/mol) as compared to a somewhat larger barrier for Sr2+ (approximately 4 kcal/mol). This may be explained by differences in the strength of Coulombic interactions between the cations and the Asp, resulting in different paths of approach toward Asp for Ca2+ and Sr2+. In contrast, the primary solvation shell of Mg2+ remains largely unchanged during interactions with Asp until the abrupt physical replacement of water by carboxylate oxygen atoms, which comes at a high energetic cost. These insights support the claim that carboxylated biomolecules increase the growth rate of calcite by lowering the energy barrier to Ca2+ dehydration. The findings also suggest a physical basis for the idea that ion-specific behaviors of Ca2+ and Mg2+ in cellular systems arise from a critical balance between water binding in the ion hydration shells versus their interactions with ligands present in intracellular environments.

Testing the cation-hydration effect on the crystallization of Ca–Mg–CO 3 systems

“…Nesquehonite is the most commonly formed phase under low temperature and pressure [e.g., 25°C and a pCO 2 of ∼10 −2 atm (25-27)], whereas hydromagnesite and other basic forms become dominant in an intermediate temperature range [e.g., 40-60°C (28-30)]. Despite being the most stable phase at all conditions, the anhydrous salt, magnesite, was reported to form only at a much elevated temperature and pressure [e.g., ∼90-180°C and pCO 2 > 50 atm (31-34)].The difficulty in precipitating magnesite (and dolomite) from ambient aqueous solutions was first suggested to be related to the strong hydration status of Mg 2+ ions in a hypothesis (35) that has since been corroborated by numerous pieces of circumstantial evidence (15,22,36). Indeed, both experimental and computational studies revealed the presence of a stable inner-sphere hydration shell around Mg 2+ ions that contains six water molecules Significance Magnesium-bearing carbonate minerals play critical roles in the health and function of the Earth system because they constitute a significant fraction of lithosphere carbon reservoir and build skeletal structures for the majority of marine invertebrate organisms.…”

“…The difficulty in precipitating magnesite (and dolomite) from ambient aqueous solutions was first suggested to be related to the strong hydration status of Mg 2+ ions in a hypothesis (35) that has since been corroborated by numerous pieces of circumstantial evidence (15,22,36). Indeed, both experimental and computational studies revealed the presence of a stable inner-sphere hydration shell around Mg 2+ ions that contains six water molecules Significance Magnesium-bearing carbonate minerals play critical roles in the health and function of the Earth system because they constitute a significant fraction of lithosphere carbon reservoir and build skeletal structures for the majority of marine invertebrate organisms.…”

“…Thus, it becomes logical to surmise that the dolomite problem and the magnesite problem probably share the same root, that is, the difficulty to incorporate unhydrated magnesium ions into carbonate from aqueous solutions without appealing to temperature and/or pressure changes. Given the 50% abundance of dolomites in the world's carbonate reservoirs (6,17) and the potential of magnesium carbonate for carbon sequestration (18,19), as well as the critical role of Mg in carbonate biomineralization (20)(21)(22), it is safe to assume that scientific interests in the Ca-Mg-CO 3 system will remain for years to come.…”

Dynamic Processes in Biology, Chemistry, and Materials Science: Opportunities for UltraFast Transmission Electron Microscopy - Workshop Summary Report

“…However, the achievable time scales are limited to the millisecond range 24,93 . As nanoparticle nucleation and growth is strongly affected by solvation and dynamic chemical interactions at the solid-liquid interface, 94 water is critical for these studies.…”

“…A variety of studies have suggested or shown that the liquid confined in nanospace volumes exhibits properties different from the bulk, such as increased viscosity 78,94,[96][97][98] . In addition, the diffusion of solution into the nanospaces between two adjacent nanocrystals may be retarded or inhibited.…”