Thermodynamic basis for evolution of apatite in calcified tissues

Abstract

International audienceBone remodeling and tooth enamel maturation are biological processes that alter the physico-chemical features of biominerals with time. However, although the ubiquity of bone remodeling is clear, why is well-crystallized bone mineral systematically replaced by immature nanocrystalline inorganic material? In enamel, a clear evolution is also seen from the first mineral formed during the secretory stage and its mature well-crystalline form, which then changes little in the adult tooth. This contribution provides the thermodynamic basis underlying these biological phenomena. We determined, for the first time, the energetics of biomimetic apatites corresponding to an increasing degree of maturation. Our data point out the progressive evolution of the enthalpy (ΔHf°) and free energy (ΔGf°) of formation toward more negative values upon maturation. Entropy contributions to ΔGf° values remained small compared to enthalpy contributions. ΔHf° varied from −12 058.9 ± 12.2 to −12 771.0 ± 21.4 kJ/mol for maturation times increasing from 20 min to 3 weeks, approaching the value for stoichiometric hydroxyapatite, −13 431.0 ± 22.7 kJ/mol. Apatite thermodynamic stability increased as its composition moved toward stoichiometry. These findings imply diminishing aqueous solubility of calcium and phosphate ions as well as decreased surface reactivity. Such thermodynamically driven maturation is favorable for enamel maturation since this biomineral is intended to resist external aggressions such as contact with acids. In contrast, maintaining a metastable highly reactive and soluble form of apatite is essential to the effective participation of bone as a source of calcium and phosphate for homeostasis. Therefore our data strongly suggest that, far from being trivial, the intrinsic thermodynamic properties of apatite mineral represent a critical driving force for continuous bone remodeling, in contrast to current views favoring a purely biologically driven cycle. These thermodynamic data may prove helpful in other domains relating, for example, to apatite-based biomaterials development or in the field of (geo)microbiology

Apatite Biominerals

“…However, as already discussed in the previous sections of this review, we should bear in mind that biological apatites are far from the stoichiometric HA in terms of composition, defects, solubility and thus thermodynamic properties [109]. Consequently, the position of synthetic and biological non-stoichiometric apatites in a free enthalpy variation diagram ( Figure 5) would not be that of HA, but would probably be between that of HA and OCP and probably closer to that of OCP [110]. In addition there are uncertainties of the supersaturation ratio at the time and place of mineral formation.…”

A comprehensive guide to experimental and predicted thermodynamic properties of phosphate apatite minerals in view of applicative purposes

“…For example, in the case of fluorapatite Ca 10 (PO 4 ) 6 F 2 , a decomposition into contributions of 9CaO + 3P 2 O 5 + 1CaF 2 could be considered, and this may be generalized to any end-member in the form 9MO + 3P 2 O 5 + 1MX 2 . In reality, this type of approximation is rather optimistic and does not generally represent the actual behavior of complex oxides: this is for example pointed out by the fact that the enthalpy of formation ''from the oxides'' is not zero, as we showed for example for nonstoichiometric apatites [15] or in other systems [82,83]. However, it was interesting at this point to check the values obtained for apatites by using this simple binary-compounds-additive method, and to compare relative errors to those previously reached by VBT.…”

“…regularly arise. Besides, stoichiometric end-members are not the only phases of interest, especially when aqueous precipitation at moderate temperature is involved [5,14]: non-stoichiometric apatite compositions are generally obtained in such conditions (unless perhaps for very long periods of time), and their thermochemical features are bound to depart from those of their stoichiometric parent phase, as we showed recently in the case of biomimetic apatites [15].…”

Evaluating the consequences of diagenesis and fossilization on bioapatite lattice structure and composition

“…In life, dynamic in vivo lattice changes and structural flexibility regulate acid-base chemistry and enhance ion exchange for the vertebrate host, such as with calcium (Ca), sodium (Na), and carbonate (CO 3 2-) (Bergstrom and Wallace, 1954;Green and Kleeman, 1991;Rollin-Martinet et al, 2013). There are two distinct Ca sites (or types) within the apatite lattice, differentiated based on shared bonds with neighboring oxygen atoms.…”

“…Some of the enrichment is due to cation exchange at Ca sites from monovalent (e.g., Na + ), divalent (e.g., Fe 2+ , Sr 2+ , Mn 2+ ), trivalent (e.g., Fe 3+ , REE 3+ ), tetravalent (e.g., U 4+ ), and hexavalent (e.g., U 6+ ) cations (Pan and Fleet, 2002). But, protonation of PO 4 3-and OH -at the mineral surface may also open the apatite lattice to substitution with CO 3 2- (Rollin-Martinet et al, 2013), which may allow for fluoride (F -) or chloride (Cl -) ion substitution in place of OH -. Such substitutions would result in a fluoride-and carbonate enriched apatite phase, although chloride enrichment in fossil bones is less common (e.g., Hubert et al, 1996).…”