A Review of Phosphate Mineral Nucleation in Biology and Geobiology

Abstract

Relationships between geological phosphorite deposition and biological apatite nucleation have often been overlooked. However, similarities in biological apatite and phosphorite mineralogy suggest that their chemical formation mechanisms may be similar. This review serves to draw parallels between two newly described phosphorite mineralization processes, and proposes a similar novel mechanism for biologically controlled apatite mineral nucleation. This mechanism integrates polyphosphate biochemistry with crystal nucleation theory. Recently, the roles of polyphosphates in the nucleation of marine phosphorites were discovered. Marine bacteria and diatoms have been shown to store and concentrate inorganic phosphate (Pi) as amorphous, polyphosphate granules. Subsequent release of these P reserves into the local marine environment as Pi results in biologically induced phosphorite nucleation. Pi storage and release through an intracellular polyphosphate intermediate may also occur in mineralizing oral bacteria. Polyphosphates may be associated with biologically controlled apatite nucleation within vertebrates and invertebrates. Historically, biological apatite nucleation has been attributed to either a biochemical increase in local Pi concentration or matrix-mediated apatite nucleation control. This review proposes a mechanism that integrates both theories. Intracellular and extracellular amorphous granules, rich in both calcium and phosphorus, have been observed in apatite-biomineralizing vertebrates, protists, and atremate brachiopods. These granules may represent stores of calcium-polyphosphate. Not unlike phosphorite nucleation by bacteria and diatoms, polyphosphate depolymerization to Pi would be controlled by phosphatase activity. Enzymatic polyphosphate depolymerization would increase apatite saturation to the level required for mineral nucleation, while matrix proteins would simultaneously control the progression of new biological apatite formation.

Apatite Biominerals

“…In addition, other functional roles have been attributed to apatite biominerals like homeostasis or the inactivation of toxic elements. Several reviews have been published on this subject with different approaches focusing on crystal structures, and calcium phosphate precursors [6], the role of OH-channels [7], the role of unstable amorphous precursors [8], the role of polyphosphates [9], general view including the organic matrices [10], apatite biominerals and biomimetic processing and materials [11], and mineralogical oriented reviews [12]. This review aims to present and discuss the specific characteristics of biomineral apatites and illustrate how these characteristics and the resulting mineral properties have been employed in the adaptation for specific biological functions, in the case of vertebrate hard tissues (bone, dentine and enamel).…”

The Bruneau Woodpile: A Miocene Phosphatized Fossil Wood Locality in Southwestern Idaho, USA

“…Microbial processes may play a role in phosphatization of faunal remains and phosphatic mineral deposits [63,64], but possible involvement of microbes during phosphatization of wood has not been studied. Previous reports provide abundant evidence for the recognition of microbial associations in aquatic mineral deposits where mineral deposition is facilitated by microbial mats or biofilms.…”

A materials science vision of extracellular matrix mineralization

“…Extracellular polyphosphate (polyPi, an extended analogue of PPi) also serves in the transport and compartmentalization of phosphates 22 . In the same way that glucose concentration is controlled by formation and destruction of glycogen, Pi concentration is regulated by formation and destruction of polyPi -a substrate for enzymatic cleavage in the skeleton 23 . PolyPi-packed granules chelate calcium ions, forming neutrally charged and amorphous complexes 23 ; thus it seems that calcium-binding PPi and polyPi are a bioreservoir of mineral ions and effectively preclude collagen-based soft tissues from undesired mineralization.…”

“…In soft tissues not destined for mineralization, the ratio of PPi/Pi remains high to inhibit mineralization. It has been suggested that polyPi granules contain alkaline phosphatase and other proteins; the notion here being that if alkaline phosphatase is activated, hydroxyapatite nucleates within the granule, displaces the protein component to the granule surface to result in the formation of a crystalline core coated with an amorphous shell 23 .…”