Contrasts between organic participation in apatite biomineralization in brachiopod shell and vertebrate bone identified by nuclear magnetic resonance spectroscopy

Abstract

Unusually for invertebrates, linguliform brachiopods employ calcium phosphate mineral in hard tissue formation, in common with the evolutionarily distant vertebrates. Using solidstate nuclear magnetic resonance spectroscopy (SSNMR) and X-ray powder diffraction, we compare the organic constitution, crystallinity and organic matrix -mineral interface of phosphatic brachiopod shells with those of vertebrate bone. In particular, the organic -mineral interfaces crucial for the stability and properties of biomineral were probed with SSNMR rotational echo double resonance (REDOR). Lingula anatina and Discinisca tenuis shell materials yield strikingly dissimilar SSNMR spectra, arguing for quite different organic constitutions. However, their fluoroapatite-like mineral is highly crystalline, unlike the poorly ordered hydroxyapatite of bone. Neither shell material shows 13 Cf 31 Pg REDOR effects, excluding strong physico-chemical interactions between mineral and organic matrix, unlike bone in which glycosaminoglycans and proteins are composited with mineral at sub-nanometre length scales. Differences between organic matrix of shell material from L. anatina and D. tenuis, and bone reflect evolutionary pressures from contrasting habitats and structural purposes. The absence of organic -mineral intermolecular associations in brachiopod shell argues that biomineralization follows different mechanistic pathways to bone; their details hold clues to the molecular structural evolution of phosphatic biominerals, and may provide insights into novel composite design.

Characterization of the phosphatic mineral of the barnacle Ibla cumingi at atomic level by solid-state nuclear magnetic resonance: comparison with other phosphatic biominerals

“…A detailed, atomic-level knowledge of the structures of the mineral phase and its interface with the embedding organic matrix is not only likely to provide clues about the evolution of calcium phosphate biomineralization strategies in general, but may also inform efforts to design new biomimetic and biocompatible mineral-organic composite materials [21,22]. This study extends previous work contrasting linguliform brachiopod biomineral with vertebrate bone [16] to the biomineral from a species of iblid barnacle. …”

“…Multinuclear SSNMR ( 13 C and 31 P) shows that the surface of vertebrate bone mineral makes intimate atomic-scale molecular connections with organic matrix macromolecules [17,18] and citrate [19]. By contrast, these close contacts between mineral and the organic matrix are not found in the phosphatic shell material of the linguliform brachiopods, suggesting a completely different molecular biomineralization strategy [16]. Similar multinuclear SSNMR techniques exploiting 1 H and 31 P have also thrown new light on phosphatic biomineral structure and composition in ways not possible using other techniques.…”

“…Solid-state nuclear magnetic resonance spectroscopy (SSNMR) [15] is a powerful technique for studying the atomic level structure of phosphatic biominerals [16], for reasons treated in detail in the latter reference. Multinuclear SSNMR ( 13 C and 31 P) shows that the surface of vertebrate bone mineral makes intimate atomic-scale molecular connections with organic matrix macromolecules [17,18] and citrate [19].…”

Calcium orthophosphates (CaPO 4 ): Occurrence and properties

“…The same was suggested for dentine and enamel (Jodaikin et al 1988;Fincham et al 1995) (see ''Teeth''), as well as for more primitive living organisms. For example, in the shell of the fossil marine animal Lingula brachiopod unguis that consists of a biological apatite, the crystal c-axes are oriented parallel to the b-chitin fibrils (Leveque et al 2004;Williams et al 1998;Rohanizadeh and LeGeros 2007;Neary et al 2011). Therefore, the orientation of biological apatite crystals parallel to the long axes of the organic framework could be a general feature of the CaPO 4 biomineralization.…”

Petrography and the REE-composition of apatite in the Paleoproterozoic Pilgujärvi Sedimentary Formation, Pechenga Greenstone Belt, Russia

“…Joosu et al, 2015 andWright et al, 1987). However, biologically precipitated apatite is a thermodynamically unstable, hydroxyapatite-like, poorly crystalline phase (Neary et al, 2011) that is readily recrystallized during diagenesis (Trueman, 2013). Consequently, biogenic hydroxylapatite has been shown to be an ambiguous carrier of information about primary redox conditions, specifically due to recrystallization and adsorption effects (e.g.…”