Organic–inorganic interfaces and spiral growth in nacre

Abstract

Nacre, the crown jewel of natural materials, has been extensively studied owing to its remarkable physical properties for over 160 years. Yet, the precise structural features governing its extraordinary strength and its growth mechanism remain elusive. In this paper, we present a series of observations pertaining to the red abalone (Haliotis rufescens) shell's organic-inorganic interface, organic interlayer morphology and properties, large-area crystal domain orientations and nacre growth. In particular, we describe unique lateral nanogrowths and paired screw dislocations in the aragonite layers, and demonstrate that the organic material sandwiched between aragonite platelets consists of multiple organic layers of varying nano-mechanical resilience. Based on these novel observations and analysis, we propose a spiral growth model that accounts for both [001] vertical propagation via helices that surround numerous screw dislocation cores and simultaneous h010i lateral growth of aragonite sheet structure. These new findings may aid in creating novel organic-inorganic micro/nano composites through synthetic or biomineralization pathways. Keywords: nacre; biomineralization; crystal growthBiomaterials provide fascinating examples of nature's ability to assemble structures of remarkable strength and toughness (Aksay et al. 1996;Addadi & Weiner 1997;Sanchez et al. 2005). Particularly well studied is nacre, or mother of pearl, a composite of aragonite CaCO 3 and organic matrix that is 3000 times more fracture resistant than the pure mineral (Currey 1977;Jackson et al. 1988). Its unique mechanical properties are attributed to a structure of polygonal aragonite platelets, approximately 5 mm across by 0.5 mm thick, wrapped in polysaccharide and protein fibres ( Weiner 1986;Jackson et al. 1989). There exist two principal types of nacre structure: columnar, composed of stacked platelets of rather uniform size with coinciding centres, and sheet, in which the centres of platelets rest on the interfaces between underlying platelets, as in a brick wall. Columnar nacre is known to be deposited in a narrow zone at the margin of the shell, while sheet nacre is deposited over most of the inner surface (Hedegaard 1997). Yet, after 160 years of scientific investigation (Carpenter 1847), the precise features governing nacre's extraordinary strength remain elusive. This is largely due to the lack of structural characterization at the atomic and nanometre scale. Understanding the physical and mechanical properties of nacre at nanometre scale dimensions could lead to the synthesis of novel materials with unprecedented performance.Here, we present a series of observations, using highresolution imaging and nanoscale force measurements, on structural features at the organic-inorganic interface, morphological and mechanical properties of the organic matrix, crystal directions and ultimately sheet nacre growth. We reveal nanometre-scale growths on vertical (010) platelet faces and new details of asperities, i.e. small protrusions, on horizonta...

Ultrastructure, chemistry and mineralogy of the growing shell of the European abalone Haliotis tuberculata

“…In abalone, there is already detailed knowledge on the microstructure and mineralogy of the adult shell (Dauphin et al, 1989;Lin and Meyers, 2005) and the inner nacreous layer has been extensively studied owing to its remarkable physical properties (Nakahara, 1991;Fritz et al, 1994;Nassif et al, 2005;Bezares et al, 2008;Gilbert et al, 2008;Yao et al, 2009). However, the early steps of shell formation and initial stages of calcification in larval gastropods remains poorly understood (Jablonski and Lutz, 1980;Kniprath, 1981;Eyster, 1986).…”

Aragonite twinning in gastropod nacre

“…These pores were observed through electron microscopy [6,25], atomic force microscopy, and scanning ion conductance microscopy [9]. In addition, direct observations of the mineral bridges have been carried out through high-resolution transmission electron microscopy (TEM) [26][27][28].…”

The Materiome

“…However, the architecture of the gastropod shell, adequately summarized at the micro-scale as a composite of organic layers and mineralized platelets, explicates only the highest level of hierarchy. Hierarchical sublevels including the protein-based composure of the organic layer(s) [39,40] and the properties of the organic-mineral interfaces [41] are still being investigated in nacreous materials, and are ultimately required for a complete description of the materiome and potential design of de novo synthetic materials [42].…”