Nacre tablet thickness records formation temperature in modern and fossil shells

Gilbert, Benjamin; Bergmann, Kristin; Myers, Christopher W.; Marcus, Matthew A.; DeVol, Ross T.; Sun, Chang‐Yu; Blonsky, Adam Z.; Tamre, Erik; Zhao, Jessica; Karan, Elizabeth A; Tamura, Nobumichi; Lemer, Sarah; Giuffre, Anthony J.; Giribet, Gonzalo; Eiler, John M.; Knoll, Andrew H.

doi:10.1016/j.epsl.2016.11.012

Cited by 53 publications

(87 citation statements)

References 58 publications

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“…As can be seen, a number of studies were successful in applying a variety of thermodynamic and kinetic models to describe the process of its formation and final morphology. Moreover, sensitivity of nacre ultrastructure to environmental pressure and temperature in which the organisms reside was previously demonstrated . Nevertheless, despite the work presented in this section, we are far from asserting a comprehensive analytical description of structural formation in nacre or even defining the parameters that determine its morphology.…”

Section: Evidence Of Spontaneous Growthmentioning

confidence: 87%

Thermodynamic Aspects of Molluscan Shell Ultrastructural Morphogenesis

Zlotnikov

Schoeppler

2017

Adv Funct Materials

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Over the years, molluscan shells have become an exemplar model system to study the process of mineral formation by living organisms, the process of biomineralization. Typically, the shells consist of a number of mineralized ultrastructural motifs, each exhibiting a specific mineral-organic composite architecture. These are made of calcium carbonate building blocks having a well-defined three-dimensional morphology that is significantly different from the shape of inorganically formed counterparts. Shell ultrastructures are known to form via a biologically controlled extracellular mineralization pathway in which the organism has no direct control over mineral formation. The cellular tissue, responsible for shell biomineralization, forms an organic framework and sets-up the physical conditions necessary for the deposition of a specific morphology, whereas the growth of the mineral part of the shell proceeds spontaneously via the process of self-assembly. In this feature article, the ability to employ thermodynamic models from classical materials science to describe the process of self-assembly and structural evolution of a variety of shell architectures is reviewed. Having the potential to offer an analytical framework to express ultrastructure formation in time and in space, these models not only provide a deeper insight into shell biomineralization, but also suggest tools for novel composite materials design.

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Section: Evidence Of Spontaneous Growthmentioning

confidence: 87%

Thermodynamic Aspects of Molluscan Shell Ultrastructural Morphogenesis

Zlotnikov

Schoeppler

2017

Adv Funct Materials

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“…56,63,64 We map the crystal orientations using polarization-dependent imaging contrast (PIC)-mapping, a method based on X-ray linear dichroism in carbonate minerals, which was initially only semiquantitative, 65−69 but is now fully quantitative in providing the c-axis orientation of carbonate minerals in three dimensions, expressed with color, including hue and brightness. 40,70,71 RESULTS AND DISCUSSION Figure 2a shows a PIC-map of the CoCs in the skeleton of a Stylophora pistillata coral. Orientations of the aragonite crystals are color-coded in this map according to their c′-axes, which are the projections of the crystals' c-axes onto the polarization plane in a photoemission electron spectromicroscopy (PEEM) experiment.…”

mentioning

confidence: 99%

“…The pixel intensity in the set of data used to generate a PIC-map varies as a function of the polarization angle χ according to a cosinesquare function 71,76 described by eq 1 in the Methods. Figure 6a shows a plot of fit parameters a/b versus c′ for all pixels within three S. pistillata coral bundles.…”

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confidence: 99%

Spherulitic Growth of Coral Skeletons and Synthetic Aragonite: Nature’s Three-Dimensional Printing

Sun¹,

Marcus

Frazier³

et al. 2017

ACS Nano

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Coral skeletons were long assumed to have a spherulitic structure, that is, a radial distribution of acicular aragonite (CaCO 3 ) crystals with their c-axes radiating from series of points, termed centers of calcification (CoCs). This assumption was based on morphology alone, not on crystallography. Here we measure the orientation of crystals and nanocrystals and confirm that corals grow their skeletons in bundles of aragonite crystals, with their caxes and long axes oriented radially and at an angle from the CoCs, thus precisely as expected for feather-like or "plumose" spherulites. Furthermore, we find that in both synthetic and coral aragonite spherulites at the nanoscale adjacent crystals have similar but not identical orientations, thus demonstrating by direct observation that even at nanoscale the mechanism of spherulite formation is non-crystallographic branching (NCB), as predicted by theory. Finally, synthetic aragonite spherulites and coral skeletons have similar angle spreads, and angular distances of adjacent crystals, further confirming that coral skeletons are spherulites. This is important because aragonite grows anisotropically, 10 times faster along the c-axis than along the a-axis direction, and spherulites fill space with crystals growing almost exclusively along the c-axis, thus they can fill space faster than any other aragonite growth geometry, and create isotropic materials from anisotropic crystals. Greater space filling rate and isotropic mechanical behavior are key to the skeleton's supporting function and therefore to its evolutionary success. In this sense, spherulitic growth is Nature's 3D printing. KEYWORDS: Ion attachment, crystallization by particle attachment, CPA, biomineralization, PEEM, PIC-mapping, mesocrystal S pherulites are polycrystalline structures in which acicular crystals radiate from a common center and grow approximately synchronously so the final shape of a spherulite resembles a sphere. 1−7 Figure 1 shows two types of spherulites: "spherical spherulite", in which the crystal fibers start from a point, or "plumose spherulite", in which crystal fibers radiate at an angle from the line. 7 Spherulites start forming as an aggregate of parallel acicular crystals termed "fibers", then form a "sheaf of wheat" structure, and with the growth of more fibers eventually become complete spheres. 8 In an ideal spherulite, fibers radiate from the center and contain all possible orientations within the sphere. Since the fast-growing axis in aragonite (CaCO 3 ) is the c-axis, 9 in spherulites each fiber elongation direction coincides with the crystalline c-axis. 10,11 In real spherulites, biogenic 12 and synthetic, 7 the crystal orientations are not perfectly radial nor continuously varying with angle, they deviate slightly from radial and exhibit small but abrupt changes in orientation, termed "branching". In Figure 1 branching angles are smaller than 30°in direction and in crystal lattice orientation. This is distinct from crystallographic branching, which occurs in sno...

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“…In P. fucata grown in Japanese lagoons, pearl growth was also found to be strongly dependent on the seasonal temperature: monthly pearl growth decreased from the hottest month (August) to the coldest (December) (Muhammad et al, 2017). The hypothesis that nacre ultrastructure in molluscs depends on environmental temperature at the time of biomineral deposition (Olson et al, 2012) was demonstrated in pen shells (Gilbert et al, 2017). The challenge of controlling the thickness of nacre tablets is at the level of the lustre; indeed, the fine layers of nacre enhance pearls' lustre (Matsui, 1958in Nagai, 2013.…”

Section: Rotation Speed Is Controlled By Pearl Shapementioning

confidence: 96%

Influence of temperature and pearl rotation on biomineralization in the pearl oyster Pinctada margaritifera

Moullac

Schuck

Chabrier

et al. 2018

Journal of Experimental Biology

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The objective of this study was to observe the impact of temperature on pearl formation using an integrative approach describing the rotation of the pearls, the rate of nacre deposition, the thickness of the aragonite tablets and the biomineralizing potential of the pearl sac tissue though the expression level of some key genes. Fifty pearl oysters were grafted with magnetized nuclei to allow the rotation of the pearls to be described. Four months later, 32 of these pearl oysters were exposed to four temperatures (22, 26, 30 and 34°C) for 2 weeks. Results showed that the rotation speed differed according to the movement direction: pearls with axial movement had a significantly higher rotation speed than those with random movement. Pearl growth rate was influenced by temperature, with a maximum between 26 and 30°C but almost no growth at 34°C. Lastly, among the nine genes implicated in the biomineralization process, only expression was significantly modified by temperature. These results showed that the rotation speed of the pearls was not linked to pearl growth or to the expression profiles of biomineralizing genes targeted in this study. On the basis of our results, we consider that pearl rotation is a more complex process than formerly thought. Mechanisms involved could include a strong environmental forcing in immediate proximity to the pearl. Another implication of our findings is that, in the context of ocean warming, pearl growth and quality can be expected to decrease in pearl oysters exposed to temperatures above 30°C.

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Nacre tablet thickness records formation temperature in modern and fossil shells

Cited by 53 publications

References 58 publications

Thermodynamic Aspects of Molluscan Shell Ultrastructural Morphogenesis

Thermodynamic Aspects of Molluscan Shell Ultrastructural Morphogenesis

Spherulitic Growth of Coral Skeletons and Synthetic Aragonite: Nature’s Three-Dimensional Printing

Influence of temperature and pearl rotation on biomineralization in the pearl oyster Pinctada margaritifera

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