The Microstructure of Biogenic Calcite: A View by High‐Resolution Synchrotron Powder Diffraction

Abstract

Biogenic crystals, i.e., crystals produced by living organisms, have attracted a great deal of attention in latter years because of their fascinating microstructures and superior properties. [1][2][3] The interrelation between the microstructure of materials and their properties is a key issue of materials science. Impressive examples of scientific achievements in this field include our ability to control the strength of metals and alloys by annealing-mediated grain size, [4] and bandgap engineering in semiconductor thin film structures by lattice mismatch-mediated interfacial strains. [5] At the same time, unique methods for controlling microstructure and, hence, crystal properties, exist in nature. In fact, organisms can control the polymorphism, [6][7][8] morphology, [9] orientation, and size of crystalline blocks [10] in biogenic crystals by means of organic molecules involved in the biomineralization process. These organic molecules can stabilize an amorphous precursor phase, [11][12][13][14] which might also play an important role in the control of the material properties of the end product. However, not much is yet known about the molecular mechanisms that control the interaction between the organic phase and the growing mineral. In this paper, we shed additional light on these interactions by tracking the microstructure modifications in biogenic calcite after heat treatments at elevated temperatures. Our findings allow us to better understand the microstructure of biocomposites on a nanometer scale, which we believe is of great importance to future design and fabrication of bio-inspired advanced materials. At the end of the 1980s, Berman et al. [15] showed that occluded organic molecules are located within biogenic calcite (CaCO 3 ) crystals and proposed that these intracrystalline molecules reveal chemical recognition to specific atomic planes. The researchers suggested that during biomineralization, the organic macromolecules adhere to specific planes and impede crystal growth in the perpendicular direction, which respectively lowers the size of coherently scattered crystal blocks. [15][16][17] This fact indicates that organisms can also control the preferred orientation (texture) of biogenic crystals. By measuring the "coherent lengths" for X-ray scattering along different directions in biogenic calcite crystals and then comparing these values with those in synthetic calcite, the researchers were able to determine the crystallographic planes on which the organic molecules presumably adhere. However, to date we have practically no information about the specific types of macromolecules, their conformation states, and how exactly they match the mineral structure. Very recently we showed that organisms could control not only the texture, but in some sense the atomic structure of biogenic crystals. Specifically, by using high-resolution X-ray powder diffraction at dedicated synchrotron beam lines, we found anisotropic lattice distortions in mollusk-made aragonite [18] and calcite, [19] as compared to their ...

Protein-induced, previously unidentified twin form of calcite

“…These findings allowed us to conclude that organic macromolecules facilitate the crystal growth in certain directions. Moreover, these molecules are apparently attached to appropriate atomic planes (and the (012)-plane has a favorable atomic structure described above) being in registry with some atomic groups of calcite (16). At this stage, we indicate deep involvement of the specific atomic plane in crystal growth and twinning, both in the presence of organic macromolecules, which may be important for further studies of biomineralization.…”

“…Note that, according to our recent structural study (16), the (012)-plane may play an important role in the growth of biogenic calcite. In particular, we observed that crystallite sizes in calcitic shell P. nobilis, from which the specific protein Caspartin was extracted, are highly anisotropic, reaching the maximum (Ϸ800 nm) along the normal to the (012)-plane.…”

“…We show that during the protein-assisted calcite growth a formerly unknown twinning form has arisen. Nowadays, it is widely accepted that in biogenic crystals specific proteins are incorporated within individual crystallites (13,(16)(17)(18). If they give rise to formerly unidentified twinning planes there, this development will influence the mechanical properties of biogenic crystals produced in nature, which in fact are different as compared with their geological counterparts (11,12).…”

Structure and Properties of Nanocomposites Formed by the Occlusion of Block Copolymer Worms and Vesicles Within Calcite Crystals

“…[ 25,32 ] Nevertheless, comparison of the calcite prisms from a range of mollusks has revealed species-specifi c variations in the microstrain and macrostrain, [ 25,33 ] where these have been attributed to differences in the compositions of the macromolecules, rather than the amounts occluded. [ 34 ] Investigations have therefore often focused on calcite crystals coprecipitated with extracted molecules, where XRD spectra from calcite crystals occluding the small protein perlucin [ 24 ] showed smaller peak shifts than calcite precipitated in the presence of "caspartin," a 17 kDa protein extracted from the calcitic prisms of Pinna nobilis .…”

“…Peak broadening is commonly reported on heating both synthetic and biogenic calcite crystals containing occluded organic phases, where this is attributed to the creation of new interfaces. [ 9,24,25 ] The vesicle/calcite crystals were therefore subjected to isochronous annealing for 30 min at intervals of 100 °C from 100-600 °C and patterns were recorded after the samples had cooled to room temperature after each heating cycle. Peak shifts to smaller d -values began on heating to 300 °C, where this continues on heating to higher temperatures ( Figure 5 a,b).…”