In the course of biomineralization, organisms produce a large variety of functional biogenic crystals that exhibit fascinating mechanical, optical, magnetic and other characteristics. More specifically, when living organisms grow crystals they can effectively control polymorph selection as well as the crystal morphology, shape, and even atomic structure. Materials existing in nature have extraordinary and specific functions, yet the materials employed in nature are quite different from those engineers would select.

One special feature of such crystals is the entrapment of organic molecules within the inorganic crystalline host. Here I will show how we have taken this principle and trslated it to bio-inspired crystal growth to control the electronic properties of various semiconductors.

Some examples include: ZnO and Cu₂O and Hybrid Perovskite. I will discuss the incoporation mechansims, the effect on crystal stricyure and the relation to manipulation of electronic properties.

In this talk, the role that intramineral proteins have played on the shape control as well as in the biomineralization of calcium carbonate in the eggshell´s formation of different avian, crocodiles and dinosaurs will be reviewed. Particularly, the collected eggshells samples of five fossilized eggshells from dinosaurs that roamed the Earth more than 65 million years ago. We characterized the eggshells of the Theropod (bipedal carnivores) and Hadrosauridae (duck-billed dinosaurs) families and an unidentified ootaxon. We have found the existence of some proteins by using micro X-ray absorption and micro-fluorescence techniques at the synchrotron facilities. From these analyses on the dinosaur eggshells, X-ray absorption methods showed a very characteristic organic sulfur bonding similar to that semi-essential proteogenic amino acid L-cysteine, which implies that there is a possibility of having a very old intramineral protein similar to those found in emu and crocodiles. On the other hand, the spectroscopical characterization on these samples showed that calcium carbonate was the primary mineral, with smaller amounts of albite and quartz crystals. Anhydrite, hydroxyapatite, and iron oxide impurities were also present in the shells, which suggests replacement of some of the original minerals during fossilization. Then, with Fourier transform infrared spectroscopy (FT-IR), we found nine amino acids among the five samples, being lysine the only amino acid present in all of them. In addition, we have found evidence of secondary protein structures, including turns, α-helices, β-sheets and disordered structures, which have been preserved for millions of years by being engrained in the minerals. The FT-IR bands corresponding to amino acids and secondary structures could be indicative of ancestral proteins that have not been characterized before. This type of chemical, spectroscopical and structural characterization together with the optical one is a relevant contribution to the field of biomineralization of calcium carbonate research, mainly because these types of samples are unique in their type due to the biological relevance in Mexico and will, therefore, allow us to understand the species that became extinct millions of years ago as well as the importance of calcium carbonate associated to ancient proteins throughout the biomineralization processes on Earth.

Crystal texture of mineral self-organized structures from soda lake water and their implication to early Earth and prebiotic chemistry

M. Getenet, J.M. García-Ruiz

Laboratorio de Estudios Cristalográficos, Instituto Andaluz de Ciencias de la Tierra, Consejo Superior de Investigaciones Científicas–Universidad de Granada, Granada, Spain

juanmanuel.garcia@csic.es

The ability of minerals to precipitate into complex shapes and textures creates fascinating patterns that has not been enough explored in natural scenarios. Among them, silica induced mineral self-organized structures have been suggested to be relevant for the earliest stages of the planet, when alkaline silica-rich oceans evolve from methane-rich to CO and CO₂-rich atmosphere and hydrosphere [1]. Under these geochemical conditions of the Hadean Earth, it is thought that silica-carbonate biomorphs and silica-metal hydr(oxide) gardens were actually forming in the alkaline oceans, rich in silica and in carbonate. In this work, we focus on chemical gardens, which are hollow membranes formed via abiotic precipitation when metal salts immerse into aqueous solutions containing anions such as silicate, carbonate, or phosphates [2]. It has been shown that these space-compartmentalized membranes are small batteries [3] that selectively catalyse the synthesis of prebiotically relevant compounds such as carboxylic acids, amino acids, and nucleobases by condensation of formamide [4]. Here, we experimentally demonstrate the formation of carbonate gardens using carbonate-rich alkaline soda lake water (Lake Magadi, Southern Kenyan rift valley). We have studied in detail the mineral composition and crystallinity of these “natural” carbonate gardens by SEM-EDX, Raman microscopy, infrared spectroscopy and X-ray diffraction, and compared to other silica and carbonate gardens made from laboratory solutions. Our result suggests that mineral self-organization could have been a geochemically plausible phenomenon in carbonate-rich closed basin environments of the early Earth, and Earth-like planets. We also discuss the implications of the textural properties of the mineral membranes to develop electrochemical potential that could catalyze prebiotic reactions.

[1] García-Ruiz, J.M., van Zuilen, M. & Bach, W. (2020). Phys Life Rev. 34-35, 62-82.

[2] Kellermeier, M., Glaab, F., Melero-García, E., & García-Ruiz, J. M. (2013). Research Methods in Biomineralization Science, edited by J.J. De Yoreo, pp. 225-256. San Diego: Academic Press.

[3] Glaab, F., Kellermeier, M., Kunz, W., Morallon, E. & Garcia-Ruiz, J. M. (2012). Angew. Chem. 124, 4393

[4] Saladino, R., Di Mauro, E. & García-Ruiz, J. M. (2019). Chem. Eur. J. 25, 3181.

Keywords: chemical gardens; self-organization; biomorphs; early Earth; Soda lakes

Acknowledgments: We acknowledge funding from the European Research Council under grant agreement no. 340863, from the Ministerio de Economía y Competitividad of Spain through the project CGL2016-78971-P and Junta de Andalucía for financing the project P18-FR-5008. M.G. acknowledges Grant No. BES-2017-081105 of the Ministerio de Ciencia, Innovacion y Universidades of the Spanish government.

Through controlled biomineralization, organisms yield complicated structures with specific functions. Here, Jania sp., an articulated coralline red alga that secretes high-Mg calcite as part of its skeleton, is in focus. It is shown that Jania sp. exhibits a remarkable structure, which is highly porous (with porosity as high as 64 vol%) and reveals several hierarchical orders from the nano to the macroscale. It is shown that the structure is helical, and proven that its helical configuration provides the alga with superior compliance that allows it to adapt to stresses in its natural environment. Thus, the combination of high porosity and a helical configuration result in a sophisticated, light-weight, compliant structure [1]. Very recently, we also showed that the high-Mg calcite cell wall nanocrystals of Jania sp. are arranged in layers with alternating Mg contents. Such non-homogenous elemental distribution assists the alga in preventing fracture caused by crack propagation. We further discover that each one of the cell wall nanocrystals in Jania sp. is not a single crystal as was previously thought, but rather comprises Mg-rich calcite nanoparticles demonstrating various crystallographic orientations, arranged periodically within the layered structure [2]. We also show that these Mg-rich nanoparticles are present in yet another species of the coralline red algae, Corallina sp., pointing to the generality of this phenomenon. To the best of our knowledge this is a first report on the existence of Mg-rich nanoparticles in the coralline red algae mineralized tissue. We envisage that our findings on the bio-strategy found in the alga to enhance the fracture toughness will have an impact on the design of structures with superior mechanical properties.

1.Bianco‐Stein N, Polishchuk I, Seiden G, Villanova J, Rack A, Zaslansky P and Pokroy B. Helical Microstructures of the Mineralized Coralline Red Algae Determine Their Mechanical Properties. Adv Sci 2020; 7:2000108.

2. Bianco-Stein N, Polishchuk I, Lang A, Atiya G, Villanova J, Zaslansky P, Katsman A and Pokroy B. Structural and Chemical Variations in the Calcitic Segments of Coralline Red Algae Lead to Improved Crack Resistance. Acta Biomater 2021; DOI:10.1016/j.actbio.2021.05.040.

Bone is a strong yet light-weight material, where several mechanical properties originate from the orientation of their molecular components – collagen fibrils mineralized with calcium phosphate in a hydroxyapatite (HA)-like structure. Knowledge of the three-dimensional (3D) microscopic orientation arrangements of the mineralized collagen in macroscopic samples, allows for a deeper understanding of the mechanical properties of bone, leading to an improved understanding of bone and cartilage-related diseases such as osteochondrosis and osteoarthritis. The distinct patterns in the HA mineral orientation can also be used to locate embedded fibres of muscle attachments in vertebrates in both modern and fossil bones. This is crucial for reconstructing evolutionary scenarios and biomechanical models of extinct species, for which soft tissues are lost during fossilization.

X-ray diffraction computed tomography (XRD-CT) is an emerging imaging technique, allowing non-destructive 3D mapping of samples with material-specific contrast [1] and has recently also been demonstrated with orientational contrast [2–4]. In this presentation we demonstrate the application of XRD-CT to study the microstructure of different types of bones without destructive sample sectioning. The HA orientation in a tibial cross-section from a fossil stem amniote Discosauriscus austriacus is used to reveal the location of muscle attachments, shown in Figs. 1a and 1b. XRD-CT can also be used to study the HA orientation close to the bone-cartilage interface in the developing bone, as illustrated in Figs. 1c and 1d. XRD-CT is becoming a powerful tool that allows studying the orientation of mineralized structures in bone, and is likely to be increasingly used due to the advent of new synchrotron sources and improved numerical methods for tomographic reconstruction.

[1] Harding, G., Kosanetzky, J. & Neitzel, U. (1987). Med. Phys. 14, 515.

[2] Liebi, M., Georgiadis, M., Menzel, A., Schneider, P., Kohlbrecher, J., Bunk, O. & Guizar-Sicairos, M. (2015). Nature. 527, 349.

[3] Mürer, F. K., Sanchez, S., Álvarez-Murga, M., Di Michiel, M., Pfeiffer, F., Bech, M. & Breiby, D. W. (2018). Sci. Rep. 8, 1.

[4] Mürer, F. K., Chattopadhyay, B., Madathiparambil, A. S., Tekseth, K. R., Di Michiel, M., Liebi, M., Lilledahl, M. B., Olstad, K. & Breiby, D. W. (2021). Sci. Rep. 11, 1.