Biomimetic Strontium Sulfate Mineralization Studied by Multiscale Microscopy and Vibrational Spectroscopy

In the present study, we investigated the in-vitro crystallization of strontium sulfate (celestite, SrSO₄) in the presence of organic matter, including the synthetic polymer poly(sodium 4-styrenesulfonate), the poly amino acid poly(<i>L</i>-glutamic acid), the polysaccharide poly(galacturonic acid) and the amino acid <i>L</i>-aspartic acid. In nature, biogenic SrSO₄ occurs in the skeleton of the unicellular plankton organisms Acantharia^[3]^,^[4]. These biomineral model systems closely mimic fundamental interactions between mineral and organic matrix in living organisms, while eliminating the complexity and heterogeneity associated with biological systems. This investigation enabled a focused fundamental investigation of SrSO₄ crystallization across multiple length scales, as biologically grown minerals often contain a variety of organic molecules in small weight percentages as well as considerable amounts of foreign ions, such as magnesium, which complicate data interpretation^[1]^,^[2]. Even though all studied biomolecules were included into the growing crystals in high weight percentages, poly(<i>L</i>-glutamic acid) had the most profound impact on crystal morphology. Using Scanning Electron Microscopy and Atomic Force Microscopy, we observed mesocrystalline features on the crystal surface, which are consistent with biomolecule incorporation. Apart from studying the chemistry of the nanocomposites using bulk infrared spectroscopy, we discerned intracrystalline organics at the nanoscale using monochromated Electron Energy-loss Spectroscopy in the Scanning Transmission Electron Microscope^[5]^,^[6]. By screening the organic-biomineral model systems with synchrotron X-ray powder diffraction^[1]^,^[2], we quantified the degree of internal residual strain resulting from biomolecules with diverse functional group chemistry.<br/><br/><b>Acknowledgements</b><br/>Dr. Merk thanks the National Science Foundation (NSF 2137663, Division of Materials Research) for supporting this study.<br/><br/><b>References</b><br/>[1] B. Pokroy, J.P. Quintana, N.C. El’ad, A. Berner, E. Zolotoyabko, Anisotropic lattice distortions in biogenic aragonite, Nat. Mater. 3 (2004) 900–902.<br/>[2] M.A. Hood, H. Leemreize, A. Scheffel, D. Faivre, Lattice distortions in coccolith calcite crystals originate from occlusion of biomacromolecules, J. Struct. Biol. 196 (2016) 147–154.<br/>[3] V. Merk, J. Decelle, S. Chen, A. Lanzirotti, M. Newville, O. Antipova, D. Joester, Selective Ion Accumulation in Biomineralizing Marine Acantharia, Microsc. Microanal. 25 (2019) 1072–1073. https://doi.org/DOI: 10.1017/S1431927619006093.<br/>[4] D. Raja Somu, T. Cracchiolo, E. Longo, I. Greving, V. Merk, On stars and spikes: Resolving the skeletal morphology of planktonic Acantharia using synchrotron X-ray nanotomography and deep learning image segmentation, Acta Biomater. (2023). https://doi.org/https://doi.org/10.1016/j.actbio.2023.01.037.<br/>[5] J.A. Hachtel, J. Huang, I. Popovs, S. Jansone-Popova, J.K. Keum, J. Jakowski, T.C. Lovejoy, N. Dellby, O.L. Krivanek, J.C. Idrobo, Identification of site-specific isotopic labels by vibrational spectroscopy in the electron microscope, Science (80-. ). 363 (2019) 525 LP – 528. https://doi.org/10.1126/science.aav5845.<br/>[6] P. Rez, T. Aoki, K. March, D. Gur, O.L. Krivanek, N. Dellby, T.C. Lovejoy, S.G. Wolf, H. Cohen, Damage-free vibrational spectroscopy of biological materials in the electron microscope, Nat. Commun. 7 (2016) 10945. https://doi.org/10.1038/ncomms10945.