Elucidating the biomineralization pathway of calcite in coccolithophores
Biomaterials
Physical Chemistry of Solids and Surfaces, Material Characterisation
Final Report Abstract
The controlled formation of minerals is a widespread trait among organisms and is referred to as biomineralization. Biomineralization takes place at ambient and physiological conditions and yields mineral structures with complex morphology that are unknown from geological-formed minerals and beyond the synthetic capabilities of current materials chemistry approaches. Coccoliths, which are 3D arrays of complex-shaped calcite (CaCO3) crystals, are one of the most spectacular examples of biomineralization. They are formed by single-celled algae, called coccolithophores, within an intracellular compartment. The mature coccolith is secreted to the cell surface and assembled into a shell around the cell. The crystallization pathway of coccoliths, which is referring to the reactions between uptake of the mineralconstituting ions and calcite crystallization within the coccolith-producing compartment, remain largely unknown. Knowledge of the crystallization pathway and the interactions between biomacromolecules and the growing crystals are important for understanding crystal morphogenesis in coccolith formation. This research project aimed at fresh insight into the crystallization pathway of coccoliths and the interaction between biomacromolecules and growing crystals. The coccolithophores Emiliania huxleyi, Pleurochrysis carterae, Coccolithus pelagicus subspecies braarudii have been the subject of study in this project. Using soft cryo X- ray tomography and spectromicroscopy, cryo-focused ion beam scanning electron microscopy, energy-dispersive x-ray spectroscopy, electron energy loss spectroscopy, and cryo-SEM freeze-fracturing, we identified a yet undescribed compartment in E. huxleyi and P. carterae, filled with high concentrations of a disordered form of calcium. Within this compartment the calcium is co-localized with phosphorous, most probably stored in the form of polyphosphates. Pulse-labeling of this Ca-P pool in E. huxleyi with strontium and pulse-chase analysis using X-ray adsorption near edge structure spectroscopy suggested the Ca-pool to be slowly transferred into the coccolith-producing compartment. Decades ago, it was discovered that organic macromolecules are tightly associated with the calcite crystals of coccoliths and that these macromolecules modulate calcite crystallization. Whether the organic material becomes occluded within the crystals, which may have an impact on the fracture resistance of the crystals, or only surface-associated remains an open question. Using synchrotron-based X-ray diffraction we found that a small portion of the organic material that is tightly associated with the coccoliths is occluded within the crystals of P. carterae and E. huxleyi. Our data suggest further that most of the coccolith-associated organic material sticks on the surface of the crystals.
Publications
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(2016) A vacuole-like compartment concentrates a disordered calcium phase in a key coccolithophorid alga. Nat. Commun. 7: 11228
Sviben S., Gal A., Hood M.A., Bertinetti L., Politi Y., Bennet M., Krishnamoorthy P., Schertel A., Wirth R., Sorrentino A., Pereiro E., Faivre D., Scheffel A.
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(2016) Lattice distortions in coccolith calcite crystals originate from occlusion of biomacromolecules. J. Struct. Biol. 196: 147-154
Hood M.A., Leemreize H., Scheffel A., Faivre D.
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(2017) Trace-element incorporation into intracellular pools uncovers calcium-pathways in a coccolithophore. Adv. Sci. 4: 1700088
Gal A., Sviben S., Wirth R., Schreiber A., Lassalle-Kaiser B., Faivre D., Scheffel A.
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(2018) How is intracellular calcite formation in coccolithophorid algae supplied with calcium? Newsletter Synchrotron SOLEIL
Scheffel A.
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(2018) Native-state imaging of calcifying and non-calcifying microalgae reveals similarities in their calcium storage organelles. Proc. Natl. Acad. Sci. U.S.A. 115(43): 11000-11005
Gal A., Sorrentino A., Kahil K., Pereiro E., Faivre D., Scheffel A.