On Biomineralization: Enzymes Switch on Mesocrystal Assembly

Abstract

Cellular machineries guide the bottom-up pathways toward crystal superstructures based on the transport of inorganic precursors and their precise integration with organic frameworks. The biosynthesis of mesocrystalline spines entails concerted interactions between biomolecules and inorganic precursors; however, the bioinorganic interactions and interfaces that regulate material form and growth as well as the selective emergence of structural complexity in the form of nanostructured crystals are not clear. By investigating mineral nucleation under the regulation of recombinant proteins, we show that SpSM50, a matrix protein of the sea urchin spine, stabilizes mineral precursors via vesicle-confinement, a function conferred by a low-complexity, disordered region. Site-specific proteolysis of this domain by a collagenase initiates phase transformation of the confined mineral phase. The residual C-type lectin domain molds the fluidic mineral precursor into hierarchical mesocrystals identical to structural crystal modules constituting the biogenic mineral. Thus, the regulatory functions of proteolytic enzymes can guide biomacromolecular domain constitutions and interfaces, in turn determining inorganic phase transformations toward hybrid materials as well as integrating organic and inorganic components across hierarchical length scales. Bearing striking resemblance to biogenic mineralization, these hybrid materials recruit bioinorganic interactions which elegantly intertwine nucleation and crystallization phenomena with biomolecular structural dynamics, hence elucidating a long-sought key of how nature can orchestrate complex biomineralization processes.

Microbe‐Mediated Extracellular and Intracellular Mineralization: Environmental, Industrial, and Biotechnological Applications

“…[ 157 ] This aggregation process is meditated by proteins such as those derived from the sea urchin spine, an excellent example of how nature mediates the formation of complex biominerals. [ 165 ] Regulation of crystallographic orientation results in the generation of biominerals that exhibit superstructural organization at multiple length scales. Coccoliths produced by coccolithophores, for example, is intermediate in structural complexity compared with single crystals produced by prokaryotes and the hierarchical composites in multicellular organisms.…”

The multiple roles of carbonic anhydrase in calcium carbonate mineralization

“…54 We therefore propose that after the initial classical nucleation and growth of calcite after ACC dissolution, non-classical growth via attachment of ACC nanoparticles occurred resulting in crystalline structures displaying the landmark features of biotic and biomimetic mesocrystals, such as the observed nanogranular structure and the single-crystal SAED pattern with a relatively small angular spreading. [12][13][14] Such structures can retain the original ACC nanogranular structure imprinted in the final crystalline polymorph, 6,11 when the amorphousto-crystalline transformation takes place via a pseudomorphic interface-coupled dissolution-precipitation mechanism, as we have demonstrated for the non-classical growth of calcite following ACC nanoparticle attachment in the presence of (poly)acrylic acid. 37 In the present case, CA molecules, either present in solution or released after dissolution of ACC attached to calcite seeds, could in turn affect the growth (kinetics and morphology) of calcite mesostructures via stepspecific interactions in a similar way to that in our in situ AFM experiments.…”

Mineral self-organization on a lifeless planet

“…When these biomineral structures are broken they display a glassy fracture that does not show flat but curved surfaces [43]. These shells are made of millions of nanocrystals that self-assemble with excellent co-orientation forming a mesocrystalline structure that sometimes even retains the point symmetry of the calcite or aragonite structure [44][45][46]. Visual records of the in situ growth of biominerals show that the crystals do not grow by classical growth mechanisms as abiotic calcite and aragonite do, but by accumulation of disordered nanodots of an amorphous precursor or a high-density cation-rich solution that afterwards recrystallized to a stable crystal polymorph [42,47,48].…”