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ACS Cent Sci
2019 Feb 27;52:357-364. doi: 10.1021/acscentsci.8b00853.
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On Biomineralization: Enzymes Switch on Mesocrystal Assembly.
Rao A
,
Roncal-Herrero T
,
Schmid E
,
Drechsler M
,
Scheffner M
,
Gebauer D
,
Kröger R
,
Cölfen H
.
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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.
Figure 1. Representative cryo-TEM
micrographs corresponding to the (a–f)
prenucleation stages and (g–k) postnucleation stages for mineral
nucleation during CTLD-controlled nucleation at pH 9.0 with protein
contents of 0.1 mg/mL. Presence of organic laminae (g and h) and vesicular
structures (j and k) are indicated. (l) Representative TEM image and
corresponding ED pattern of a nucleated particle. Scale bars represent
(a and i) 100 nm, (b–e, k, and l) 200 nm, (f and j) 0.5 μm,
and (h) 10 nm.
Figure 2. Representative TEM micrographs of (a and
b) CTLD-mediated multilaminar
mesocrystals formed during mineral nucleation at pH 9. Mesocrystal
deconstruction by (c) sonication, (d) ultramicrotomy, or (e) proteinase
K treatment reveals crystallographic co-orientation between particles
of adjacent laminae and a space-filling nanoparticle arrangement.
(f) Color-mapped crystallographic spread of a wet mount mesocrystal
by quantitative polarization microscopy. Structural analyses of the
constituents from the adult spine of Strongylocentrotus
purpuratus by means of (g) dark field polarization
light microscopy, (h) quantitative polarization microscopy, and (i)
TEM. Insets represent (a, c–e, and i) ED patterns, (f–h)
bright-field images, and (i) TEM image at lower magnification. Scale
bars represent (a) 1 μm, (b–e and i) 200 nm, (f) 50 μm,
(g) 100 μm, and (h) 20 μm.
Figure 3. (a) Western blots representing the proteolytic susceptibility
of
SM50 toward type VI collagenase and thermolysin developed using anti-SM50
polyclonal antibodies and protease contents of 10 (+) or 100 (++)
μg/mL. (b) Time required for mineral nucleation in reference
experiments (R) and in mineralization solutions containing only 1
mg/mL SM50 (−) and also supplemented with type VI collagenase.
(c) Black bars represent the sequence coverage of SM50 proteolytic
products produced by collagenase activity (box a). (d) Representative
cryo-TEM images of mineral products formed in the presence of SM50
alone and in combination with a type VI collagenase. (e) Snapshots
of mineralization reactions in the presence of the CTLD (Supplementary Video 1) or a SM50/type VI collagenase
mixture acquired by using LC-STEM. Note the high aggregation propensity
of vesicles and their hollow cores in the presence of collagenase.
Scale bars represent (d) 500 (left) and 200 (right) nm and (e) 100
nm.
Figure 4. (a) Scheme
illustrating different stages of the formative process
of crystalline minerals involving (1) a population of stable, structurally
dynamic ion-clusters, (2) at a critical ion activity, the liquid–liquid
demixing of mineral nanodroplets and the subsequent nucleation of
(3) amorphous calcium carbonate and (4) crystalline polymorphs. (b)
Schematic representation of the multifunctionality of SM50 (1) initially
forming vesicles that confine and stabilize a liquid-like amorphous
mineral form. (2) At the site for mineral growth, MMP activity specifically
cleaves the disordered domain of SM50 (pink), which is crucial for
vesicle stability. This initiates the phase transformation of the
amorphous phase to calcite under regulation of the residual CTLD (blue).
Conditions of pH and supersaturation drive the assembly of CTLD to
scaffolding structures. (3) The destabilized fluidic (and possibly
transient particulate45,46) precursors infiltrate and mineralize
the organic laminae, generating calcite mesocrystals. (c) Structural
similarities between vesicles trafficking mineral precursors and laminar
modules from the sea urchin spine (left) to SM50-based vesicular structures
and CTL-mediated calcite mesocrystals (right). Scale bars represent
1 μm, 200 nm, 500 nm, and 1 μm, left to right. (*The left-hand
image in panel c is reproduced with permission from ref (32). Copyright 2014 National
Academy of Sciences.)
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