TY - JOUR

T1 - On Biomineralization: Enzymes Switch on Mesocrystal Assembly

AU - Rao, Ashit

AU - Roncal-Herrero, Teresa

AU - Schmid, Elina

AU - Drechsler, Markus

AU - Scheffner, Martin

AU - Gebauer, Denis

AU - Kröger, Roland

AU - Cölfen, Helmut

N1 - Funding Information: A.R. acknowledges a fellowship from Konstanz Research School Chemical Biology. M.D. thanks the Bavarian Polymer Institute and the collaborative research centre SFB840 of the German Research Foundation for financial support. R.K and T.R.-H. acknowledge funding by the European Research Council in the framework of the project SMILEY (FP7-NMP-2012-SMALL-6-310637) and the Engineering and Physical Sciences Research Council (EP/I001514/1). D.G. is a Research Fellow of the Zukunftskolleg, University of Konstanz. We also thank Dr. Joachim Hentschel from the Electron Microscopy Centre; Dr. Andreas Marquardt and Dr. Anna Sladewska-Marquardt from the Proteomics Core Facility, University of Konstanz; and Dr. Alexander Titz, Helmholtz Institute for Pharmaceutical Research Saarland.

PY - 2019/2/27

Y1 - 2019/2/27

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85061275599&partnerID=8YFLogxK

U2 - 10.1021/acscentsci.8b00853

DO - 10.1021/acscentsci.8b00853

M3 - Article

VL - 5

SP - 357

EP - 364

JO - ACS Central Science

JF - ACS Central Science

IS - 2

ER -