Directing polymorph specific calcium carbonate formation with de novo protein templates

Davila-Hernandez, Fatima A.; Jin, Biao; Pyles, Harley; Zhang, Shuai; Wang, Zheming; Huddy, Timothy F.; Bera, Asim K.; Kang, Alex; Chen, Chun-Long; De Yoreo, James J.; Baker, David

doi:10.1038/s41467-023-43608-1

Directing polymorph specific calcium carbonate formation with de novo protein templates

Journal Article · Wed Dec 13 23:00:00 EST 2023 · Nature Communications

DOI:https://doi.org/10.1038/s41467-023-43608-1· OSTI ID:2274875

Davila-Hernandez, Fatima A. ^[1]; Jin, Biao ^[2]; Pyles, Harley ^[3]; ^[2]; Wang, Zheming ^[4]; Huddy, Timothy F. ^[3]; ^[3]; Kang, Alex ^[3]; ^[2]; ^[2]; ^[3]

University of Washington, Seattle, WA (United States); University of Washington
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); University of Washington, Seattle, WA (United States)
University of Washington, Seattle, WA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Biomolecules modulate inorganic crystallization to generate hierarchically structured biominerals, but the atomic structure of the organic-inorganic interfaces that regulate mineralization remain largely unknown. We hypothesized that heterogeneous nucleation of calcium carbonate could be achieved by a structured flat molecular template that pre-organizes calcium ions on its surface. To test this hypothesis, we design helical repeat proteins (DHRs) displaying regularly spaced carboxylate arrays on their surfaces and find that both protein monomers and protein-C^a2+ supramolecular assemblies directly nucleate nano-calcite with non-natural {110} or {202} faces while vaterite, which forms first in the absence of the proteins, is bypassed. These protein-stabilized nanocrystals then assemble by oriented attachment into calcite mesocrystals. We find further that nanocrystal size and polymorph can be tuned by varying the length and surface chemistry of the designed protein templates. Thus, bio-mineralization can be programmed using de novo protein design, providing a route to next-generation hybrid materials.

View Accepted Manuscript (DOE)

Research Organization:: University of Washington, Seattle, WA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0019288; AC05-76RL01830; AC02-05CH11231; AC02-06CH11357

OSTI ID:: 2274875

Alternate ID(s):: OSTI ID: 2341501
OSTI ID: 2341502

Report Number(s):: PNNL-SA--186141

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Biochemistry and Molecular Genetics of Silica Biomineralization in Diatoms Kroger, Nils; Poulsen, Nicole Handbook of Biomineralization https://doi.org/10.1002/9783527619443.ch3	book	May 2007
The Transient Phase of Amorphous Calcium Carbonate in Sea Urchin Larval Spicules: The Involvement of Proteins and Magnesium Ions in Its Formation and Stabilization Raz, S.; Hamilton, P. C.; Wilt, F. H. Advanced Functional Materials, Vol. 13, Issue 6 https://doi.org/10.1002/adfm.200304285	journal	June 2003
Citrate Effects on Amorphous Calcium Carbonate (ACC) Structure, Stability, and Crystallization Tobler, Dominique J.; Rodriguez-Blanco, Juan Diego; Dideriksen, Knud Advanced Functional Materials, Vol. 25, Issue 20 https://doi.org/10.1002/adfm.201500400	journal	April 2015
Stabilization of Mineral Precursors by Intrinsically Disordered Proteins Rao, Ashit; Drechsler, Markus; Schiller, Stefan Advanced Functional Materials, Vol. 28, Issue 37 https://doi.org/10.1002/adfm.201802063	journal	July 2018
Control and Design Principles in Biological Mineralization Addadi, Lia; Weiner, Stephen Angewandte Chemie International Edition in English, Vol. 31, Issue 2 https://doi.org/10.1002/anie.199201531	journal	February 1992
Iron Biomineral Growth from the Initial Nucleation Seed in L‐Ferritin Ciambellotti, Silvia; Pozzi, Cecilia; Mangani, Stefano Chemistry – A European Journal, Vol. 26, Issue 26 https://doi.org/10.1002/chem.202000064	journal	March 2020
High-Throughput SAXS for the Characterization of Biomolecules in Solution: A Practical Approach Dyer, Kevin N.; Hammel, Michal; Rambo, Robert P. Structural Genomics https://doi.org/10.1007/978-1-62703-691-7_18	book	October 2013
Comparison of nacre with other ceramic composites Jackson, A. P.; Vincent, J. F. V.; Turner, R. M. Journal of Materials Science, Vol. 25, Issue 7 https://doi.org/10.1007/BF00587670	journal	July 1990
Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Biophysical Journal, Vol. 105, Issue 4 https://doi.org/10.1016/j.bpj.2013.07.020	journal	August 2013
Intrinsically disordered proteins and biomineralization Boskey, Adele L.; Villarreal-Ramirez, Eduardo Matrix Biology, Vol. 52-54 https://doi.org/10.1016/j.matbio.2016.01.007	journal	May 2016
The Effect of Aspartic Acid and Glycine on Amorphous Calcium Carbonate (ACC) Structure, Stability and Crystallization Tobler, D. J.; Blanco, J. D. Rodriguez; Dideriksen, K. Procedia Earth and Planetary Science, Vol. 10 https://doi.org/10.1016/j.proeps.2014.08.047	journal	January 2014
Organized Arrangement of Calcium Carbonate Crystals, Directed by a Rationally Designed Protein Ping, Hang; Wan, Yamin; Xie, Hao Crystal Growth & Design, Vol. 18, Issue 6 https://doi.org/10.1021/acs.cgd.8b00365	journal	April 2018
Self-Assembly of a Barnacle Cement Protein (MrCP20) into Adhesive Nanofibrils with Concomitant Regulation of CaCO₃Polymorphism Mohanram, Harini; Georges, Tristan; Pervushin, Konstantin Chemistry of Materials, Vol. 33, Issue 24 https://doi.org/10.1021/acs.chemmater.1c03477	journal	December 2021
Water Orientation at the Calcite-Water Interface Söngen, Hagen; Schlegel, Simon J.; Morais Jaques, Ygor The Journal of Physical Chemistry Letters, Vol. 12, Issue 31 https://doi.org/10.1021/acs.jpclett.1c01729	journal	August 2021
On Biomineralization: Enzymes Switch on Mesocrystal Assembly Rao, Ashit; Roncal-Herrero, Teresa; Schmid, Elina ACS Central Science, Vol. 5, Issue 2 https://doi.org/10.1021/acscentsci.8b00853	journal	February 2019
Intrinsically Disordered Mollusk Shell Prismatic Protein That Modulates Calcium Carbonate Crystal Growth Ndao, Moise; Keene, Ellen; Amos, Fairland F. Biomacromolecules, Vol. 11, Issue 10 https://doi.org/10.1021/bm100738r	journal	October 2010
Self-Assembly and Biphasic Iron-Binding Characteristics of Mms6, A Bacterial Protein That Promotes the Formation of Superparamagnetic Magnetite Nanoparticles of Uniform Size and Shape Wang, Lijun; Prozorov, Tanya; Palo, Pierre E. Biomacromolecules, Vol. 13, Issue 1 https://doi.org/10.1021/bm201278u	journal	December 2011
Interactions of various skeletal intracrystalline components with calcite crystals Albeck, S.; Aizenberg, J.; Addadi, L. Journal of the American Chemical Society, Vol. 115, Issue 25 https://doi.org/10.1021/ja00078a005	journal	December 1993
De Novo Design of Peptide−Calcite Biomineralization Systems Masica, David L.; Schrier, Sarah B.; Specht, Elizabeth A. Journal of the American Chemical Society, Vol. 132, Issue 35 https://doi.org/10.1021/ja1001086	journal	September 2010
Phosphate–Water Interplay Tunes Amorphous Calcium Carbonate Metastability: Spontaneous Phase Separation and Crystallization vs Stabilization Viewed by Solid State NMR Kababya, Shifi; Gal, Assaf; Kahil, Keren Journal of the American Chemical Society, Vol. 137, Issue 2 https://doi.org/10.1021/ja511869g	journal	January 2015
Control of Calcite Crystal Morphology by a Peptide Designed To Bind to a Specific Surface DeOliveira, Daniel B.; Laursen, Richard A. Journal of the American Chemical Society, Vol. 119, Issue 44 https://doi.org/10.1021/ja972270w	journal	November 1997
Oriented Growth of Calcite Controlled by Self-Assembled Monolayers of Functionalized Alkanethiols Supported on Gold and Silver Aizenberg, Joanna; Black, Andrew J.; Whitesides, George M. Journal of the American Chemical Society, Vol. 121, Issue 18 https://doi.org/10.1021/ja984254k	journal	May 1999
Ubiquitin Designer Proteins as a New Additive Generation toward Controlling Crystallization Ruiz-Agudo, Cristina; Lutz, Joachim; Keckeis, Philipp Journal of the American Chemical Society, Vol. 141, Issue 31 https://doi.org/10.1021/jacs.9b06473	journal	July 2019
Surface Selectivity of Calcite on Self-Assembled Monolayers Freeman, Colin L.; Hu, Q.; Nielsen, M. H. The Journal of Physical Chemistry C, Vol. 117, Issue 10 https://doi.org/10.1021/jp312108j	journal	March 2013
Simulation of Organic Monolayers as Templates for the Nucleation of Calcite Crystals Duffy, Dorothy M.; Harding, John H. Langmuir, Vol. 20, Issue 18 https://doi.org/10.1021/la049552b	journal	August 2004
Molecular recognition in biomineralization Mann, Stephen Nature, Vol. 332, Issue 6160 https://doi.org/10.1038/332119a0	journal	March 1988
Control of crystal phase switching and orientation by soluble mollusc-shell proteins Belcher, A. M.; Wu, X. H.; Christensen, R. J. Nature, Vol. 381, Issue 6577 https://doi.org/10.1038/381056a0	journal	May 1996
Nanoscale chemical tomography of buried organic–inorganic interfaces in the chiton tooth Gordon, Lyle M.; Joester, Derk Nature, Vol. 469, Issue 7329 https://doi.org/10.1038/nature09686	journal	January 2011
Exploring the repeat protein universe through computational protein design Brunette, Tj; Parmeggiani, Fabio; Huang, Po-Ssu Nature, Vol. 528, Issue 7583 https://doi.org/10.1038/nature16162	journal	December 2015
The coming of age of de novo protein design Huang, Po-Ssu; Boyken, Scott E.; Baker, David Nature, Vol. 537, Issue 7620 https://doi.org/10.1038/nature19946	journal	September 2016
Chiral acidic amino acids induce chiral hierarchical structure in calcium carbonate Jiang, Wenge; Pacella, Michael S.; Athanasiadou, Dimitra Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15066	journal	April 2017
Nucleation of apatite crystals in vitro by self-assembled dentin matrix protein 1 He, Gen; Dahl, Tom; Veis, Arthur Nature Materials, Vol. 2, Issue 8 https://doi.org/10.1038/nmat945	journal	July 2003
Role of carbonate burial in Blue Carbon budgets Saderne, V.; Geraldi, N. R.; Macreadie, P. I. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08842-6	journal	March 2019
Design of multi-scale protein complexes by hierarchical building block fusion Hsia, Yang; Mout, Rubul; Sheffler, William Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-22276-z	journal	April 2021
De novo protein design by citizen scientists Koepnick, Brian; Flatten, Jeff; Husain, Tamir Nature, Vol. 570, Issue 7761 https://doi.org/10.1038/s41586-019-1274-4	journal	June 2019
Controlling protein assembly on inorganic crystals through designed protein interfaces Pyles, Harley; Zhang, Shuai; De Yoreo, James J. Nature, Vol. 571, Issue 7764 https://doi.org/10.1038/s41586-019-1361-6	journal	July 2019
Self-similar mesocrystals form via interface-driven nucleation and assembly Zhu, Guomin; Sushko, Maria L.; Loring, John S. Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/s41586-021-03300-0	journal	February 2021
Macromolecular modeling and design in Rosetta: recent methods and frameworks Leman, Julia Koehler; Weitzner, Brian D.; Lewis, Steven M. Nature Methods, Vol. 17, Issue 7 https://doi.org/10.1038/s41592-020-0848-2	journal	June 2020
Bio-inspired crystal morphogenesis by hydrophilic polymers Yu, Shu-Hong; Cölfen, Helmut J. Mater. Chem., Vol. 14, Issue 14 https://doi.org/10.1039/B401420K	journal	January 2004
From ice-binding proteins to bio-inspired antifreeze materials Voets, I. K. Soft Matter, Vol. 13, Issue 28 https://doi.org/10.1039/C6SM02867E	journal	January 2017
Near surface nucleation and particle mediated growth of colloidal Au nanocrystals Cheng, Yingwen; Tao, Jinhui; Zhu, Guomin Nanoscale, Vol. 10, Issue 25 https://doi.org/10.1039/C8NR03408G	journal	January 2018
Calcium carbonate: controlled synthesis, surface functionalization, and nanostructured materials Niu, Yu-Qin; Liu, Jia-Hui; Aymonier, Cyril Chemical Society Reviews, Vol. 51, Issue 18 https://doi.org/10.1039/D1CS00519G	journal	January 2022
The thermodynamics of calcite nucleation at organic interfaces: Classical vs. non-classical pathways Hu, Q.; Nielsen, M. H.; Freeman, C. L. Faraday Discussions, Vol. 159 https://doi.org/10.1039/c2fd20124k	journal	January 2012
Investigation of the role of ansocalcin in the biomineralization in goose eggshell matrix Lakshminarayanan, Rajamani; Kini, R. Manjunatha; Valiyaveettil, Suresh Proceedings of the National Academy of Sciences, Vol. 99, Issue 8 https://doi.org/10.1073/pnas.072658899	journal	April 2002
Hierarchical self-assembly of amelogenin and the regulation of biomineralization at the nanoscale Fang, P. -A.; Conway, J. F.; Margolis, H. C. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1106228108	journal	August 2011
Phase transitions in biogenic amorphous calcium carbonate Gong, Y. U. T.; Killian, C. E.; Olson, I. C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 16 https://doi.org/10.1073/pnas.1118085109	journal	April 2012
Polysaccharide chemistry regulates kinetics of calcite nucleation through competition of interfacial energies Giuffre, Anthony J.; Hamm, Laura M.; Han, Nizhou Proceedings of the National Academy of Sciences, Vol. 110, Issue 23 https://doi.org/10.1073/pnas.1222162110	journal	May 2013
Reconciling disparate views of template-directed nucleation through measurement of calcite nucleation kinetics and binding energies Hamm, L. M.; Giuffre, A. J.; Han, N. Proceedings of the National Academy of Sciences, Vol. 111, Issue 4 https://doi.org/10.1073/pnas.1312369111	journal	January 2014
De novo design of protein homodimers containing tunable symmetric protein pockets Hicks, Derrick R.; Kennedy, Madison A.; Thompson, Kirsten A. Proceedings of the National Academy of Sciences, Vol. 119, Issue 30 https://doi.org/10.1073/pnas.2113400119	journal	July 2022
Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Addadi, L.; Weiner, S. Proceedings of the National Academy of Sciences, Vol. 82, Issue 12 https://doi.org/10.1073/pnas.82.12.4110	journal	June 1985
Blueprinting expandable nanomaterials with standardized protein building blocks Huddy, Timothy F.; Hsia, Yang; Kibler, Ryan D. Nature https://doi.org/10.1101/2023.06.09.544258	posted_content	June 2023
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Control of nacre biomineralization by Pif80 in pearl oyster Bahn, So Yeong; Jo, Byung Hoon; Choi, Yoo Seong Science Advances, Vol. 3, Issue 8 https://doi.org/10.1126/sciadv.1700765	journal	August 2017
An Acidic Matrix Protein, Pif, Is a Key Macromolecule for Nacre Formation Suzuki, M.; Saruwatari, K.; Kogure, T. Science, Vol. 325, Issue 5946 https://doi.org/10.1126/science.1173793	journal	August 2009
In situ TEM imaging of CaCO3 nucleation reveals coexistence of direct and indirect pathways Nielsen, M. H.; Aloni, S.; De Yoreo, J. J. Science, Vol. 345, Issue 6201 https://doi.org/10.1126/science.1254051	journal	September 2014
Crystallization by particle attachment in synthetic, biogenic, and geologic environments De Yoreo, J. J.; Gilbert, P. U. P. A.; Sommerdijk, N. A. J. M. Science, Vol. 349, Issue 6247 https://doi.org/10.1126/science.aaa6760	journal	July 2015
Biological control of aragonite formation in stony corals Von Euw, Stanislas; Zhang, Qihong; Manichev, Viacheslav Science, Vol. 356, Issue 6341 https://doi.org/10.1126/science.aam6371	journal	June 2017
Osteopontin Sodek, J.; Ganss, B.; McKee, M. D. Critical Reviews in Oral Biology & Medicine, Vol. 11, Issue 3 https://doi.org/10.1177/10454411000110030101	journal	July 2000
Biomineralization Sourcebook DiMasi, Elaine; Gower, Laurie B. https://doi.org/10.1201/b16621	book	March 2014
Formation, Chemical Evolution, and Solidification of the Calcium Carbonate Dense Liquid Phase De Yoreo, James; Jin, Biao; Chen, Ying https://doi.org/10.21203/rs.3.rs-1743346/v1	preprint	July 2022