Shape-preserving amorphous-to-crystalline transformation of CaCO 3 revealed by in situ TEM

Liu, Zhaoming; Zhang, Zhisen; Wang, Zheming; Jin, Biao; Li, Dongsheng; Tao, Jinhui; Tang, Ruikang; De Yoreo, James J.

doi:10.1073/pnas.1914813117

Shape-preserving amorphous-to-crystalline transformation of CaCO ₃ revealed by in situ TEM

Journal Article · Mon Feb 03 00:00:00 EST 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1914813117· OSTI ID:1597119

Liu, Zhaoming ^[1]; Zhang, Zhisen ^[2]; Wang, Zheming ^[3]; Jin, Biao ^[1]; ^[3]; Tao, Jinhui ^[3]; Tang, Ruikang ^[4]; De Yoreo, James J. ^[5]

Department of Chemistry, Zhejiang University, Hangzhou, Zhejiang 310027, China,, Physical Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99352,
Department of Physics, Xiamen University, Xiamen, Fujian 361005, China,, Research Institute for Biomimetics and Soft Matter, Xiamen University, Xiamen, Fujian 361005, China,, Fujian Provincial Key Laboratory for Soft Functional Materials Research, Xiamen University, Xiamen, Fujian 361005, China,
Physical Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99352,
Department of Chemistry, Zhejiang University, Hangzhou, Zhejiang 310027, China,
Physical Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99352,, Department of Materials Science and Engineering, University of Washington, Seattle, WA 98195

Organisms use inorganic ions and macromolecules to regulate crystallization from amorphous precursors, endowing natural biominerals with complex morphologies and enhanced properties. The mechanisms by which modifiers enable these shape-preserving transformations are poorly understood. We used in situ liquid-phase transmission electron microscopy to follow the evolution from amorphous calcium carbonate to calcite in the presence of additives. A combination of contrast analysis and infrared spectroscopy shows that Mg ions, which are widely present in seawater and biological fluids, alter the transformation pathway in a concentration-dependent manner. The ions bring excess (structural) water into the amorphous bulk so that a direct transformation is triggered by dehydration in the absence of morphological changes. Molecular dynamics simulations suggest Mg-incorporated water induces structural fluctuations, allowing transformation without the need to nucleate a separate crystal. Thus, the obtained calcite retains the original morphology of the amorphous state, biomimetically achieving the morphological control of crystals seen in biominerals.

View Journal Article

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1597119

Alternate ID(s):: OSTI ID: 1657072

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 7 Vol. 117; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (58)

Formation of High-Magnesian Calcites via an Amorphous Precursor Phase: Possible Biological Implications Raz, S.; Weiner, S.; Addadi, L. Advanced Materials, Vol. 12, Issue 1, p. 38-42 https://doi.org/10.1002/(SICI)1521-4095(200001)12:1<38::AID-ADMA38>3.0.CO;2-I	journal	January 2000
Mesocrystals and Nonclassical Crystallization Clfen, Helmut; Antonietti, Markus John Wiley & Sons, Ltd https://doi.org/10.1002/9780470994603	book	January 2008
Particle Accretion Mechanism Underlies Biological Crystal Growth from an Amorphous Precursor Phase Gal, Assaf; Kahil, Keren; Vidavsky, Netta Advanced Functional Materials, Vol. 24, Issue 34 https://doi.org/10.1002/adfm.201400676	journal	July 2014
Taking Advantage of Disorder: Amorphous Calcium Carbonate and Its Roles in Biomineralization Addadi, L.; Raz, S.; Weiner, S. Advanced Materials, Vol. 15, Issue 12 https://doi.org/10.1002/adma.200300381	journal	June 2003
Revealing the Cluster‐Cloud and Its Role in Nanocrystallization Jin, Biao; Wang, Yanming; Liu, Zhaoming Advanced Materials, Vol. 31, Issue 16 https://doi.org/10.1002/adma.201808225	journal	February 2019
Calcium Carbonate Polyamorphism and Its Role in Biomineralization: How Many Amorphous Calcium Carbonates Are There? Cartwright, Julyan H. E.; Checa, Antonio G.; Gale, Julian D. Angewandte Chemie International Edition, Vol. 51, Issue 48 https://doi.org/10.1002/anie.201203125	journal	November 2012
Calcite Crystal Growth by a Solid-State Transformation of Stabilized Amorphous Calcium Carbonate Nanospheres in a Hydrogel Gal, Assaf; Habraken, Wouter; Gur, Dvir Angewandte Chemie International Edition, Vol. 52, Issue 18 https://doi.org/10.1002/anie.201210329	journal	April 2013
Pressure-Induced Polyamorphism and Formation of ‘Aragonitic’ Amorphous Calcium Carbonate Fernandez-Martinez, Alejandro; Kalkan, Bora; Clark, Simon M. Angewandte Chemie International Edition, Vol. 52, Issue 32 https://doi.org/10.1002/anie.201302974	journal	July 2013
Studies of the growth and dissolution kinetics of the CaCO₃ polymorphs calcite and aragonite II. The influence of divalent cation additives on the growth and dissolution rates Gutjahr, Astrid; Dabringhaus, Heinz; Lacmann, Rolf Journal of Crystal Growth, Vol. 158, Issue 3, p. 310-315 https://doi.org/10.1016/0022-0248(95)00447-5	journal	January 1996
Morphological influence of magnesium and organic additives on the precipitation of calcite Meldrum, Fiona C.; Hyde, Stephen T. Journal of Crystal Growth, Vol. 231, Issue 4 https://doi.org/10.1016/S0022-0248(01)01519-6	journal	October 2001
The role of magnesium in stabilising amorphous calcium carbonate and controlling calcite morphologies Loste, Eva; Wilson, Rory M.; Seshadri, Ram Journal of Crystal Growth, Vol. 254, Issue 1-2, p. 206-218 https://doi.org/10.1016/S0022-0248(03)01153-9	journal	June 2003
FTIR techniques in clay mineral studies Madejová, J. Vibrational Spectroscopy, Vol. 31, Issue 1 https://doi.org/10.1016/S0924-2031(02)00065-6	journal	January 2003
Chemical controls on the magnesium content of amorphous calcium carbonate Blue, C. R.; Dove, P. M. Geochimica et Cosmochimica Acta, Vol. 148 https://doi.org/10.1016/j.gca.2014.08.003	journal	January 2015
Chemical and physical controls on the transformation of amorphous calcium carbonate into crystalline CaCO3 polymorphs Blue, C. R.; Giuffre, A.; Mergelsberg, S. Geochimica et Cosmochimica Acta, Vol. 196 https://doi.org/10.1016/j.gca.2016.09.004	journal	January 2017
Biomimetic synthesis of calcite films by a polymer-induced liquid-precursor (PILP) process Cheng, Xingguo; Varona, Philip L.; Olszta, Matthew J. Journal of Crystal Growth, Vol. 307, Issue 2 https://doi.org/10.1016/j.jcrysgro.2007.07.006	journal	September 2007
Hydrogen Bonding in Amorphous Calcium Carbonate and Molecular Reorientation Induced by Dehydration Jensen, Anders C. S.; Imberti, Silvia; Parker, Stewart F. The Journal of Physical Chemistry C, Vol. 122, Issue 6 https://doi.org/10.1021/acs.jpcc.7b10459	journal	February 2018
Role of Impurities in the Kinetic Persistence of Amorphous Calcium Carbonate: A Nanoscopic Dynamics View Koishi, Ayumi; Fernandez-Martinez, Alejandro; Ruta, Beatrice The Journal of Physical Chemistry C, Vol. 122, Issue 29 https://doi.org/10.1021/acs.jpcc.8b05189	journal	July 2018
Role of Magnesium Ion in the Stabilization of Biogenic Amorphous Calcium Carbonate: A Structure−Function Investigation Politi, Yael; Batchelor, David R.; Zaslansky, Paul Chemistry of Materials, Vol. 22, Issue 1 https://doi.org/10.1021/cm902674h	journal	January 2010
Calcium Carbonate Formation and Dissolution Morse, John W.; Arvidson, Rolf S.; Lüttge, Andreas Chemical Reviews, Vol. 107, Issue 2 https://doi.org/10.1021/cr050358j	journal	February 2007
Biomimetic Model Systems for Investigating the Amorphous Precursor Pathway and Its Role in Biomineralization Gower, Laurie B. Chemical Reviews, Vol. 108, Issue 11 https://doi.org/10.1021/cr800443h	journal	November 2008
The Development of Morphology and Structure in Hexagonal Vaterite Pouget, Emilie M.; Bomans, Paul H. H.; Dey, Archan Journal of the American Chemical Society, Vol. 132, Issue 33 https://doi.org/10.1021/ja102439r	journal	August 2010
Water Is the Key to Nonclassical Nucleation of Amorphous Calcium Carbonate Raiteri, Paolo; Gale, Julian D. Journal of the American Chemical Society, Vol. 132, Issue 49 https://doi.org/10.1021/ja108508k	journal	December 2010
Mechanism of Calcite Co-Orientation in the Sea Urchin Tooth Killian, Christopher E.; Metzler, Rebecca A.; Gong, Y. U. T. Journal of the American Chemical Society, Vol. 131, Issue 51 https://doi.org/10.1021/ja907063z	journal	December 2009
Understanding the Control of Mineralization by Polyelectrolyte Additives: Simulation of Preferential Binding to Calcite Surfaces Shen, Jia-Wei; Li, Chunli; van der Vegt, Nico F. A. The Journal of Physical Chemistry C, Vol. 117, Issue 13 https://doi.org/10.1021/jp402341w	journal	March 2013
Effects of Magnesium Ions and Water Molecules on the Structure of Amorphous Calcium Carbonate: A Molecular Dynamics Study Tomono, Hidekazu; Nada, Hiroki; Zhu, Fangjie The Journal of Physical Chemistry B, Vol. 117, Issue 47 https://doi.org/10.1021/jp407721x	journal	November 2013
Electron–Water Interactions and Implications for Liquid Cell Electron Microscopy Schneider, Nicholas M.; Norton, Michael M.; Mendel, Brian J. The Journal of Physical Chemistry C, Vol. 118, Issue 38 https://doi.org/10.1021/jp507400n	journal	September 2014
Derivation of an Accurate Force-Field for Simulating the Growth of Calcium Carbonate from Aqueous Solution: A New Model for the Calcite−Water Interface Raiteri, Paolo; Gale, Julian D.; Quigley, David The Journal of Physical Chemistry C, Vol. 114, Issue 13 https://doi.org/10.1021/jp910977a	journal	February 2010
Inhibitory Effect of Magnesium and Zinc on Crystallization Kinetics of Hydroxyapatite (0001) Face Kanzaki, Noriko; Onuma, Kazuo; Treboux, Gabin The Journal of Physical Chemistry B, Vol. 104, Issue 17 https://doi.org/10.1021/jp9939726	journal	May 2000
Formation and Growth of Amorphous Colloidal CaCO ₃ Precursor Particles as Detected by Time-Resolved SAXS Bolze, J.; Peng, B.; Dingenouts, N. Langmuir, Vol. 18, Issue 22 https://doi.org/10.1021/la025918d	journal	October 2002
Controlled Growth of Nanoparticles from Solution with In Situ Liquid Transmission Electron Microscopy Evans, James E.; Jungjohann, Katherine L.; Browning, Nigel D. Nano Letters, Vol. 11, Issue 7 https://doi.org/10.1021/nl201166k	journal	July 2011
Direct in Situ Determination of the Mechanisms Controlling Nanoparticle Nucleation and Growth Woehl, Taylor J.; Evans, James E.; Arslan, Ilke ACS Nano, Vol. 6, Issue 10 https://doi.org/10.1021/nn303371y	journal	September 2012
Abiotic tooth enamel Yeom, Bongjun; Sain, Trisha; Lacevic, Naida Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21410	journal	March 2017
Multistep nucleation of nanocrystals in aqueous solution Loh, N. Duane; Sen, Soumyo; Bosman, Michel Nature Chemistry, Vol. 9, Issue 1 https://doi.org/10.1038/nchem.2618	journal	October 2016
Dehydration and crystallization of amorphous calcium carbonate in solution and in air Ihli, Johannes; Wong, Wai Ching; Noel, Elizabeth H. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4169	journal	January 2014
In situ liquid-cell electron microscopy of silver–palladium galvanic replacement reactions on silver nanoparticles Sutter, E.; Jungjohann, K.; Bliznakov, S. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5946	journal	September 2014
Calcium carbonate nucleation driven by ion binding in a biomimetic matrix revealed by in situ electron microscopy Smeets, Paul J. M.; Cho, Kang Rae; Kempen, Ralph G. E. Nature Materials, Vol. 14, Issue 4 https://doi.org/10.1038/nmat4193	journal	January 2015
Dynamic microscopy of nanoscale cluster growth at the solid–liquid interface Williamson, M. J.; Tromp, R. M.; Vereecken, P. M. Nature Materials, Vol. 2, Issue 8 https://doi.org/10.1038/nmat944	journal	July 2003
Is Mg-stabilized amorphous calcium carbonate a homogeneous mixture of amorphous magnesium carbonate and amorphous calcium carbonate? Yang, Sheng-Yu; Chang, Hsun-Hui; Lin, Cang-Jie Chemical Communications, Vol. 52, Issue 77 https://doi.org/10.1039/C6CC04522G	journal	January 2016
Mobility of hydrous species in amorphous calcium/magnesium carbonates Jensen, Anders C. S.; Rodriguez, Ignacio; Habraken, Wouter J. E. M. Physical Chemistry Chemical Physics, Vol. 20, Issue 29 https://doi.org/10.1039/C8CP01782D	journal	January 2018
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
Freeze-drying yields stable and pure amorphous calcium carbonate (ACC) Ihli, Johannes; Kulak, Alexander N.; Meldrum, Fiona C. Chemical Communications, Vol. 49, Issue 30 https://doi.org/10.1039/c3cc40807h	journal	January 2013
Amorphous layer around aragonite platelets in nacre Nassif, N.; Pinna, N.; Gehrke, N. Proceedings of the National Academy of Sciences, Vol. 102, Issue 36 https://doi.org/10.1073/pnas.0502577102	journal	August 2005
Transformation mechanism of amorphous calcium carbonate into calcite in the sea urchin larval spicule Politi, Y.; Metzler, R. A.; Abrecht, M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 45 https://doi.org/10.1073/pnas.0806604105	journal	November 2008
Carboxylated molecules regulate magnesium content of amorphous calcium carbonates during calcification Wang, D.; Wallace, A. F.; De Yoreo, J. J. Proceedings of the National Academy of Sciences, Vol. 106, Issue 51 https://doi.org/10.1073/pnas.0906741106	journal	December 2009
Magnesium-aspartate-based crystallization switch inspired from shell molt of crustacean Tao, Jinhui; Zhou, Dongming; Zhang, Zhisen Proceedings of the National Academy of Sciences, Vol. 106, Issue 52 https://doi.org/10.1073/pnas.0909040106	journal	December 2009
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
Nucleation of metastable aragonite CaCO ₃ in seawater Sun, Wenhao; Jayaraman, Saivenkataraman; Chen, Wei Proceedings of the National Academy of Sciences, Vol. 112, Issue 11 https://doi.org/10.1073/pnas.1423898112	journal	March 2015
Bubble nucleation and migration in a lead–iron hydr(oxide) core–shell nanoparticle Niu, Kaiyang; Frolov, Timofey; Xin, Huolin L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 42 https://doi.org/10.1073/pnas.1510342112	journal	October 2015
A classical view on nonclassical nucleation Smeets, Paul J. M.; Finney, Aaron R.; Habraken, Wouter J. E. M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 38 https://doi.org/10.1073/pnas.1700342114	journal	September 2017
Sea Urchin Spine Calcite Forms via a Transient Amorphous Calcium Carbonate Phase Politi, Y. Science, Vol. 306, Issue 5699 https://doi.org/10.1126/science.1102289	journal	November 2004
Observation of Single Colloidal Platinum Nanocrystal Growth Trajectories Zheng, H.; Smith, R. K.; Jun, Y. -w. Science, Vol. 324, Issue 5932 https://doi.org/10.1126/science.1172104	journal	June 2009
High-Resolution EM of Colloidal Nanocrystal Growth Using Graphene Liquid Cells Yuk, Jong Min; Park, Jungwon; Ercius, Peter Science, Vol. 336, Issue 6077 https://doi.org/10.1126/science.1217654	journal	April 2012
Direction-Specific Interactions Control Crystal Growth by Oriented Attachment Li, D.; Nielsen, M. H.; Lee, J. R. I. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1219643	journal	May 2012
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
The Role of Mg2+ as an Impurity in Calcite Growth Davis, K. J. Science, Vol. 290, Issue 5494 https://doi.org/10.1126/science.290.5494.1134	journal	November 2000
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
Single-particle mapping of nonequilibrium nanocrystal transformations Ye, Xingchen; Jones, Matthew R.; Frechette, Layne B. Science, Vol. 354, Issue 6314 https://doi.org/10.1126/science.aah4434	journal	November 2016
Coherently aligned nanoparticles within a biogenic single crystal: A biological prestressing strategy Polishchuk, Iryna; Bracha, Avigail Aronhime; Bloch, Leonid Science, Vol. 358, Issue 6368 https://doi.org/10.1126/science.aaj2156	journal	December 2017

Similar Records

Shape-preserving amorphous-to-crystalline transformation of CaCO3 revealed by in situ TEM

Journal Article · Mon Feb 17 23:00:00 EST 2020 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1657072

Transformation and Crystallization Energetics of Synthetic and Biogenic Amorphous Calcium Carbonate

Journal Article · Thu Dec 31 23:00:00 EST 2009 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1065525

Complementary Control by Additives of the Kinetics of Amorphous CaCO{sub 3} Mineralization at an Organic Interface: In-Situ Synchrotron X-Ray Observations

Journal Article · Fri Jul 28 00:00:00 EDT 2006 · Physical Review Letters · OSTI ID:20860580

Shape-preserving amorphous-to-crystalline transformation of CaCO 3 revealed by in situ TEM

Citation Formats

References (58)

Similar Records

Related Subjects

Shape-preserving amorphous-to-crystalline transformation of CaCO ₃ revealed by in situ TEM