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

Abstract

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.

Authors:
; ; ; ; ORCiD logo; ; ;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1597119
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 117 Journal Issue: 7; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Liu, Zhaoming, Zhang, Zhisen, Wang, Zheming, Jin, Biao, Li, Dongsheng, Tao, Jinhui, Tang, Ruikang, and De Yoreo, James J. Shape-preserving amorphous-to-crystalline transformation of CaCO 3 revealed by in situ TEM. United States: N. p., 2020. Web. doi:10.1073/pnas.1914813117.
Liu, Zhaoming, Zhang, Zhisen, Wang, Zheming, Jin, Biao, Li, Dongsheng, Tao, Jinhui, Tang, Ruikang, & De Yoreo, James J. Shape-preserving amorphous-to-crystalline transformation of CaCO 3 revealed by in situ TEM. United States. doi:10.1073/pnas.1914813117.
Liu, Zhaoming, Zhang, Zhisen, Wang, Zheming, Jin, Biao, Li, Dongsheng, Tao, Jinhui, Tang, Ruikang, and De Yoreo, James J. Mon . "Shape-preserving amorphous-to-crystalline transformation of CaCO 3 revealed by in situ TEM". United States. doi:10.1073/pnas.1914813117.
@article{osti_1597119,
title = {Shape-preserving amorphous-to-crystalline transformation of CaCO 3 revealed by in situ TEM},
author = {Liu, Zhaoming and Zhang, Zhisen and Wang, Zheming and Jin, Biao and Li, Dongsheng and Tao, Jinhui and Tang, Ruikang and De Yoreo, James J.},
abstractNote = {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.},
doi = {10.1073/pnas.1914813117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 7,
volume = 117,
place = {United States},
year = {2020},
month = {2}
}

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Works referenced in this record:

Direction-Specific Interactions Control Crystal Growth by Oriented Attachment
journal, May 2012


Particle Accretion Mechanism Underlies Biological Crystal Growth from an Amorphous Precursor Phase
journal, July 2014

  • Gal, Assaf; Kahil, Keren; Vidavsky, Netta
  • Advanced Functional Materials, Vol. 24, Issue 34
  • DOI: 10.1002/adfm.201400676

Sea Urchin Spine Calcite Forms via a Transient Amorphous Calcium Carbonate Phase
journal, November 2004


Taking Advantage of Disorder: Amorphous Calcium Carbonate and Its Roles in Biomineralization
journal, June 2003


Hydrogen Bonding in Amorphous Calcium Carbonate and Molecular Reorientation Induced by Dehydration
journal, February 2018

  • Jensen, Anders C. S.; Imberti, Silvia; Parker, Stewart F.
  • The Journal of Physical Chemistry C, Vol. 122, Issue 6
  • DOI: 10.1021/acs.jpcc.7b10459

Derivation of an Accurate Force-Field for Simulating the Growth of Calcium Carbonate from Aqueous Solution: A New Model for the Calcite−Water Interface
journal, February 2010

  • Raiteri, Paolo; Gale, Julian D.; Quigley, David
  • The Journal of Physical Chemistry C, Vol. 114, Issue 13
  • DOI: 10.1021/jp910977a

Crystallization by particle attachment in synthetic, biogenic, and geologic environments
journal, July 2015

  • De Yoreo, J. J.; Gilbert, P. U. P. A.; Sommerdijk, N. A. J. M.
  • Science, Vol. 349, Issue 6247
  • DOI: 10.1126/science.aaa6760

Observation of Single Colloidal Platinum Nanocrystal Growth Trajectories
journal, June 2009


Dehydration and crystallization of amorphous calcium carbonate in solution and in air
journal, January 2014

  • Ihli, Johannes; Wong, Wai Ching; Noel, Elizabeth H.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4169

In situ TEM imaging of CaCO3 nucleation reveals coexistence of direct and indirect pathways
journal, September 2014


Freeze-drying yields stable and pure amorphous calcium carbonate (ACC)
journal, January 2013

  • Ihli, Johannes; Kulak, Alexander N.; Meldrum, Fiona C.
  • Chemical Communications, Vol. 49, Issue 30
  • DOI: 10.1039/c3cc40807h

Revealing the Cluster‐Cloud and Its Role in Nanocrystallization
journal, February 2019


Calcium carbonate nucleation driven by ion binding in a biomimetic matrix revealed by in situ electron microscopy
journal, January 2015

  • Smeets, Paul J. M.; Cho, Kang Rae; Kempen, Ralph G. E.
  • Nature Materials, Vol. 14, Issue 4
  • DOI: 10.1038/nmat4193

Amorphous layer around aragonite platelets in nacre
journal, August 2005

  • Nassif, N.; Pinna, N.; Gehrke, N.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 36
  • DOI: 10.1073/pnas.0502577102

Direct in Situ Determination of the Mechanisms Controlling Nanoparticle Nucleation and Growth
journal, September 2012

  • Woehl, Taylor J.; Evans, James E.; Arslan, Ilke
  • ACS Nano, Vol. 6, Issue 10
  • DOI: 10.1021/nn303371y

Formation and Growth of Amorphous Colloidal CaCO 3 Precursor Particles as Detected by Time-Resolved SAXS
journal, October 2002

  • Bolze, J.; Peng, B.; Dingenouts, N.
  • Langmuir, Vol. 18, Issue 22
  • DOI: 10.1021/la025918d

Role of Magnesium Ion in the Stabilization of Biogenic Amorphous Calcium Carbonate: A Structure−Function Investigation
journal, January 2010

  • Politi, Yael; Batchelor, David R.; Zaslansky, Paul
  • Chemistry of Materials, Vol. 22, Issue 1
  • DOI: 10.1021/cm902674h

Inhibitory Effect of Magnesium and Zinc on Crystallization Kinetics of Hydroxyapatite (0001) Face
journal, May 2000

  • Kanzaki, Noriko; Onuma, Kazuo; Treboux, Gabin
  • The Journal of Physical Chemistry B, Vol. 104, Issue 17
  • DOI: 10.1021/jp9939726

Electron–Water Interactions and Implications for Liquid Cell Electron Microscopy
journal, September 2014

  • Schneider, Nicholas M.; Norton, Michael M.; Mendel, Brian J.
  • The Journal of Physical Chemistry C, Vol. 118, Issue 38
  • DOI: 10.1021/jp507400n

Biomimetic synthesis of calcite films by a polymer-induced liquid-precursor (PILP) process
journal, September 2007


Biomimetic Model Systems for Investigating the Amorphous Precursor Pathway and Its Role in Biomineralization
journal, November 2008


Water Is the Key to Nonclassical Nucleation of Amorphous Calcium Carbonate
journal, December 2010

  • Raiteri, Paolo; Gale, Julian D.
  • Journal of the American Chemical Society, Vol. 132, Issue 49
  • DOI: 10.1021/ja108508k

Dynamic microscopy of nanoscale cluster growth at the solid–liquid interface
journal, July 2003

  • Williamson, M. J.; Tromp, R. M.; Vereecken, P. M.
  • Nature Materials, Vol. 2, Issue 8
  • DOI: 10.1038/nmat944

Calcium Carbonate Polyamorphism and Its Role in Biomineralization: How Many Amorphous Calcium Carbonates Are There?
journal, November 2012

  • Cartwright, Julyan H. E.; Checa, Antonio G.; Gale, Julian D.
  • Angewandte Chemie International Edition, Vol. 51, Issue 48
  • DOI: 10.1002/anie.201203125

Multistep nucleation of nanocrystals in aqueous solution
journal, October 2016

  • Loh, N. Duane; Sen, Soumyo; Bosman, Michel
  • Nature Chemistry, Vol. 9, Issue 1
  • DOI: 10.1038/nchem.2618

Calcite Crystal Growth by a Solid-State Transformation of Stabilized Amorphous Calcium Carbonate Nanospheres in a Hydrogel
journal, April 2013

  • Gal, Assaf; Habraken, Wouter; Gur, Dvir
  • Angewandte Chemie International Edition, Vol. 52, Issue 18
  • DOI: 10.1002/anie.201210329

Is Mg-stabilized amorphous calcium carbonate a homogeneous mixture of amorphous magnesium carbonate and amorphous calcium carbonate?
journal, January 2016

  • Yang, Sheng-Yu; Chang, Hsun-Hui; Lin, Cang-Jie
  • Chemical Communications, Vol. 52, Issue 77
  • DOI: 10.1039/C6CC04522G

Effects of Magnesium Ions and Water Molecules on the Structure of Amorphous Calcium Carbonate: A Molecular Dynamics Study
journal, November 2013

  • Tomono, Hidekazu; Nada, Hiroki; Zhu, Fangjie
  • The Journal of Physical Chemistry B, Vol. 117, Issue 47
  • DOI: 10.1021/jp407721x

Carboxylated molecules regulate magnesium content of amorphous calcium carbonates during calcification
journal, December 2009

  • Wang, D.; Wallace, A. F.; De Yoreo, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 51
  • DOI: 10.1073/pnas.0906741106

Single-particle mapping of nonequilibrium nanocrystal transformations
journal, November 2016


Morphological influence of magnesium and organic additives on the precipitation of calcite
journal, October 2001


A classical view on nonclassical nucleation
journal, September 2017

  • Smeets, Paul J. M.; Finney, Aaron R.; Habraken, Wouter J. E. M.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 38
  • DOI: 10.1073/pnas.1700342114

Controlled Growth of Nanoparticles from Solution with In Situ Liquid Transmission Electron Microscopy
journal, July 2011

  • Evans, James E.; Jungjohann, Katherine L.; Browning, Nigel D.
  • Nano Letters, Vol. 11, Issue 7
  • DOI: 10.1021/nl201166k

FTIR techniques in clay mineral studies
journal, January 2003


Nucleation of metastable aragonite CaCO 3 in seawater
journal, March 2015

  • Sun, Wenhao; Jayaraman, Saivenkataraman; Chen, Wei
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
  • DOI: 10.1073/pnas.1423898112

Calcium Carbonate Formation and Dissolution
journal, February 2007

  • Morse, John W.; Arvidson, Rolf S.; Lüttge, Andreas
  • Chemical Reviews, Vol. 107, Issue 2
  • DOI: 10.1021/cr050358j

Pressure-Induced Polyamorphism and Formation of ‘Aragonitic’ Amorphous Calcium Carbonate
journal, July 2013

  • Fernandez-Martinez, Alejandro; Kalkan, Bora; Clark, Simon M.
  • Angewandte Chemie International Edition, Vol. 52, Issue 32
  • DOI: 10.1002/anie.201302974

The thermodynamics of calcite nucleation at organic interfaces: Classical vs. non-classical pathways
journal, January 2012

  • Hu, Q.; Nielsen, M. H.; Freeman, C. L.
  • Faraday Discussions, Vol. 159
  • DOI: 10.1039/c2fd20124k

The Development of Morphology and Structure in Hexagonal Vaterite
journal, August 2010

  • Pouget, Emilie M.; Bomans, Paul H. H.; Dey, Archan
  • Journal of the American Chemical Society, Vol. 132, Issue 33
  • DOI: 10.1021/ja102439r

Mobility of hydrous species in amorphous calcium/magnesium carbonates
journal, January 2018

  • Jensen, Anders C. S.; Rodriguez, Ignacio; Habraken, Wouter J. E. M.
  • Physical Chemistry Chemical Physics, Vol. 20, Issue 29
  • DOI: 10.1039/C8CP01782D

Coherently aligned nanoparticles within a biogenic single crystal: A biological prestressing strategy
journal, December 2017

  • Polishchuk, Iryna; Bracha, Avigail Aronhime; Bloch, Leonid
  • Science, Vol. 358, Issue 6368
  • DOI: 10.1126/science.aaj2156

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
journal, January 1996

  • Gutjahr, Astrid; Dabringhaus, Heinz; Lacmann, Rolf
  • Journal of Crystal Growth, Vol. 158, Issue 3, p. 310-315
  • DOI: 10.1016/0022-0248(95)00447-5

Chemical controls on the magnesium content of amorphous calcium carbonate
journal, January 2015


High-Resolution EM of Colloidal Nanocrystal Growth Using Graphene Liquid Cells
journal, April 2012


Bubble nucleation and migration in a lead–iron hydr(oxide) core–shell nanoparticle
journal, October 2015

  • Niu, Kaiyang; Frolov, Timofey; Xin, Huolin L.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 42
  • DOI: 10.1073/pnas.1510342112

In situ liquid-cell electron microscopy of silver–palladium galvanic replacement reactions on silver nanoparticles
journal, September 2014

  • Sutter, E.; Jungjohann, K.; Bliznakov, S.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5946

Magnesium-aspartate-based crystallization switch inspired from shell molt of crustacean
journal, December 2009

  • Tao, Jinhui; Zhou, Dongming; Zhang, Zhisen
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 52
  • DOI: 10.1073/pnas.0909040106

Mechanism of Calcite Co-Orientation in the Sea Urchin Tooth
journal, December 2009

  • Killian, Christopher E.; Metzler, Rebecca A.; Gong, Y. U. T.
  • Journal of the American Chemical Society, Vol. 131, Issue 51
  • DOI: 10.1021/ja907063z

Understanding the Control of Mineralization by Polyelectrolyte Additives: Simulation of Preferential Binding to Calcite Surfaces
journal, March 2013

  • Shen, Jia-Wei; Li, Chunli; van der Vegt, Nico F. A.
  • The Journal of Physical Chemistry C, Vol. 117, Issue 13
  • DOI: 10.1021/jp402341w

Abiotic tooth enamel
journal, March 2017

  • Yeom, Bongjun; Sain, Trisha; Lacevic, Naida
  • Nature, Vol. 543, Issue 7643
  • DOI: 10.1038/nature21410

Phase transitions in biogenic amorphous calcium carbonate
journal, April 2012

  • Gong, Y. U. T.; Killian, C. E.; Olson, I. C.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 16
  • DOI: 10.1073/pnas.1118085109

Formation of High-Magnesian Calcites via an Amorphous Precursor Phase: Possible Biological Implications
journal, January 2000


Chemical and physical controls on the transformation of amorphous calcium carbonate into crystalline CaCO3 polymorphs
journal, January 2017


Transformation mechanism of amorphous calcium carbonate into calcite in the sea urchin larval spicule
journal, November 2008

  • Politi, Y.; Metzler, R. A.; Abrecht, M.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 45
  • DOI: 10.1073/pnas.0806604105

The role of magnesium in stabilising amorphous calcium carbonate and controlling calcite morphologies
journal, June 2003


The Role of Mg2+ as an Impurity in Calcite Growth
journal, November 2000


Role of Impurities in the Kinetic Persistence of Amorphous Calcium Carbonate: A Nanoscopic Dynamics View
journal, July 2018

  • Koishi, Ayumi; Fernandez-Martinez, Alejandro; Ruta, Beatrice
  • The Journal of Physical Chemistry C, Vol. 122, Issue 29
  • DOI: 10.1021/acs.jpcc.8b05189