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Title: Direct observation of mineral–organic composite formation reveals occlusion mechanism

Abstract

Manipulation of inorganic materials with organic macromolecules enables organisms to create biominerals such as bones and seashells, where occlusion of biomacromolecules within individual crystals generates superior mechanical properties. Current understanding of this process largely comes from studying the entrapment of micron-size particles in cooling melts. Here, by investigating micelle incorporation in calcite with atomic force microscopy and micromechanical simulations, we show that different mechanisms govern nanoscale occlusion. By simultaneously visualizing the micelles and propagating step edges, we demonstrate that the micelles experience significant compression during occlusion, which is accompanied by cavity formation. This generates local lattice strain, leading to enhanced mechanical properties. Furthermore, these results give new insight into the formation of occlusions in natural and synthetic crystals, and will facilitate the synthesis of multifunctional nanocomposite crystals.

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [5];  [2];  [6];  [6];  [3];  [2];  [7]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  2. Univ. of Leeds, Leeds (United Kingdom)
  3. Univ. of Sheffield, Sheffield (United Kingdom)
  4. Stanford Univ., Stanford, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Zhejiang Univ., Hangzhou (China)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1249368
Alternate Identifier(s):
OSTI ID: 1379025; OSTI ID: 1474347; OSTI ID: 1526977
Report Number(s):
PNNL-SA-114998; LLNL-JRNL-673292
Journal ID: ISSN 2041-1723; ncomms10187
Grant/Contract Number:  
AC05-76RL01830; AC02-05CH11231; AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 36 MATERIALS SCIENCE; physical sciences; bioengineering; materials science; physical chemistry; Materials science, Biological and medical sciences, Chemistry - Inorganic, organic, physical and analytical chemistry

Citation Formats

Cho, Kang Rae, Kim, Yi -Yeoun, Yang, Pengcheng, Cai, Wei, Pan, Haihua, Kulak, Alexander N., Lau, Jolene L., Kulshreshtha, Prashant, Armes, Steven P., Meldrum, Fiona C., and De Yoreo, James J. Direct observation of mineral–organic composite formation reveals occlusion mechanism. United States: N. p., 2016. Web. doi:10.1038/ncomms10187.
Cho, Kang Rae, Kim, Yi -Yeoun, Yang, Pengcheng, Cai, Wei, Pan, Haihua, Kulak, Alexander N., Lau, Jolene L., Kulshreshtha, Prashant, Armes, Steven P., Meldrum, Fiona C., & De Yoreo, James J. Direct observation of mineral–organic composite formation reveals occlusion mechanism. United States. doi:10.1038/ncomms10187.
Cho, Kang Rae, Kim, Yi -Yeoun, Yang, Pengcheng, Cai, Wei, Pan, Haihua, Kulak, Alexander N., Lau, Jolene L., Kulshreshtha, Prashant, Armes, Steven P., Meldrum, Fiona C., and De Yoreo, James J. Wed . "Direct observation of mineral–organic composite formation reveals occlusion mechanism". United States. doi:10.1038/ncomms10187. https://www.osti.gov/servlets/purl/1249368.
@article{osti_1249368,
title = {Direct observation of mineral–organic composite formation reveals occlusion mechanism},
author = {Cho, Kang Rae and Kim, Yi -Yeoun and Yang, Pengcheng and Cai, Wei and Pan, Haihua and Kulak, Alexander N. and Lau, Jolene L. and Kulshreshtha, Prashant and Armes, Steven P. and Meldrum, Fiona C. and De Yoreo, James J.},
abstractNote = {Manipulation of inorganic materials with organic macromolecules enables organisms to create biominerals such as bones and seashells, where occlusion of biomacromolecules within individual crystals generates superior mechanical properties. Current understanding of this process largely comes from studying the entrapment of micron-size particles in cooling melts. Here, by investigating micelle incorporation in calcite with atomic force microscopy and micromechanical simulations, we show that different mechanisms govern nanoscale occlusion. By simultaneously visualizing the micelles and propagating step edges, we demonstrate that the micelles experience significant compression during occlusion, which is accompanied by cavity formation. This generates local lattice strain, leading to enhanced mechanical properties. Furthermore, these results give new insight into the formation of occlusions in natural and synthetic crystals, and will facilitate the synthesis of multifunctional nanocomposite crystals.},
doi = {10.1038/ncomms10187},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {1}
}

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Works referenced in this record:

Intercalation of Sea Urchin Proteins in Calcite: Study of a Crystalline Composite Material
journal, November 1990


Limits on Surface Vicinality and Growth Rate due to Hollow Dislocation Cores on KDP { 101 }
journal, June 1997


Calcite Prisms from Mollusk Shells (Atrina Rigida): Swiss-cheese-like Organic-Inorganic Single-crystal Composites
journal, April 2011

  • Li, Hanying; Xin, Huolin L.; Kunitake, Miki E.
  • Advanced Functional Materials, Vol. 21, Issue 11
  • DOI: 10.1002/adfm.201002709

Thermodynamics of Calcite Growth: Baseline for Understanding Biomineral Formation
journal, October 1998


Nacre Protein Fragment Templates Lamellar Aragonite Growth
journal, May 2010

  • Metzler, Rebecca A.; Evans, John Spencer; Killian, Christopher E.
  • Journal of the American Chemical Society, Vol. 132, Issue 18
  • DOI: 10.1021/ja909735y

One-pot synthesis of an inorganic heterostructure: uniform occlusion of magnetite nanoparticles within calcite single crystals
journal, January 2014

  • Kulak, Alexander N.; Semsarilar, Mona; Kim, Yi-Yeoun
  • Chem. Sci., Vol. 5, Issue 2
  • DOI: 10.1039/C3SC52615A

Interaction Between Particles and a Solid‐Liquid Interface
journal, October 1964

  • Uhlmann, D. R.; Chalmers, B.; Jackson, K. A.
  • Journal of Applied Physics, Vol. 35, Issue 10
  • DOI: 10.1063/1.1713142

Colouring crystals with inorganic nanoparticles
journal, January 2014

  • Kulak, Alexander N.; Yang, Pengcheng; Kim, Yi-Yeoun
  • Chem. Commun., Vol. 50, Issue 1
  • DOI: 10.1039/C3CC47904H

Interactions of sea-urchin skeleton macromolecules with growing calcite crystals— a study of intracrystalline proteins
journal, February 1988

  • Herman, A.; Addadi, L.; Weiner, S.
  • Nature, Vol. 331, Issue 6156
  • DOI: 10.1038/331546a0

Investigations of voids in the aragonite platelets of nacre
journal, October 2009


Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth
journal, December 2006

  • Elhadj, S.; De Yoreo, J. J.; Hoyer, J. R.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 51, p. 19237-19242
  • DOI: 10.1073/pnas.0605748103

Synthesis of Zwitterionic Diblock Copolymers without Protecting Group Chemistry
journal, January 2007

  • Vo, Cong-Duan; Armes, Steven P.; Randall, David P.
  • Macromolecules, Vol. 40, Issue 2
  • DOI: 10.1021/ma062648n

Materials design in biology
journal, June 2000


Bio-Inspired Synthesis and Mechanical Properties of Calcite-Polymer Particle Composites
journal, March 2010

  • Kim, Yi-Yeoun; Ribeiro, Luis; Maillot, Fabien
  • Advanced Materials, Vol. 22, Issue 18
  • DOI: 10.1002/adma.200903743

New insights into mechanisms of biomolecular control on growth of inorganic crystals
journal, January 2007

  • De Yoreo, James J.; Wierzbicki, Andrzej; Dove, Patricia M.
  • CrystEngComm, Vol. 9, Issue 12
  • DOI: 10.1039/b713006f

Bio-Inspired Band Gap Engineering of Zinc Oxide by Intracrystalline Incorporation of Amino Acids
journal, October 2013

  • Brif, Anastasia; Ankonina, Guy; Drathen, Christina
  • Advanced Materials, Vol. 26, Issue 3
  • DOI: 10.1002/adma.201303596

An artificial biomineral formed by incorporation of copolymer micelles in calcite crystals
journal, September 2011

  • Kim, Yi-Yeoun; Ganesan, Kathirvel; Yang, Pengcheng
  • Nature Materials, Vol. 10, Issue 11
  • DOI: 10.1038/nmat3103

Visualizing the 3D Internal Structure of Calcite Single Crystals Grown in Agarose Hydrogels
journal, November 2009


An in-situ AFM investigation of canavalin crystallization kinetics
journal, July 1997


Additive controlled crystallization
journal, January 2011


The interaction between a particle and an advancing solidification front
journal, September 1999


Calcite Growth in Hydrogels: Assessing the Mechanism of Polymer-Network Incorporation into Single Crystals
journal, January 2009


The Microstructure of Biogenic Calcite: A View by High-Resolution Synchrotron Powder Diffraction
journal, September 2006


Nanoscale chemical tomography of buried organic–inorganic interfaces in the chiton tooth
journal, January 2011


Design strategies in mineralized biological materials
journal, January 1997

  • Weiner, Stephen; Addadi, Lia
  • Journal of Materials Chemistry, Vol. 7, Issue 5
  • DOI: 10.1039/a604512j

Controlling Mineral Morphologies and Structures in Biological and Synthetic Systems
journal, November 2008

  • Meldrum, Fiona C.; Cölfen, Helmut
  • Chemical Reviews, Vol. 108, Issue 11
  • DOI: 10.1021/cr8002856

A critical analysis of calcium carbonate mesocrystals
journal, July 2014

  • Kim, Yi-Yeoun; Schenk, Anna S.; Ihli, Johannes
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5341

    Works referencing / citing this record:

    The Effect of Additives on the Early Stages of Growth of Calcite Single Crystals
    journal, August 2017

    • Kim, Yi-Yeoun; Freeman, Colin L.; Gong, Xiuqing
    • Angewandte Chemie International Edition, Vol. 56, Issue 39
    • DOI: 10.1002/anie.201706800

    3D visualization of additive occlusion and tunable full-spectrum fluorescence in calcite
    journal, November 2016

    • Green, David C.; Ihli, Johannes; Thornton, Paul D.
    • Nature Communications, Vol. 7, Issue 1
    • DOI: 10.1038/ncomms13524