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Title: On Simulating the Formation of Structured, Crystalline Systems via Non-classical Pathways

Abstract

Observations in crystal growth and assembly from recent in situ methods suggest alternative, non-classical crystallization pathways play an important role in the determination of the micro- and meso- structures in crystalline systems. These processes display parallels that cross-cut multiple disciplines investigating crystallization across four orders of magnitude in size scales and widely differing environments, hinting that alternative crystal growth pathways may be a fundamental scheme in natural crystal formation. Using a system of short-range attractive microbeads, we demonstrate that the addition of a small concentration of sub-species incommensurate with the lattice spacing of the dominant species results in a stark change in crystal size and morphology. These changes are attributed to the presence of fleeting, amorphous-like configurations of beads that ultimately change the melting and growth dynamics in preferred directions. From these real-time observations, we hypothesize the amorphous mineral precursors present in biological mineralized tissues undergo similar non-classical crystallization processes resulting in the complex structures found in biomineralization.

Authors:
 [1];  [2]
  1. BitWrex, LLC, Morton, IL (United States)
  2. Univ. of California, San Francisco, CA (United States). Dept. of Bioengineering and Therapeutic Sciences; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Foundry
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
OSTI Identifier:
1635187
Grant/Contract Number:  
AC02-05CH11231; 1507607; 0654193
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Materials
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2296-8016
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; non-classical crystallization pathways; biological mineralization; multiscale interactions; bead-bead interactions; amorphous precursors; colloidal crystallization

Citation Formats

Mergo III, John C., and Seto, Jong. On Simulating the Formation of Structured, Crystalline Systems via Non-classical Pathways. United States: N. p., 2020. Web. doi:10.3389/fmats.2020.00075.
Mergo III, John C., & Seto, Jong. On Simulating the Formation of Structured, Crystalline Systems via Non-classical Pathways. United States. https://doi.org/10.3389/fmats.2020.00075
Mergo III, John C., and Seto, Jong. Wed . "On Simulating the Formation of Structured, Crystalline Systems via Non-classical Pathways". United States. https://doi.org/10.3389/fmats.2020.00075. https://www.osti.gov/servlets/purl/1635187.
@article{osti_1635187,
title = {On Simulating the Formation of Structured, Crystalline Systems via Non-classical Pathways},
author = {Mergo III, John C. and Seto, Jong},
abstractNote = {Observations in crystal growth and assembly from recent in situ methods suggest alternative, non-classical crystallization pathways play an important role in the determination of the micro- and meso- structures in crystalline systems. These processes display parallels that cross-cut multiple disciplines investigating crystallization across four orders of magnitude in size scales and widely differing environments, hinting that alternative crystal growth pathways may be a fundamental scheme in natural crystal formation. Using a system of short-range attractive microbeads, we demonstrate that the addition of a small concentration of sub-species incommensurate with the lattice spacing of the dominant species results in a stark change in crystal size and morphology. These changes are attributed to the presence of fleeting, amorphous-like configurations of beads that ultimately change the melting and growth dynamics in preferred directions. From these real-time observations, we hypothesize the amorphous mineral precursors present in biological mineralized tissues undergo similar non-classical crystallization processes resulting in the complex structures found in biomineralization.},
doi = {10.3389/fmats.2020.00075},
journal = {Frontiers in Materials},
number = ,
volume = 7,
place = {United States},
year = {Wed Apr 08 00:00:00 EDT 2020},
month = {Wed Apr 08 00:00:00 EDT 2020}
}

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Figures / Tables:

FIGURE 1 FIGURE 1: Biological crystallization of diverse mineralized tissues ranging from sea urchin spines to bones and teeth demonstrate a non-classical crystallization pathway. From calcium carbonate (CaCO3) to hydroxyapatite (Ca10(PO4)6(OH)), these divergent mineralization systems have been found to contain intermediates mineral phases not explained by classical crystallization theories. Adapted from Coelfenmore » and Antonietti (2008) with permission from John Wiley and Sons.« less

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Works referenced in this record:

Prediction of absolute crystal-nucleation rate in hard-sphere colloids
journal, February 2001

  • Auer, Stefan; Frenkel, Daan
  • Nature, Vol. 409, Issue 6823
  • DOI: 10.1038/35059035

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


Observing crystal nucleation in four dimensions using atomic electron tomography
journal, June 2019


Multiscale Toughening Mechanisms in Biological Materials and Bioinspired Designs
journal, July 2019

  • Huang, Wei; Restrepo, David; Jung, Jae‐Young
  • Advanced Materials, Vol. 31, Issue 43
  • DOI: 10.1002/adma.201901561

Entropy-driven crystal formation on highly strained substrates
journal, May 2013

  • Savage, John R.; Hopp, Stefan F.; Ganapathy, Rajesh
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 23
  • DOI: 10.1073/pnas.1221529110

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


Crystallization Pathways in Biomineralization
journal, August 2011


Control of Polymorph Selection in Amorphous Calcium Carbonate Crystallization by Poly(Aspartic Acid): Two Different Mechanisms
journal, April 2017


Density of Nanometrically Thin Amorphous Films Varies by Thickness
journal, May 2017


Crystal nucleation of hard spheres using molecular dynamics, umbrella sampling, and forward flux sampling: A comparison of simulation techniques
journal, December 2010

  • Filion, L.; Hermes, M.; Ni, R.
  • The Journal of Chemical Physics, Vol. 133, Issue 24
  • DOI: 10.1063/1.3506838

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


On Mineral Retrosynthesis of a Complex Biogenic Scaffold
journal, March 2017


Direct measurement of the free energy by optical microscopy
journal, January 2006

  • Dullens, R. P. A.; Aarts, D. G. A. L.; Kegel, W. K.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507052103

Building two-dimensional materials one row at a time: Avoiding the nucleation barrier
journal, December 2018


Mesocrystals and Nonclassical Crystallization
book, January 2008


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

Shaping Magnetite with Poly- l -arginine and pH: From Small Single Crystals to Large Mesocrystals
journal, August 2019

  • Kuhrts, Lucas; Macías-Sánchez, Elena; Tarakina, Nadezda V.
  • The Journal of Physical Chemistry Letters, Vol. 10, Issue 18
  • DOI: 10.1021/acs.jpclett.9b01771

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


Experimental Evidence for Two-Step Nucleation in Colloidal Crystallization
journal, May 2009


Artificial coiled coil biomineralisation protein for the synthesis of magnetic nanoparticles
journal, June 2019

  • Rawlings, Andrea E.; Somner, Lori A.; Fitzpatrick-Milton, Michaela
  • Nature Communications, Vol. 10, Issue 1
  • DOI: 10.1038/s41467-019-10578-2

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

The Stomatopod Dactyl Club: A Formidable Damage-Tolerant Biological Hammer
journal, June 2012


From Ostwald Ripening to Single Chirality
journal, November 2009

  • Noorduin, Wim L.; Vlieg, Elias; Kellogg, Richard M.
  • Angewandte Chemie International Edition, Vol. 48, Issue 51
  • DOI: 10.1002/anie.200905215

Biomineralization-Inspired Material Design for Bone Regeneration
journal, September 2018

  • de Melo Pereira, Daniel; Habibovic, Pamela
  • Advanced Healthcare Materials, Vol. 7, Issue 22
  • DOI: 10.1002/adhm.201800700

Crack driving force in twisted plywood structures
journal, June 2017


Stable prenucleation mineral clusters are liquid-like ionic polymers
journal, September 2011

  • Demichelis, Raffaella; Raiteri, Paolo; Gale, Julian D.
  • Nature Communications, Vol. 2, Issue 1
  • DOI: 10.1038/ncomms1604

Rationally Designed Complex, Hierarchical Microarchitectures
journal, May 2013


Methods of Digital Video Microscopy for Colloidal Studies
journal, April 1996

  • Crocker, John C.; Grier, David G.
  • Journal of Colloid and Interface Science, Vol. 179, Issue 1
  • DOI: 10.1006/jcis.1996.0217

Hierarchical Calcite Crystals with Occlusions of a Simple Polyelectrolyte Mimic Complex Biomineral Structures
journal, July 2012

  • Schenk, Anna S.; Zlotnikov, Igor; Pokroy, Boaz
  • Advanced Functional Materials, Vol. 22, Issue 22
  • DOI: 10.1002/adfm.201201158

Impact of the colloidal state on the oriented attachment growth mechanism
journal, January 2010

  • Dalmaschio, Cleocir José; Ribeiro, Caue; Leite, Edson Roberto
  • Nanoscale, Vol. 2, Issue 11
  • DOI: 10.1039/c0nr00338g

Three-dimensional oriented attachment growth of single-crystal pre-perovskite PbTiO 3 hollowed fibers
journal, January 2018

  • Zhao, Ruoyu; Li, Ming; Ren, Zhaohui
  • CrystEngComm, Vol. 20, Issue 4
  • DOI: 10.1039/c7ce01780d

On Interaction between Two Bodies Immersed in a Solution of Macromolecules
journal, July 1954

  • Asakura, Sho; Oosawa, Fumio
  • The Journal of Chemical Physics, Vol. 22, Issue 7
  • DOI: 10.1063/1.1740347

Role of clusters in nonclassical nucleation and growth of protein crystals
journal, January 2014

  • Sleutel, Mike; Van Driessche, Alexander E. S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 5
  • DOI: 10.1073/pnas.1309320111

Self-catalyzed growth of S layers via an amorphous-to-crystalline transition limited by folding kinetics
journal, September 2010

  • Chung, S.; Shin, S. -H.; Bertozzi, C. R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 38
  • DOI: 10.1073/pnas.1008280107

Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate
journal, February 2013

  • Habraken, Wouter J. E. M.; Tao, Jinhui; Brylka, Laura J.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms2490

Melting of Metastable Crystallites in Charge-Stabilized Colloidal Suspensions
journal, May 1996


Biomimetic mineralization of collagen via an enzyme-aided PILP process
journal, April 2010


Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite
journal, August 2002

  • Weiss, Ingrid Maria; Tuross, Noreen; Addadi, Lia
  • Journal of Experimental Zoology, Vol. 293, Issue 5
  • DOI: 10.1002/jez.90004

Formation and transformation of a short range ordered iron carbonate precursor
journal, September 2015

  • Dideriksen, Knud; Frandsen, Cathrine; Bovet, Nicolas
  • Geochimica et Cosmochimica Acta, Vol. 164
  • DOI: 10.1016/j.gca.2015.05.005

Tough, Bio-Inspired Hybrid Materials
journal, December 2008


Nucleation and growth of magnetite from solution
journal, February 2013

  • Baumgartner, Jens; Dey, Archan; Bomans, Paul H. H.
  • Nature Materials, Vol. 12, Issue 4
  • DOI: 10.1038/nmat3558

Structural Biological Materials: Critical Mechanics-Materials Connections
journal, February 2013


Principles of Crystal Nucleation and Growth
journal, January 2003

  • De Yoreo, J. J.
  • Reviews in Mineralogy and Geochemistry, Vol. 54, Issue 1
  • DOI: 10.2113/0540057

The role of prenucleation clusters in surface-induced calcium phosphate crystallization
journal, November 2010

  • Dey, Archan; Bomans, Paul H. H.; Müller, Frank A.
  • Nature Materials, Vol. 9, Issue 12
  • DOI: 10.1038/nmat2900

Mesocrystalline calcium silicate hydrate: A bioinspired route toward elastic concrete materials
journal, November 2017

  • Picker, Andreas; Nicoleau, Luc; Burghard, Zaklina
  • Science Advances, Vol. 3, Issue 11
  • DOI: 10.1126/sciadv.1701216

The energetic basis for hydroxyapatite mineralization by amelogenin variants provides insights into the origin of amelogenesis imperfecta
journal, June 2019

  • Tao, Jinhui; Shin, Yongsoon; Jayasinha, Rajith
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 28
  • DOI: 10.1073/pnas.1815654116

The localization of occluded matrix proteins in calcareous spicules of sea urchin larvae
journal, October 2004

  • Seto, Jong; Zhang, Yang; Hamilton, Patricia
  • Journal of Structural Biology, Vol. 148, Issue 1
  • DOI: 10.1016/j.jsb.2004.04.001

Imaging the Sublimation Dynamics of Colloidal Crystallites
journal, November 2006


Formation of Aragonitic Layered Structures from Kaolinite and Amorphous Calcium Carbonate Precursors
journal, December 2012

  • Seto, Jong; Azaı̈s, Thierry; Cölfen, Helmut
  • Langmuir, Vol. 29, Issue 24
  • DOI: 10.1021/la400442j

Influence of metal coordination and light irradiation on hierarchical self-assembly processes
journal, January 2019

  • Kartha, Kalathil K.; Allampally, Naveen Kumar; Politi, Antiope T.
  • Chemical Science, Vol. 10, Issue 3
  • DOI: 10.1039/c8sc03875a

Ostwald’s Rule of Stages and Its Role in CdSe Quantum Dot Crystallization
journal, October 2012

  • Washington, Aaron L.; Foley, Megan E.; Cheong, Soshan
  • Journal of the American Chemical Society, Vol. 134, Issue 41
  • DOI: 10.1021/ja302964e

Tuning crystallization pathways through sequence engineering of biomimetic polymers
journal, April 2017

  • Ma, Xiang; Zhang, Shuai; Jiao, Fang
  • Nature Materials, Vol. 16, Issue 7
  • DOI: 10.1038/nmat4891

Minerals formed by organisms
journal, March 1981


The two-step mechanism of nucleation of crystals in solution
journal, January 2010


The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite
journal, July 2012

  • Wang, Yan; Azaïs, Thierry; Robin, Marc
  • Nature Materials, Vol. 11, Issue 8
  • DOI: 10.1038/nmat3362

Stable Prenucleation Calcium Carbonate Clusters
journal, December 2008


Nacre Protein Sequence Compartmentalizes Mineral Polymorphs in Solution
journal, March 2014

  • Seto, Jong; Picker, Andreas; Chen, Yong
  • Crystal Growth & Design, Vol. 14, Issue 4
  • DOI: 10.1021/cg401421h

Amorphous calcium carbonate particles form coral skeletons
journal, August 2017

  • Mass, Tali; Giuffre, Anthony J.; Sun, Chang-Yu
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
  • DOI: 10.1073/pnas.1707890114

Nucleation precursors in protein crystallization
journal, February 2014

  • Vekilov, Peter G.; Vorontsova, Maria A.
  • Acta Crystallographica Section F Structural Biology Communications, Vol. 70, Issue 3
  • DOI: 10.1107/S2053230X14002386

Fluid-solid transitions on walls in binary hard-sphere mixtures
journal, November 1997


Nature’s hierarchical materials
journal, November 2007


Do protein crystals nucleate within dense liquid clusters?
journal, June 2015

  • Maes, Dominique; Vorontsova, Maria A.; Potenza, Marco A. C.
  • Acta Crystallographica Section F Structural Biology Communications, Vol. 71, Issue 7
  • DOI: 10.1107/S2053230X15008997

Crystallization in Patterns: A Bio-Inspired Approach
journal, August 2004


Direct observation of mineral–organic composite formation reveals occlusion mechanism
journal, January 2016

  • Rae Cho, Kang; Kim, Yi-Yeoun; Yang, Pengcheng
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10187

Biological Composites
journal, June 2010


Crystallization kinetics of colloidal model suspensions: recent achievements and new perspectives
journal, July 2014


Flat pearls from biofabrication of organized composites on inorganic substrates
journal, September 1994

  • Fritz, Monika; Belcher, Angela M.; Radmacher, Manfred
  • Nature, Vol. 371, Issue 6492
  • DOI: 10.1038/371049a0

Understanding the Formation Mechanism of Magnetic Mesocrystals with (Cryo-)Electron Microscopy
journal, August 2019


Structure-property relationships of a biological mesocrystal in the adult sea urchin spine
journal, February 2012

  • Seto, J.; Ma, Y.; Davis, S. A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 10
  • DOI: 10.1073/pnas.1109243109

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

Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays
journal, March 2010

  • Mahamid, J.; Aichmayer, B.; Shimoni, E.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 14
  • DOI: 10.1073/pnas.0914218107

Selective nucleation in porous media
journal, January 2013

  • Hedges, Lester O.; Whitelam, Stephen
  • Soft Matter, Vol. 9, Issue 41
  • DOI: 10.1039/c3sm51946e

Multiphase transformation and Ostwald’s rule of stages during crystallization of a metal phosphate
journal, November 2008

  • Chung, Sung-Yoon; Kim, Young-Min; Kim, Jin-Gyu
  • Nature Physics, Vol. 5, Issue 1
  • DOI: 10.1038/nphys1148

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

Size limits of self-assembled colloidal structures made using specific interactions
journal, October 2014

  • Zeravcic, Zorana; Manoharan, Vinothan N.; Brenner, Michael P.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 45
  • DOI: 10.1073/pnas.1411765111

Direct Measurements of Island Growth and Step-Edge Barriers in Colloidal Epitaxy
journal, January 2010


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.