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Investigating materials formation with liquid-phase and cryogenic TEM

Abstract

The recent advent of liquid-phase transmission electron microscopy (TEM) and advances in cryogenic TEM are transforming our understanding of the physical and chemical mechanisms underlying the formation of materials in synthetic, biological and geochemical systems. These techniques have been applied to study the dynamic processes of nucleation, self-assembly, crystal growth and coarsening for metallic and semiconductor nanoparticles, (bio)minerals, electrochemical systems, macromolecular complexes, and organic and inorganic self-assembling systems. New instrumentation and methodologies that are currently on the horizon promise new opportunities for advancing the science of materials synthesis.

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Figure 1: Different LP-TEM cell designs that isolate the sample from the vacuum.
Figure 2: Examples of LP-TEM used to investigate the dynamics of materials formation processes.
Figure 3: Cryo-TEM captures snapshots of materials evolution through rapid freezing of the sample.
Figure 4: Cryo-TEM can be used to investigate materials formation in various specimens.
Figure 5: Cryo-TEM time series showing nucleation and growth.
Figure 6: LP-TEM investigations of nucleation, transformation and faceting.
Figure 7: Growth of crystals via nanoparticle interaction and assembly.
Figure 8: Organization of soft matter.
Figure 9: Nucleation and growth in biomimetic environments.

References

  1. 1

    Wang, C. M., Liao, H. G. & Ross, F. M. Observation of materials processes in liquids by electron microscopy. MRS Bull. 40, 46–52 (2015).

    Article  Google Scholar 

  2. 2

    Nielsen, M. H., Aloni, S. & De Yoreo, J. J. In situ TEM imaging of CaCO3 nucleation reveals coexistence of direct and indirect pathways. Science 345, 1158–1162 (2014). A mixing cell is used for the first time in LP-TEM to observe pathways of CaCO3 nucleation over a wide range of supersaturations, revealing that multiple pathways are simultaneously operative, including formation both directly from solution and indirectly through transformation of amorphous and crystalline precursors.

    Article  CAS  Google Scholar 

  3. 3

    Smeets, P. J. M., Cho, K. R., Kempen, R. G. E., Sommerdijk, N. A. J. M. & De Yoreo, J. J. Calcium carbonate nucleation driven by ion binding in a biomimetic matrix revealed by in situ electron microscopy. Nat. Mater. 14, 394–399 (2015). First paper in which LP-TEM is used to study a process related to biomineralization. The kinetic data revealed a so far unobserved mechanism of phase selection.

    Article  CAS  Google Scholar 

  4. 4

    den Heijer, M., Shao, I., Radisic, A., Reuter, M. C. & Ross, F. M. Patterned electrochemical deposition of copper using an electron beam. APL Mater. 2, 022101 (2014).

    Article  CAS  Google Scholar 

  5. 5

    Radisic, A., Vereecken, P. M., Hannon, J. B., Searson, P. C. & Ross, F. M. Quantifying electrochemical nucleation and growth of nanoscale clusters using real-time kinetic data. Nano Lett. 6, 238–242 (2006).

    Article  CAS  Google Scholar 

  6. 6

    Williamson, M. J., Tromp, R. M., Vereecken, P. M., Hull, R. & Ross, F. M. Dynamic microscopy of nanoscale cluster growth at the solid–liquid interface. Nat. Mater. 2, 532–536 (2003). This pioneering study reports the first use of LP-TEM using a microfabricated fluid cell, here used to observe electrochemically driven nucleation and growth of copper nanoclusters from aqueous solution.

    Article  CAS  Google Scholar 

  7. 7

    Chen, X. et al. Effects associated with nanostructure fabrication using in situ liquid cell TEM technology. Nano-Micro Lett. 7, 385–391 (2015).

    Article  CAS  Google Scholar 

  8. 8

    Van de Put, M. W. P. et al. Writing silica structures in liquid with scanning transmission electron microscopy. Small 11, 585–590 (2015).

    Article  CAS  Google Scholar 

  9. 9

    Xin, H. L. L. & Zheng, H. M. In situ observation of oscillatory growth of bismuth nanoparticles. Nano Lett. 12, 1470–1474 (2012).

    Article  CAS  Google Scholar 

  10. 10

    Ross, F. M. Opportunities and challenges in liquid cell electron microscopy. Science 350, http://dx.doi.org/10.1126/science.aaa9886 (2015).

  11. 11

    Nielsen, M. H., Lee, J. R. I., Hu, Q. N., Han, T. Y. J. & De Yoreo, J. J. Structural evolution, formation pathways and energetic controls during template-directed nucleation of CaCO3 . Faraday Discuss. 159, 105–121 (2012).

    Article  CAS  Google Scholar 

  12. 12

    Yuk, J. M. et al. High-resolution EM of colloidal nanocrystal growth using graphene liquid cells. Science 336, 61–64 (2012). Graphene liquid cells are introduced to LP-TEM for the first time, enabling atomic resolution of platinum nanocrystals undergoing site-selective coalescence, structural reshaping after coalescence and surface faceting.

    Article  CAS  Google Scholar 

  13. 13

    Nielsen, M. H. et al. Investigating processes of nanocrystal formation and transformation via liquid cell TEM. Microsc. Microanal. 20, 425–436 (2014).

    Article  CAS  Google Scholar 

  14. 14

    de Jonge, N. & Ross, F. M. Electron microscopy of specimens in liquid. Nat. Nanotechnol 6, 695–704 (2011).

    Article  CAS  Google Scholar 

  15. 15

    Jungjohann, K. L., Bliznakov, S., Sutter, P. W., Stach, E. A. & Sutter, E. A. In situ liquid cell electron microscopy of the solution growth of Au–Pd core–shell nanostructures. Nano Lett. 13, 2964–2970 (2013).

    Article  CAS  Google Scholar 

  16. 16

    Patterson, J. P. et al. Observing the growth of metal–organic frameworks by in situ liquid cell transmission electron microscopy. J. Am. Chem. Soc. 137, 7322–7328 (2015).

    Article  CAS  Google Scholar 

  17. 17

    Holtz, M. E., Yu, Y. C., Gao, J., Abruna, H. D. & Muller, D. A. In situ electron energy-loss spectroscopy in liquids. Microsc. Microanal. 19, 1027–1035 (2013).

    Article  CAS  Google Scholar 

  18. 18

    Sutter, E. et al. In situ liquid-cell electron microscopy of silver–palladium galvanic replacement reactions on silver nanoparticles. Nat. Commun. 5, 4946 (2014).

    Article  CAS  Google Scholar 

  19. 19

    Zaluzec, N. J., Burke, M. G., Haigh, S. J. & Kulzick, M. A. X-ray energy-dispersive spectrometry during in situ liquid cell studies using an analytical electron microscope. Microsc. Microanal. 20, 323–329 (2014).

    Article  CAS  Google Scholar 

  20. 20

    Schneider, N. M. et al. Electron–water interactions and implications for liquid cell electron microscopy. J. Phys. Chem. C 118, 22373–22382 (2014).

    Article  CAS  Google Scholar 

  21. 21

    Woehl, T. J., Evans, J. E., Arslan, L., Ristenpart, W. D. & Browning, N. D. Direct in situ determination of the mechanisms controlling nanoparticle nucleation and growth. ACS Nano 6, 8599–8610 (2012).

    Article  CAS  Google Scholar 

  22. 22

    Abellan, P. et al. Factors influencing quantitative liquid (scanning) transmission electron microscopy. Chem. Commun. 50, 4873–4880 (2014).

    Article  CAS  Google Scholar 

  23. 23

    Park, J. H. et al. Control of electron beam-induced Au nanocrystal growth kinetics through solution chemistry. Nano Lett. 15, 5314–5320 (2015).

    Article  CAS  Google Scholar 

  24. 24

    Woehl, T. J. et al. Experimental procedures to mitigate electron beam induced artifacts during in situ fluid imaging of nanomaterials. Ultramicroscopy 127, 53–63 (2013).

    Article  CAS  Google Scholar 

  25. 25

    Friedrich, H., Frederik, P. M., de With, G. & Sommerdijk, N. Imaging of self-assembled structures: interpretation of TEM and cryo-TEM images. Angew. Chem. Int. Ed. Engl. 49, 7850–7858 (2010).

    Article  CAS  Google Scholar 

  26. 26

    Nudelman, F., de With, G. & Sommerdijk, N. A. J. M. Cryo-electron tomography: 3-dimensional imaging of soft matter. Soft Matter 7, 17–24 (2011).

    Article  CAS  Google Scholar 

  27. 27

    Bellare, J. R., Davis, H. T., Scriven, L. E. & Talmon, Y. Controlled environment vitrification system: an improved sample preparation technique. J. Electron Microsc. Tech. 10, 87–111 (1988).

    Article  CAS  Google Scholar 

  28. 28

    Wirix, M. J. M., Bomans, P. H. H., Friedrich, H., Sommerdijk, N. A. J. M. & de With, G. Three-dimensional structure of P3HT assemblies in organic solvents revealed by cryo-TEM. Nano Lett. 14, 2033–2038 (2014).

    Article  CAS  Google Scholar 

  29. 29

    Reznikov, N. et al. A materials science vision of extracellular matrix mineralization. Nat. Rev. Mater. 1, 16041 (2016).

    Article  CAS  Google Scholar 

  30. 30

    Vos, M. R. J. et al. Insights in the organization of DNA-surfactant monolayers using cryo-electron tomography. J. Am. Chem. Soc. 129, 11894–11895 (2007).

    Article  CAS  Google Scholar 

  31. 31

    Dankers, P. Y. W. et al. Hierarchical formation of supramolecular transient networks in water: a modular injectable delivery system. Adv. Mater. 24, 2703–2709 (2012).

    Article  CAS  Google Scholar 

  32. 32

    Pichon, B. P., Bomans, P. H. H., Frederik, P. M. & Sommerdijk, N. A quasi-time-resolved CryoTEM study of the nucleation of CaCO3 under langmuir monolayers. J. Am. Chem. Soc. 130, 4034–4040 (2008).

    Article  CAS  Google Scholar 

  33. 33

    Tidhar, Y., Weissman, H., Tworowski, D. & Rybtchinski, B. Mechanism of crystalline self-assembly in aqueous medium: a combined cryo-TEM/kinetic study. Chemistry 20, 10332–10342 (2014).

    Article  CAS  Google Scholar 

  34. 34

    Cenker, C. C. et al. Peptide nanotube formation: a crystal growth process. Soft Matter 8, 7463–7470 (2012).

    Article  CAS  Google Scholar 

  35. 35

    Frindt, N. et al. In-focus electrostatic Zach phase plate imaging for transmission electron microscopy with tunable phase contrast of frozen hydrated biological samples. Microsc. Microanal. 20, 175–183 (2014).

    Article  CAS  Google Scholar 

  36. 36

    Migunov, V. et al. Rapid low dose electron tomography using a direct electron detection camera. Sci. Rep. 5, 14516 (2015).

    Article  CAS  Google Scholar 

  37. 37

    Bartesaghi, A. et al. 2.2 angstrom resolution cryo-EM structure of β-galactosidase in complex with a cell-permeant inhibitor. Science 348, 1147–1151 (2015).

    Article  CAS  Google Scholar 

  38. 38

    Gibbs, J. W. & Smith, A. W. in Transactions of the Connecticut Academy of Arts and Sciences Vol. 3 Ch. 5,9 108–248; 343–524 (Tuttle, 1874).

    Google Scholar 

  39. 39

    Kuhs, M., Zeglinski, J. & Rasmuson, A. C. Influence of history of solution in crystal nucleation of fenoxycarb: kinetics and mechanisms. Cryst. Growth Des. 14, 905–915 (2014).

    Article  CAS  Google Scholar 

  40. 40

    Bots, P., Benning, L. G., Rodriguez-Blanco, J. D., Roncal-Herrero, T. & Shaw, S. Mechanistic insights into the crystallization of amorphous calcium carbonate (ACC). Cryst. Growth Des. 12, 3806–3814 (2012).

    Article  CAS  Google Scholar 

  41. 41

    Habraken, W. J. E. M. et al. Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate. Nat Commun. 4, 1507 (2013). 2D and 3D cryo-TEM are used to unveil the multistep nucleation and transformation process underlying the biomimetic formation of apatite, and show that the first step consists of the aggregation of pre-nucleation complexes of Ca(HPO4)34−.

    Article  CAS  Google Scholar 

  42. 42

    Gebauer, D., Volkel, A. & Colfen, H. Stable prenucleation calcium carbonate clusters. Science 322, 1819–1822 (2008).

    Article  CAS  Google Scholar 

  43. 43

    Carcouet, C. C. M. C. et al. Nucleation and growth of monodisperse silica nanoparticles. Nano Lett. 14, 1433–1438 (2014).

    Article  CAS  Google Scholar 

  44. 44

    Stober, W., Fink, A. & Bohn, E. Controlled growth of monodisperse silica spheres in micron size range. J. Colloid Interface Sci. 26, 62–69 (1968).

    Article  Google Scholar 

  45. 45

    Davis, T. M. et al. Mechanistic principles of nanoparticle evolution to zeolite crystals. Nat. Mater. 5, 400–408 (2006).

    Article  CAS  Google Scholar 

  46. 46

    Kumar, S., Wang, Z., Penn, R. L. & Tsapatsis, M. A. Structural resolution cryo-TEM study of the early stages of MFI growth. J. Am. Chem. Soc. 130, 17284–17286 (2008).

    Article  CAS  Google Scholar 

  47. 47

    Nudelman, F., Sonmezler, E., Bomans, P. H. H., de With, G. & Sommerdijk, N. A. J. M. Stabilization of amorphous calcium carbonate by controlling its particle size. Nanoscale 2, 2436–2439 (2010).

    Article  CAS  Google Scholar 

  48. 48

    Pouget, E. M. et al. The development of morphology and structure in hexagonal vaterite. J. Am. Chem. Soc. 132, 11560–11565 (2010). 2D and 3D Cryo-TEM are combined with electron diffraction and dark-field imaging to show that the amorphous-to-crystal transition in a single nanoparticle is a solid-state process.

    Article  CAS  Google Scholar 

  49. 49

    Nijhuis, A. W. G. et al. Enzymatic pH control for biomimetic deposition of calcium phosphate coatings. Acta Biomater. 10, 931–939 (2014).

    Article  CAS  Google Scholar 

  50. 50

    Saha, A. et al. New insights into the transformation of calcium sulfate hemihydrate to gypsum using time-resolved cryogenic transmission electron microscopy. Langmuir 28, 11182–11187 (2012).

    Article  CAS  Google Scholar 

  51. 51

    Lenders, J. J. M. et al. A bioinspired coprecipitation method for the controlled synthesis of magnetite nanoparticles. Cryst. Growth Des. 14, 5561–5568 (2014).

    Article  CAS  Google Scholar 

  52. 52

    Altan, C. L. et al. Partial oxidation as a rational approach to kinetic control in bioinspired magnetite synthesis. Chemistry 21, 6150–6156 (2015).

    Article  CAS  Google Scholar 

  53. 53

    Dey, A., Lenders, J. J. M. & Sommerdijk, N. A. J. M. Bioinspired magnetite formation from a disordered ferrihydrite-derived precursor. Faraday Discuss. 179, 215–225 (2015).

    Article  CAS  Google Scholar 

  54. 54

    Alloyeau, D. et al. Unravelling kinetic and thermodynamic effects on the growth of gold nanoplates by liquid transmission electron microscopy. Nano Lett. 15, 2574–2581 (2015).

    Article  CAS  Google Scholar 

  55. 55

    Evans, J. E., Jungjohann, K. L., Browning, N. D. & Arslan, I. Controlled growth of nanoparticles from solution with in situ liquid transmission electron microscopy. Nano Lett. 11, 2809–2813 (2011).

    Article  CAS  Google Scholar 

  56. 56

    Grogan, J. M., Rotkina, L. & Bau, H. H. In situ liquid–cell electron microscopy of colloid aggregation and growth dynamics. Phys. Rev. E 83, 061405 (2011).

    Article  CAS  Google Scholar 

  57. 57

    Liao, H. G. et al. TEM study of fivefold twined gold nanocrystal formation mechanism. Mater. Lett. 116, 299–303 (2014).

    Article  CAS  Google Scholar 

  58. 58

    Liao, H. G. & Zheng, H. M. Liquid cell transmission electron microscopy study of platinum iron nanocrystal growth and shape evolution. J. Am. Chem. Soc. 135, 5038–5043 (2013).

    Article  CAS  Google Scholar 

  59. 59

    Liao, H. G. et al. Facet development during platinum nanocube growth. Science 345, 916–919 (2014). The development of nanocrystal facets during the earliest stages of platinum nanoparticle growth are followed at high spatial and temporal resolution by LP-TEM, revealing distinct atomic pathways of cluster attachment, step growth and 2D nucleation, and providing a rationale for the evolution of particle shape.

    Article  CAS  Google Scholar 

  60. 60

    Liu, Y., Tai, K. P. & Dillon, S. J. Growth kinetics and morphological evolution of ZnO precipitated from solution. Chem. Mater. 25, 2927–2933 (2013).

    Article  CAS  Google Scholar 

  61. 61

    Niu, K. Y., Park, J., Zheng, H. M. & Aivisatos, A. P. Revealing bismuth oxide hollow nanoparticle formation by the kirkendall effect. Nano Lett. 13, 5715–5719 (2013).

    Article  CAS  Google Scholar 

  62. 62

    Radisic, A., Ross, F. M. & Searson, P. C. In situ study of the growth kinetics of individual island electrodeposition of copper. J. Phys. Chem. B 110, 7862–7868 (2006).

    Article  CAS  Google Scholar 

  63. 63

    Verch, A., Morrison, I. E. G., van de Locht, R. & Kroger, R. In situ electron microscopy studies of calcium carbonate precipitation from aqueous solution with and without organic additives. J. Struct. Biol. 183, 270–277 (2013).

    Article  CAS  Google Scholar 

  64. 64

    Woehl, T. J. et al. Direct observation of aggregative nanoparticle growth: kinetic modeling of the size distribution and growth rate. Nano Lett. 14, 373–378 (2014).

    Article  CAS  Google Scholar 

  65. 65

    Zheng, H. M. et al. Observation of single colloidal platinum nanocrystal growth trajectories. Science 324, 1309–1312 (2009).

    Article  CAS  Google Scholar 

  66. 66

    Kraus, T. & de Jonge, N. Dendritic gold nanowire growth observed in liquid with transmission electron microscopy. Langmuir 29, 8427–8432 (2013).

    Article  CAS  Google Scholar 

  67. 67

    Sun, M. H., Liao, H. G., Niu, K. Y. & Zheng, H. M. Structural and morphological evolution of lead dendrites during electrochemical migration. Sci. Rep. 3, 3227 (2013).

    Article  Google Scholar 

  68. 68

    White, E. R. et al. In situ transmission electron microscopy of lead dendrites and lead ions in aqueous solution. ACS Nano 6, 6308–6317 (2012).

    Article  CAS  Google Scholar 

  69. 69

    Zhu, G. M. et al. In situ study of the growth of two-dimensional palladium dendritic nanostructures using liquid-cell electron microscopy. Chem. Commun. 50, 9447–9450 (2014).

    Article  CAS  Google Scholar 

  70. 70

    Noh, K. W., Liu, Y., Sun, L. & Dillon, S. J. Challenges associated with in situ TEM in environmental systems: the case of silver in aqueous solutions. Ultramicroscopy 116, 34–38 (2012).

    Article  CAS  Google Scholar 

  71. 71

    Rieger, J. et al. Precursor structures in the crystallization/precipitation processes of CaCO3 and control of particle formation by polyelectrolytes. Faraday Discuss. 136, 265–277 (2007).

    Article  CAS  Google Scholar 

  72. 72

    De Yoreo, J. J. et al. CRYSTAL GROWTH. Crystallization by particle attachment in synthetic, biogenic, and geologic environments. Science 349, aaa6760 (2015).

    Article  CAS  Google Scholar 

  73. 73

    Penn, R. L. & Banfield, J. F. Imperfect oriented attachment: dislocation generation in defect-free nanocrystals. Science 281, 969–971 (1998).

    Article  CAS  Google Scholar 

  74. 74

    Oaki, Y. & Imai, H. The hierarchical architecture of nacre and its mimetic material. Angew. Chem. Int. Ed. Engl. 44, 6571–6575 (2005).

    Article  CAS  Google Scholar 

  75. 75

    Penn, R. L. & Banfield, J. F. Oriented attachment and growth, twinning, polytypism, and formation of metastable phases: insights from nanocrystalline TiO2 . Am. Miner. 83, 1077–1082 (1998).

    Article  CAS  Google Scholar 

  76. 76

    Ivanov, V. K., Fedorov, P. P., Baranchikov, A. Y. & Osiko, V. V. Oriented attachment of particles: 100 years of investigations of non-classical crystal growth. Russ. Chem. Rev. 83, 1204–1222 (2014).

    Article  CAS  Google Scholar 

  77. 77

    Zhang, H. Z. & Banfield, J. F. Energy calculations predict nanoparticle attachment orientations and asymmetric crystal formation. J. Phys. Chem. Lett. 3, 2882–2886 (2012).

    Article  CAS  Google Scholar 

  78. 78

    Judat, B. & Kind, M. Morphology and internal structure of barium sulfate: derivation of a new growth mechanism. J. Colloid Interface Sci. 269, 341–353 (2004).

    Article  CAS  Google Scholar 

  79. 79

    Yuwono, V. M., Burrows, N. D., Soltis, J. A. & Penn, R. L. Oriented aggregation: formation and transformation of mesocrystal intermediates revealed. J. Am. Chem. Soc. 132, 2163–2165 (2010).

    Article  CAS  Google Scholar 

  80. 80

    Baumgartner, J. et al. Nucleation and growth of magnetite from solution. Nat. Mater. 12, 310–314 (2013).

    Article  CAS  Google Scholar 

  81. 81

    Frandsen, C. et al. Aggregation-induced growth and transformation of β-FeOOH nanorods to micron-sized α-Fe2O3 spindles. CrystEngComm 16, 1451–1458 (2014).

    Article  CAS  Google Scholar 

  82. 82

    Legg, B. A., Zhu, M., Comolli, L. R., Gilbert, B. & Banfield, J. F. Determination of the three-dimensional structure of ferrihydrite nanoparticle aggregates. Langmuir 30, 9931–9940 (2014).

    Article  CAS  Google Scholar 

  83. 83

    Li, D. S. et al. Direction-specific interactions control crystal growth by oriented attachment. Science 336, 1014–1018 (2012). LP-TEM data is used to follow the crystallographic orientations of iron oxyhydroxide particles undergoing oriented attachment events, to estimate forces driving oriented attachment, and to show that oriented attachment and classical ion-by-ion growth proceed concurrently.

    Article  CAS  Google Scholar 

  84. 84

    De Yoreo, J. J. & Vekilov, P. G. in Biomineralization Vol. 54 (eds Dove, P. M., DeYoreo, J. J., & Weiner, S. ) 57–93 (Mineralogical Society of America, 2003).

    Book  Google Scholar 

  85. 85

    Liao, H. G., Cui, L. K., Whitelam, S. & Zheng, H. M. Real-time imaging of Pt3 Fe nanorod growth in solution. Science 336, 1011–1014 (2012).

    Article  CAS  Google Scholar 

  86. 86

    Liu, Y. Z., Lin, X. M., Sun, Y. G. & Rajh, T. In situ visualization of self-assembly of charged gold nanoparticles. J. Am. Chem. Soc. 135, 3764–3767 (2013).

    Article  CAS  Google Scholar 

  87. 87

    Chen, Q. C. et al. Interaction potentials of anisotropic nanocrystals from the trajectory sampling of particle motion using in situ liquid phase transmission electron microscopy. ACS Cent. Sci. 1, 33–39 (2015).

    Article  CAS  Google Scholar 

  88. 88

    Welch, D. A. et al. Understanding the role of solvation forces on the preferential attachment of nanoparticles in liquid. ACS Nano 10, 181–187 (2016).

    Article  CAS  Google Scholar 

  89. 89

    Anand, U. et al. Hydration layer-mediated pairwise interaction of nanoparticles. Nano Lett. 16, 786–790 (2016).

    Article  CAS  Google Scholar 

  90. 90

    Whitesides, G. M., Mathias, J. P. & Seto, C. T. Molecular self-assembly and nanochemistry: a chemical strategy for the synthesis of nanostructures. Science 254, 1312–1319 (1991).

    Article  CAS  Google Scholar 

  91. 91

    Albertazzi, L. et al. Probing exchange pathways in one-dimensional aggregates with super-resolution microscopy. Science 344, 491–495 (2014).

    Article  CAS  Google Scholar 

  92. 92

    Chung, S., Shin, S. H., Bertozzi, C. R. & De Yoreo, J. J. Self-catalyzed growth of S layers via an amorphous-to-crystalline transition limited by folding kinetics. Proc. Natl Acad. Sci. USA 107, 16536–16541 (2010).

    Article  Google Scholar 

  93. 93

    Cisneros, D. A., Hung, C., Franz, C. A. & Muller, D. J. Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy. J. Struct. Biol. 154, 232–245 (2006).

    Article  CAS  Google Scholar 

  94. 94

    Cui, H. et al. Elucidating the assembled structure of amphiphiles in solution via cryogenic transmission electron microscopy. Soft Matter 3, 945–955 (2007).

    Article  CAS  Google Scholar 

  95. 95

    Weissman, H. & Rybtchinski, B. Noncovalent self-assembly in aqueous medium: mechanistic insights from time-resolved cryogenic electron microscopy. Curr. Opin. Colloid Interface Sci. 17, 330–342 (2012).

    Article  CAS  Google Scholar 

  96. 96

    McKenzie, B. E., Holder, S. J. & Sommerdijk, N. Assessing internal structure of polymer assemblies from 2D to 3D cryoTEM: bicontinuous micelles. Curr. Opin. Colloid Interface Sci. 17, 343–349 (2012).

    Article  CAS  Google Scholar 

  97. 97

    Berlepsch, H. V., Ludwig, K., Schade, B., Haag, R. & Boettcher, C. Progress in the direct structural characterization of fibrous amphiphilic supramolecular assemblies in solution by transmission electron microscopic techniques. Adv. Colloid Interface Sci. 208, 279–292 (2014).

    Article  CAS  Google Scholar 

  98. 98

    Parry, A. L., Bomans, P. H. H., Holder, S. J., Sommerdijk, N. & Biagini, S. C. G. Cryo electron tomography reveals confined complex morphologies of tripeptide-containing amphiphilic double-comb diblock copolymers. Angew. Chem. Int. Ed. Engl. 47, 8859–8862 (2008). For the first time cryo-ET is used to reveal the complex 3D internal structure of block copolymer aggregates.

    Article  CAS  Google Scholar 

  99. 99

    Loebling, T. I. et al. Hidden structural features of multicompartment micelles revealed by cryogenic transmission electron tomography. ACS Nano 8, 11330–11340 (2014).

    Article  CAS  Google Scholar 

  100. 100

    Comolli, L. R. et al. Conformational transitions at an S-Layer growing boundary resolved by cryo-TEM. Angew. Chem. Int. Ed. Engl. 52, 4829–4832 (2013).

    Article  CAS  Google Scholar 

  101. 101

    de Jonge, N., Dukes, M. J., Ring, E. A. & Peckys, D. B. Scanning transmission electron microscopy of eukaryotic cells in liquid. Biophys. J. 100, 323–323 (2011).

    Article  Google Scholar 

  102. 102

    de Jonge, N., Peckys, D. B., Kremers, G. J. & Piston, D. W. Electron microscopy of whole cells in liquid with nanometer resolution. Proc. Natl Acad. Sci. USA 106, 2159–2164 (2009).

    Article  Google Scholar 

  103. 103

    Peckys, D. B., Veith, G. M., Joy, D. C. & de Jonge, N. Nanoscale imaging of whole cells using a liquid enclosure and a scanning transmission electron microscope. PLoS ONE 4, e8214 (2009).

    Article  CAS  Google Scholar 

  104. 104

    Gilmore, B. L. et al. Visualizing viral assemblies in a nanoscale biosphere. Lab Chip 13, 216–219 (2013).

    Article  CAS  Google Scholar 

  105. 105

    Evans, J. E. et al. Visualizing macromolecular complexes with in situ liquid scanning transmission electron microscopy. Micron 43, 1085–1090 (2012).

    Article  CAS  Google Scholar 

  106. 106

    Liu, L. L., Liu, Y., Wu, W. J., Miller, C. M. & Dickey, E. C. Visualization of film-forming polymer particles with a liquid cell technique in a transmission electron microscope. Analyst 140, 6330–6334 (2015).

    Article  CAS  Google Scholar 

  107. 107

    Parent, L. R. et al. Direct in situ observation of nanoparticle synthesis in a liquid crystal surfactant template. ACS Nano 6, 3589–3596 (2012).

    Article  CAS  Google Scholar 

  108. 108

    Plamper, F. A. et al. Spontaneous assembly of miktoarm stars into vesicular interpolyelectrolyte complexes. Macromol. Rapid Commun. 34, 855–860 (2013).

    Article  CAS  Google Scholar 

  109. 109

    Proetto, M. T. et al. Dynamics of soft nanomaterials captured by transmission electron microscopy in liquid water. J. Am. Chem. Soc. 136, 1162–1165 (2014).

    Article  CAS  Google Scholar 

  110. 110

    Dey, A. de With, G. & Sommerdijk, N. A. J. M. In situ techniques in biomimetic mineralization studies of calcium carbonate. Chem. Soc. Rev. 39, 397–409 (2010).

    Article  CAS  Google Scholar 

  111. 111

    Pouget, E. M. et al. The initial stages of template-controlled CaCO3 formation revealed by cryo-TEM. Science 323, 1455–1458 (2009).

    Article  CAS  Google Scholar 

  112. 112

    Tester, C. C. et al. In vitro synthesis and stabilization of amorphous calcium carbonate (ACC) nanoparticles within liposomes. CrystEngComm 13, 3975–3978 (2011).

    Article  CAS  Google Scholar 

  113. 113

    Gower, L. B. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 108, 4551–4627 (2008).

    Article  CAS  Google Scholar 

  114. 114

    Cantaert, B. et al. Think positive: phase separation enables a positively charged additive to induce dramatic changes in calcium carbonate morphology. Adv. Funct. Mater. 22, 907–915 (2012).

    Article  CAS  Google Scholar 

  115. 115

    Nudelman, F. et al. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. 9, 1004–1009 (2010). 2D and 3D cryo-TEM is used in combination with electron diffraction and cryogenic energy-dispersive X-ray spectroscopy to unravel the mechanism of collagen mineralization.

    Article  CAS  Google Scholar 

  116. 116

    Dey, A. et al. The role of prenucleation clusters in surface-induced calcium phosphate crystallization. Nat. Mater. 9, 1010–1014 (2010).

    Article  CAS  Google Scholar 

  117. 117

    Wang, Y. et al. The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite. Nat. Mater. 11, 724–733 (2012).

    Article  CAS  Google Scholar 

  118. 118

    Lausch, A. J., Quan, B. D., Miklas, J. W. & Sone, E. D. Extracellular matrix control of collagen mineralization in vitro. Adv. Funct. Mater. 23, 4906–4912 (2013).

    Article  CAS  Google Scholar 

  119. 119

    Fang, P. A., Conway, J. F., Margolis, H. C., Simmer, J. P. & Beniash, E. Hierarchical self-assembly of amelogenin and the regulation of biomineralization at the nanoscale. Proc. Natl Acad. Sci. USA 108, 14097–14102 (2011).

    Article  Google Scholar 

  120. 120

    Krogstad, D. V., Wang, D. & Lin-Gibson, S. Kinetics of aggregation and crystallization of polyaspartic acid stabilized calcium phosphate particles at high concentrations. Biomacromolecules 16, 1550–1555 (2015).

    Article  CAS  Google Scholar 

  121. 121

    Kashyap, S., Woehl, T. J., Liu, X. P., Mallapragada, S. K. & Prozorov, T. Nucleation of iron oxide nanoparticles mediated by Mms6 protein in situ. ACS Nano 8, 9097–9106 (2014).

    Article  CAS  Google Scholar 

  122. 122

    Hamm, L. M. et al. Reconciling disparate views of template-directed nucleation through measurement of calcite nucleation kinetics and binding energies. Proc. Natl Acad. Sci. USA 111, 1304–1309 (2014).

    Article  CAS  Google Scholar 

  123. 123

    Browning, N. D. et al. Recent developments in dynamic transmission electron microscopy. Curr. Opin. Solid State Mater. Sci. 16, 23–30 (2012).

    Article  CAS  Google Scholar 

  124. 124

    Jungjohann, K. L., Evans, J. E., Aguiar, J. A., Arslan, I. & Browning, N. D. Atomic-scale imaging and spectroscopy for in situ liquid scanning transmission electron microscopy. Microsc. Microanal. 18, 621–627 (2012).

    Article  CAS  Google Scholar 

  125. 125

    Stevens, A., Yang, H., Carin, L., Arslan, I. & Browning, N. D. The potential for Bayesian compressive sensing to significantly reduce electron dose in high-resolution STEM images. Microscopy (Oxf). 63, 41–51 (2014).

    Article  Google Scholar 

  126. 126

    Stevens, A. et al. Applying compressive sensing to TEM video: a substantial frame rate increase on any camera. Adv. Struct. Chem. Imaging 1, 10 http://dx.doi.org/10.1186/s40679-015-0009-3 (2015).

    Article  Google Scholar 

  127. 127

    Park, J. et al. 3D structure of individual nanocrystals in solution by electron microscopy. Science 349, 290–295 (2015).

    Article  CAS  Google Scholar 

  128. 128

    Evans, J. E. & Browning, N. D. Enabling direct nanoscale observations of biological reactions with dynamic TEM. Microscopy (Oxf). 62, 147–156 (2013).

    Article  CAS  Google Scholar 

  129. 129

    van de Put, M. W. P. et al. Graphene oxide single sheets as substrates for high resolution cryoTEM. Soft Matter 11, 1265–1270 (2015).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by a VICI grant of the Dutch Science Foundation, NWO, The Netherlands, and the US Department of Energy, Office of Basic Energy Sciences, Division of Materials Science and Engineering at the Pacific Northwest National Laboratory (PNNL). PNNL is operated by Battelle for the US Department of Energy under Contract DE-AC05-76RL01830.

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Correspondence to J. J. De Yoreo or Sommerdijk N. A. J. M..

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De Yoreo, J., N. A. J. M., S. Investigating materials formation with liquid-phase and cryogenic TEM. Nat Rev Mater 1, 16035 (2016). https://doi.org/10.1038/natrevmats.2016.35

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