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Accessing crystal–crystal interaction forces with oriented nanocrystal atomic force microscopy probes

Nature Protocols volume 13, pages 2005–2030 (2018)Cite this article

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Abstract

Biominerals serve as critical structures of living systems and play important roles in biochemical processes. Understanding their crystallization mechanisms is therefore central to many areas of biology, biogeoscience, and biochemistry. Some biominerals, such as bone and dentin, are hierarchical nanocomposite structures constructed by sequential addition of individual oriented nanocrystals. The driving forces that enable this oriented assembly are still poorly understood, with advances in understanding limited in part by the availability of techniques that can precisely measure the delicate interactions between nanocrystals as a function of their separation distance and mutual orientation. Here, we provide a comprehensive protocol for (i) fabricating oriented single-nanocrystal atomic force microscopy (AFM) probes using focused ion beam (FIB) milling and (ii) performing oriented nanocrystal interaction force measurements using dynamic force spectroscopy (DFS)-based AFM and environmental transmission electron microscopy (ETEM)–AFM techniques. We illustrate how to fabricate oriented nanocrystal force probes using commercial bulk crystals or nano/microcrystals of calcite, zinc oxide, and rutile. The typical protocol for fabricating one AFM crystal probe takes 2–3 h. In addition, we illustrate how to quantify the direction-specific interaction forces for a given pair of interacting oriented nanocrystal faces. The methods are fully transferrable to other minerals of interest, such as the apatites constituting bone minerals. This allows researchers across many fields to measure and understand particle-based crystallization processes.

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Fig. 1: Schematic of crystal–crystal interaction force measurements with oriented nanocrystal AFM probes.
Fig. 2: EDX, SEM, AFM, and TEM images of a nanocrystal AFM tip.
Fig. 3: The crystal lattice orientation measurement.
Fig. 4: Schematic illustration of the ETEM–AFM setup.
Fig. 5: An ETEM–AFM force–distance sequence with corresponding TEM images.
Fig. 6: Procedure for FIB-cutting a commercial AFM tip.
Fig. 7: Procedure for FIB-cutting the microslab in a commercial ZnO (0001) crystal substrate.
Fig. 8: Procedure for lift-out of the microslab.
Fig. 9: Procedure for transferring and aligning the nanocrystal on the AFM probe.
Fig. 10: Procedure for using FIB milling to sharpen the nanocrystal to the desired surface area exposure.
Fig. 11: Direction-specific interaction forces at different azimuthal orientations for ZnO (0001)–ZnO (000\({\overline{1}}\)) using different loading rates.
Fig. 12: Direction-specific interaction forces at different azimuthal orientations for rutile (001) nanocrystals with different water vapor pressures.

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Acknowledgements

This protocol is based upon work supported by the U.S. Department of Energy (DOE), Office of Science, Office of Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division through its Geosciences Program at Pacific Northwest National Laboratory (PNNL). The Materials Synthesis and Simulation across Scales Initiative, a Laboratory Directed Research and Development Program at PNNL, supported the development of tip fabrication methods. We acknowledge fruitful discussions with J. Tao on the dynamic force measurements and calcite crystal growth. The work was performed using the Environmental and Molecular Sciences Laboratory (EMSL), a national scientific user facility at PNNL sponsored by the DOE’s Office of Biological and Environmental Research. PNNL is a multi-program national laboratory operated by Battelle Memorial Institute under contract no. DE-AC05-76RL01830 for the DOE.

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Author notes

  1. These authors contributed equally: Yang He, Jia Liu

Authors and Affiliations

  1. Physical and Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, USA

    Xin Zhang, James J. De Yoreo & Kevin M. Rosso

  2. Department of Mechanical Engineering and Materials Science, University of Pittsburgh, Pittsburgh, PA, USA

    Yang He & Scott X. Mao

  3. Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, USA

    Jia Liu, Mark E. Bowden, Libor Kovarik & Chongmin Wang

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  1. Xin Zhang
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Contributions

X.Z., J.J.D.Y., and K.M.R. conceived and designed the experiments. X.Z. and J.L. developed the crystal AFM tip fabrication method and fabricated all tips. Y.H., X.Z., C.W., and S.X.M. conducted the ETEM–AFM experiments and force data analysis. X.Z. conducted the AFM experiments and force data analysis. M.E.B. conducted the XRD analyses. L.K. developed the gas delivery system in the environmental TEM. X.Z., Y.H., and K.M.R. co-wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Xin Zhang or Kevin M. Rosso.

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Key references using this protocol

1. Zhang, X. et al. Science 356, 434–437 (2017): https://doi.org/10.1126/science.aah6902

2. Zhang, X. et al. Nat. Commun. 8, 835 (2017): https://doi.org/10.1038/s41467-017-00844-6

Integrated supplementary information

Supplementary Figure 1

AFM topographic images of the SrTO3 substrate used for polishing the nanocrystal AFM tips.

Supplementary Figure 2 Nanocrystal-nanocrystal interaction force measurements.

(a) Representative force curves for ZnO (0001)-ZnO (000) nanocrystal interaction in 0.2 mM Zn(NO3)2 solution. Point 1 to 2 presents the approach process until jump-to-contact (point 2 to 3); followed by a chosen amount of increasing applied force up the contact ramp from point 3 to 4; after a chosen dwell time to stabilize the interaction, tip retraction is performed (point 4 to 5) until jump-from-contact (point 5 to 6). (b) Data fitting using the multiple bond model developed by Friddle et al.25 for the different retraction rates at each azimuthal orientation between ZnO (0001)-ZnO (000) nanocrystals to obtain the equilibrium rupture forces from 0° to 60°. Error bars in b and c represent the standard error (n=25). Adapted with permission from Zhang et al.34 (original material licensed under a Creative Commons Attribution License 4.0).

Supplementary Figure 3 The original AFM tip-cutting strategy.

Schematics illustrating (a) an original AFM tip, (b) a FIB cut AFM tip without tilt angle correction, and (c) with tilt angle correction; (d) and (e) SEM images of the AFM tip glued on a stage with 11° tilt for adjusting the AFM tip surface to the horizontal plane during tip fabrication. Adapted with permission from Zhang et al.34 (original material licensed under a Creative Commons Attribution License 4.0).

Supplementary Figure 4 Procedure for fabricating oriented nanoscale ZnO (0001) AFM tips using ZnO nanowire on substrate.

(a) Binding a ZnO NW onto the Omniprobe (scale bar 5 µm) (Step 4-5 of Box 1); (b) FIB milled hole in pre-milled AFM tip (scale bar 5 µm) (Step 7-8 of Box 1); (c) ZnO NW secured by Pt on the AFM tip (scale bar 5 µm) (Step 9-14 of Box 1); (d) The ZnO (0001) AFM tip after FIB sharpening (scale bar 0.5 µm) (Step 15-19 of Box 1); (e) The ZnO (0001) AFM tip after high-speed polishing using AFM (scale bar 0.5 µm) (Step 20 of Box 1). Adapted with permission from Zhang et al.34 (original material licensed under a Creative Commons Attribution License 4.0).

Supplementary Figure 5 Procedure for fabricating an oriented face-specific rutile (001) AFM tip with an atomically flat surface.

(a) FIB cut a small piece of rutile (001) crystal with Ag and Pt protective layers followed by lift-off using the Omniprobe (Step 5 of Box 2); (b) Make a groove in the original AFM tip (Step 3 of Box 2); (c) Transfer the rutile (001) microcrystal from Omniprobe to the AFM tip and then stabilize it using Pt glue (Step 6 of Box 2); (d) FIB milling (30 KV) the rutile (001) microcrystal to a cylindrical shape (Step 7 of Box 2); (e) Further FIB milling (30 KV) the rutile (001) microcrystal to a needle-like shape and then remove the Pt protective layer using a lower milling voltage (2 KV) (Step 8-9 of Box 2); (f) Remove the Ag protective layer after FIB milling using the 0.5 M iron nitrate etching solution (Step 11 of Box 2). Adapted with permission from ref. 33, American Association for the Advancement of Science.

Supplementary Figure 6

The AFM tip holder was made using the Hastelloy C-276 material.

Supplementary Figure 7 Procedure for fabricating an oriented face-specific calcite (104) AFM tip.

(a) Calcite (104) crystal on silicon substrate (Step 1 of Box 4); (b) FIB cut a calcite microslab (Step 4-5 of Box 4); (c) lift-out the calcite microslab (Step 4-5 of Box 4) (d) transfer the calcite microslab on the AFM tip (Step 6 of Box 4); (e) cut a small size calcite crystal in the AFM tip (Step 6 of Box 4); (f) FIB milling the calcite crystal to the target size (Step 7-8 of Box 4).

Supplementary Figure 8 Procedure for fabricating an oriented face-specific rutile (001) nanocrystal needle with an atomically flat surface.

(a) original gold needle; (b) FIB cut the needle with a flat surface ~ 4 µm in diameter (Step 3 of Box 3); (c) Transfer the rutile (001) microcrystal from Omniprobe to the gold needle and then stabilize it using Pt glue (Step 4-5 of Box 3); (d) FIB milling (30 KV, 93 pA) the rutile (001) microcrystal to a cylindrical shape with a diameter ~1.0 µm and a height ~1.0 µm (Step 5 of Box 3); (e) Further FIB milling (30 KV, 28 pA) the rutile (001) microcrystal to a cylindrical shape and then remove the Pt protective layer using a lower milling voltage (2 KV) (Step 6 of Box 3); (f) Remove the Ag protective layer after FIB milling using the 0.5 M iron nitrate etching solution (Step 8-9 of Box 3). f adapted with permission from ref. 33, American Association for the Advancement of Science.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8, Supplementary Methods

Reporting Summary

Supplementary Video 1

Jump-to-contact process. Real-time movie to showing the jump-to-contact happen when the rutile (001) substrate on the gold needle is driven close to the rutile (001) nanocrystal on the AFM tip. The azimuthal angle is 26.83° and the water vapor pressure is 10-1 mbar. Adapted with permission from ref. 33, American Association for the Advancement of Science

Supplementary Video 2

Jump-from-contact process in water vapors. Real-time movie showing the rutile (001) AFM tip remains attractively bound in contact with the substrate during retraction until the elastic force of the AFM cantilever exceeds the attractive force and the deflection returns to its starting value, as noted by the red line, at long-range. The azimuthal angle is 1.63° and the water pressure is 10-3 mbar

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Zhang, X., He, Y., Liu, J. et al. Accessing crystal–crystal interaction forces with oriented nanocrystal atomic force microscopy probes. Nat Protoc 13, 2005–2030 (2018). https://doi.org/10.1038/s41596-018-0027-4

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