Long-Range Hierarchical Nanocrystal Assembly Driven by Molecular

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Long-range hierarchical nanocrystal assembly driven by molecular structural transformation Enbo Zhu, Shiyi Wang, Xucheng Yan, Masoud Sobani, Lingyan Ruan, Chen Wang, Yuan Liu, Xiangfeng Duan, Hendrik Heinz, and Yu Huang J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.8b08023 • Publication Date (Web): 26 Nov 2018 Downloaded from http://pubs.acs.org on November 27, 2018

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Journal of the American Chemical Society

Long-Range Hierarchical Nanocrystal Assembly Driven by Molecular Structural Transformation Enbo Zhu,†,⊥ Shiyi Wang,‡, ⊥ Xucheng Yan,† Masoud Sobani,# Lingyan Ruan,† Chen Wang,† Yuan Liu,† Xiangfeng Duan,∥, § Hendrik Heinz*,‡ and Yu Huang*,†,§ †Department

of Materials Science and Engineering, ∥Department of Chemistry and Biochemistry, §California NanoSystems Institute, University of California, Los Angeles, CA 90095, USA. ‡Department

of Chemical and Biological Engineering, University of Colorado Boulder, Boulder, CO 80309, USA.

#Department

of Polymer Engineering, University of Akron, Akron, Ohio 45433, USA.

ABSTRACT: The hierarchical control in biogenic minerals, from precise nanomorphology control to subsequent macroscopic assembly, remains a formidable challenge in artificial synthesis. Studies in biomineralization, however, are largely limited to atomic/molecular scale crystallization, devoting little attention to biomolecular higher order structures (HOSs) which impact critically on long-range assembly of biominerals. Here we demonstrate a biomimetic route that explores peptide HOSs on guiding nanocrystal formation and anisotropic assembly into hierarchical structures. It is found that Pt{100} specific peptide T7 (Ac-TLTTLTN-CONH2) adopts ST-turn, promoting cubic Pt nanocrystal formation at low concentration, and spontaneously transforms into β-sheet with increased concentration. The β-sheet T7-Pt{100} specificity drives cubic Pt nanocrystals to self-assemble into large-area, long-range, [100] linear assemblies. This study provides a robust demonstration for bio/non-biogenic material specificity, nanoscale synthesis, and long-range self-organization with biomolecular HOSs, and opens vast opportunities for multiscale programmable structures.

1. INTRODUCITION Molecular specificities have been widely employed to manipulate the morphologies and assemblies of nanostructures.1 Methods inspired from molecular evolution in biochemistry have been devised for effectively identifying artificial biomolecules with highly specific surface recognition properties, leading to exquisite synthetic control of nanocrystals.2-13 Beyond synthetic control, hierarchical assembly of nanocrystals represents another critical challenge in nanotechnology.14-24 Several strategies, including employing DNA linkers,25 block copolymers26,27 or patchy particles,16,28,29 have led to nanocrystal assemblies that were difficult to achieve otherwise. Nevertheless, most efforts to date focus on the discovery and utilization of the primary structure and chemical functions of specific (bio)molecules in guiding nanocrystal formation or assembly.4 It is well known that many biomolecules exhibit rich HOSs that play important roles in biomaterial growth and assembly.30 Such HOSs, however, remain largely unexplored for material structure creation.31-34 Here we show the Pt{100}-specific peptide molecules can not only exert atomic scale control over nanocrystal formation with selectively displayed crystallographic facets,8 but also through their HOSs to drive long-range assembly of the resulting nanocrystals (0D) into onedimensional (1D) lines in two-dimensional (2D) extended sheets over tens of micrometer scale (Figure 1). To our

knowledge, this is the first demonstration showing that HOSs of biomolecules can be harvested to guide material structure formation and defines a powerful pathway to hierarchical nanostructure assemblies.

2.

RESULTS AND DISCUSSION

2.1. ST-turns of T7 guide the formation of 0D cubic Pt nanocrystals. The Pt{100}-facet-specific peptide T7 (sequence Ac-TLTTLTN-CONH2; T, Threonine; L, Leucine; N, Asparagine) was identified using phage display technique on cubic nanocrystals.8 However, calculations based on random coil structures of T7 in dilute solution give a positive adsorption energy (+13±2 kcal/mol) between T7 and extended Pt{100} surface, indicating T7 does not favor Pt{100}.35 Such discrepancy derived from experiment and simulations suggests that there are other factors dictating the Pt{100} specificity of T7. At the same time, independently folded HOSs, besides the commonly seen random coils,36 are structurally viable in short peptides.3742 Indeed, our experimental results show that ST-turn HOS dominates in T7 at low peptide concentration while βsheet HOS is favored at high concentration (Figure 1). Taking the ST-turn into account, the calculated Pt{100} adsorption energy of T7 renders a negative value of 1.46±0.93 kcal/mol on the extended surface and -8.78±1.26 kcal/mol on a nanocrystal (Figure 2 and S1), suggesting preferential T7-Pt{100} binding that encourages the growth of cubic Pt nanocrystals with only {100} facets. We further show that the nanocrystals self-assemble into long-range

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1D assemblies with the average length reaching tens of micrometers (10s’ µm), simply by increasing the concentration of T7.14-19 Both the crystal growth and assembly process are guided directly by the molecularnanocrystal specific interactions without involving complicated surface modification of the nanocrystals (Figure 1). The presence and dominance of T7 turn structures at low concentration (aqueous T7 solutions from 20 μg/mL to 200 μg/mL, room temperature, pH=7) are suggested by the valley at ~225 nm in the circular dichroism (CD) spectra (Figure 2A),43 and confirmed by the amide I band in Fourier transform infrared spectroscopy (FTIR), where the wavenumber of the deconvoluted peaks clearly show the dominance of turn as the secondary structure (Figure 2B).44

Since a single TLT unit has two threonine residues at both ends, T7 is very likely to form an ST-turn structure within each TLT unit and expresses the characteristic spatial relationship of two close threonines as confirmed by the nuclear Overhauser effect spectroscopy (NOESY) (Figure 2C,D). The cross peaks of H1 in one threonine and H2 in another threonine at 20 μg/mL of T7 in D2O suggest that the hydrogen atoms are spatially close. This spatial adjacency automatically excludes the possibility of β-turns due to steric hindrance. Our simulation results also demonstrate a stable ST-turn conformation with H-bonds formed within a TLT unit in T7 molecules both relaxed in water (3.45 Å H-bond in ST-turn, 2.82-4.43 Å H1-H2 distance, Figure 2D) and on Pt{100} surface (3.28 Å H-bond in ST-turn, 3.35-4.85 Å H1-H2 distance, Figure 2E).

Figure 1. Schematic illustration of the hierarchical nanocrystal assembly. It shows that molecular conformation change of T7 from ST-turns at low concentration to β-sheets at high concentration drives the Pt cubic nanocrystals formation and their subsequent long-range assembly in 1D and 2D. Blue represents T, green represents L, and yellow represents N residues in T7 peptide, respectively.

Additional experiments were performed to further confirm that the ST-turn in T7 directly leads to Pt{100} specific binding and cubic Pt nanocrystal formation. First, we tested the temperature dependence of Pt nanocrystal formation. As expected with increasing reaction temperature, cubic morphology of Pt nanocrystals gradually disappears while entropy-favored random coils emerge instead of the ST-turns in T7 (Figure S2).45 This is consistent with prior studies showing that proteins46 and short peptides39-41 will unfold due to the breakage of Hbonds at elevated temperature. However, as temperature variation may also directly impact peptide binding strength to Pt surface, we deliberately designed a set of T7 variants to investigate the contributions of amino acid residues on ST-turn formation and on peptide’s recognition to Pt{100} facets at room temperature (20 ºC) (Figure S3). The two leucine residues in T7 were replaced with other amino acids with different hydrophobicities and

steric hindrances, such as valine (Ac-TVTTVTN-CONH2, termed T7-V), alanine (Ac-TATTATN-CONH2, termed T7A) and glycine (Ac-TGTTGTN-CONH2, termed T7-G) to examine the effect of hydrophobic aliphatic amino acids (Figure S3A). According to the CD spectra (Figure S3G), T7-V was found to organize similar to T7, adopting STturns, while T7-A and T7-G were mostly random coils. The structural distinction implied that the isopropyl groups in L and V were decisive in terms of high hydrophobicity and steric hindrance. All four T7 variants were then used to synthesize Pt nanocrystals under the same reaction condition. The T7-V-mediated nanocrystals were characterized as cubes by transmission electron microscopy (TEM) whereas cuboctahedra prevailed in the T7-A- and T7-G-mediated nanocrystals (Figure S3B-E). These results agree with our hypothesis that the cubic morphology of nanocrystals is favored by ST-turns rather than random coils. In addition, the variant T7-S (Ac-


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Journal of the American Chemical Society SLSSLSN-CONH2) was also employed (Figure S3A) to examine the role of T. In this case, the secondary structure of T7 is no longer ST-turn but random coil, meaning that T is more critical in ST-turn formation than S. The hydroxyl group in the side chain of T was pushed to a position in favor of the formation of H-bonds to overcome the steric hindrance due to the methyl group on the beta carbon (Figure 2D,E). TEM images also showed that T7-S yielded cuboctahedral instead of cubic nanocrystals (Figure S3F), confirming the correlation between ST-turns and Pt{100} recognition in Pt cube production. 2.2. T7 transforms to 2D β-sheets at high concentrations. Interestingly, with increasing T7 concentration, UV-Raman spectroscopy of aqueous T7 solution shows the shift of the amide I band to high wavenumbers from 200 μg/mL, 800 μg/mL and 1,000 μg/mL, which indicates that the secondary structure of T7 switches from ST-turns to β-sheets as the concentration goes up (Figure S4).47 This concentration-dependent transformation is also confirmed by the amide I bands in FTIR, where the wavenumbers of the deconvoluted peaks clearly show that the dominance of turn structure in 100 μg/mL solution (Figure 2B) changes to β-sheet (Figure 2I)

after the solution is dried up (43). We suggest that ST-turns form at low T7 concentration because the peptide molecules are at a distance from each other so that most hydrogen bonds are intramolecular and the effect of intermolecular forces is negligible. However, at high concentrations the intermolecular hydrogen bonds dominate in T7, and as a result large β-sheets become energetically favorable. Indeed the fringes of dry T7 βsheets are clearly observable under high resolution TEM (HRTEM). The TEM image of slowly dried T7 β-sheets in Figure 2F shows a characteristic striped pattern. The striped pattern is comprised of well aligned β-strand structures whose linearity can be identified by the two conspicuous opposite points in the diffraction pattern of βsheets (Figure 2G). The HRTEM images of T7 β-sheets further showed that the average distance between two adjacent strands is 0.49±0.1 nm (Figure 2G), which agrees well with the reported value.48 It also agrees with our simulation result (Figure 2H) showing 1.6 Å of hydrogen bond between the amine groups in the backbone of one strand and the carbonyl groups in the backbone of the adjacent strands, and about 5 Å distance when including their full geometry and van der Waals radii.

Figure 2. T7 transform from ST-turns under low concentration to β-sheet at high concentration. (A) CD spectra of T7 in H2O at different low concentrations showing clear valley at ~225 nm. (B) FTIR amide I band of 100 μg/mL T7. (C) NOESY of 20 μg/mL T7 in D2O. (D-E) Simulations of T7 peptide structures (D) relaxed in H2O at low concentration, and (E) adsorbed on Pt {100} facets, respectively. In the red circles we highlight ST-turns with N-O distance in red and H1(purple)-H2(green) distances in black. (F)



TEM of slowly dried T7 β-sheets; the scale bar is 1 μm. (G) HRTEM of the designated area in (F) showing clear striped pattern and measured spacing between neighboring strands. The inset shows the diffraction pattern confirming ordering of the structure; the scale bar is 1 nm. (H) Simulation result of T7 β-sheets with consistent spacing between adjacent β strands as shown in (G). (I) FTIR amide I band of slowly dried T7 sheets.

The large-scale assembly of T7 into β-sheets driven by pure H-bond formation is interesting. We note there are reports of lucid approaches leading to peptide assembly based on π-π stacking to acquire biomolecule macrostructures.49 In natural biosystems nevertheless Hbonds rather than π-π stacking is the typical construction mechanism that drives the formation of hierarchical assemblies. Using H-bonds to drive assembly of molecules and materials also provides added advantages of its configurability by simply tuning pH or temperature. For example, in the case of T7 herein, at pH=3 and concentration of 500 μg/mL T7 mainly exist as ST-turns while at pH=12 they form β-sheets (Figure S5). This is because the threonine hydroxyl group has an acid dissociation constant (pKa) of ~13 and begins to partially ionize in a pH=12 environment, which leads to the formation of stronger ionic bonds in addition to intramolecular hydrogen bonds, which are necessary in stabilizing ST-turns50. Consequently, even with a relatively low T7 concentration predominant β-sheets formation is possible at high pH, which can be used to expand the conditions for molecular assembly.

Figure 3. T7 β-sheet drives the unidirectional assembly of Pt nanocrystals in the [100] direction across large area. (A and B) TEM images of assembled nanocrystals under different magnifications. The scale bar in (A) is 2 μm. The scale bar in (B) is 100 nm. (C) The striped pattern of T7 β-sheets in the area squared red in (B). The scale bar in (C) is 1 nm. (D) The fast Fourier transform (FFT) of entire (B) confirming onedirectionality of the assembled Pt nanocrystal structure. (E) The schematics of derived directional interactions between T7 β-sheets and Pt nanocrystal surfaces according to (B) and (C). The β-sheet plane is perpendicular to the two parallel {100} facets on the Pt nanocrystals. Here we designate the y direction as the direction of the 1D assembly of Pt nanocrystals, and the x-y plane as the β-sheet plane. (F) HRTEM image of close-packed nanocrystals linearly assembled along [100] with regular inter-nanocrystal spacing. The scale bar in (F) is 2 nm. (G) Simulation result of the most stable close-packed cubic Pt nanocrystals. Water molecules form a strongly adsorbed interlayer between metal surfaces and peptides (highlighted in blue shading). Peptides were shown in VMD newcartoon representation. The distance between the two close-packed Pt nanocrystals is 12.6±0.1 Å, which agrees well with (F). The scale bar in (G) is 10 Å.

2.3. T7 β-sheets guide regular 1D and 2D hierarchical nanocrystal assembly formation. Significantly, when T7 peptides self-assemble into β-sheets, this process automatically organizes Pt nanocrystals in the same solution into long 1D chains, which organize in parallel fashion within the extended 2D β-sheets. Well-dispersed cubic Pt nanocrystals will gradually align in the [100] direction with evident linearity (Figure 3A,B,F) upon incubation in 1,000 μg/mL T7 solution with temperature dropping from 45 ºC to 20 ºC over a period of 2 hours (Figure S6). The average length of the 1D assemblies is about tens of micrometers (Figure 3A), which is much longer than previous reported numbers.14-19 Furthermore, the nanocrystal assembled structure was also found in the cryo-TEM image made of the frozen T7-Pt nanocrystal sample from solution, confirming that these 1D structures and their 2D assemblies indeed form homogeneously in the solution rather than assemble on a solid surface during the drying process (Figure S7). FTIR measurement on a slowly dried sample including T7 and Pt nanocrystals shows that β-sheets are still the dominant T7 secondary structure, indicating that the 1D Pt nanocrystal lines and their 2D assemblies were guided/templated by the T7 βsheets (Figure S8). We found three factors can be tuned to impact the assembly of nanocrystals: the concentration of T7 (Figure S9), pH (Figure S5) and temperature (Figure S10). Cubic Pt nanocrystals cannot align neatly to form linear structures at high temperature or in an environment with either a T7 concentration lower than 800 μg/mL or at low pH. When


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Journal of the American Chemical Society the temperature is high, entropy dominates and the hydrogen bonds are disturbed. β-sheets therefore are no longer competitive with entropy-favored structures such as random coils.46 To obtain the assembly of Pt nanocrystals with T7, we first incubate the nanocrystals with T7 at higher temperature (45 ºC) to allow for a uniform mixture of Pt nanocrystals and T7 ST-turns. The temperature then gradually decreases to allow β-sheet formation and Pt nanocrystal assembly in 1D and 2D. We found the small temperature gradient (45 ºC to 20 ºC in 2 hrs) could prevent rapid β-sheet formation and enable better interaction between nanocrystals and T7, leading to better assembly (Figure S6). In contrast, a large temperature gradient (from 45 ºC to 20 ºC in 3 min) typically yields nanocrystals without distinguishable assembly pattern. (Figure S10) Remarkably, the nanocrystal assembly process is reversible with varying temperature or pH (Figure S5), suggesting the potential for reconfigurable material assembly by modulating H-bonds among the peptides, highly resembling the hierarchical structures found in biologically assembled structures. Interestingly, within the 1D assembly of Pt nanocrystals, even though not all nanocrystals are close-packed, they still display a straight linear structure (Figure 3B and 5B), which is evidenced by observing the confined movement of the nanocrystals along the 1D assembly direction (y direction) in cryo-TEM [Figure S7 and Movie S1, see details on analyses in the Supporting Information (SI)]. Meanwhile the movement of the Pt nanocrystal in the direction perpendicular to the 1D assembly (x direction) is

limited within the β-sheet. We further examined 200 sets of two closely packed neighboring nanocrystals and found the spacing between two closely packed nanocrystals is 1.22±0.09 nm (Figure 3B,F), which corresponds to an interlayer of water and peptide according to computational results (Figure 3G). In summary, we suggest that the anisotropic assembly of Pt nanocrystals to form linear 1D rows in the y direction, and the parallel assembly of these 1D rows into 2D sheets in the x-y plane are the result of the orientation specific interactions between the Pt nanocrystal surface and T7 β-sheets, and is mediated by βsheet extension in solution. 2.4. Orientation-specific β-sheet-Pt{100} interaction drives the anisotropic nanocrystal assembly. Molecular dynamics simulations were performed to analyze the driving forces for the observed anisotropic nanocrystal assembly in molecular detail (Figure 4). We employed the CHARMM-Interface force field which reproduces metal interfacial properties and mechanisms of ligand binding in high accuracy (see SI for computational details).51-53 The energy change to peptide-peptide interactions within β-sheets from ST-turn at high concentration, the adsorption energies onto the Pt{100} surfaces in various orientations, and the nanocrystalpeptide-nanocrystal interaction energies were analyzed. At high concentration, the formation of ordered β-sheets of T7 peptides from ST-turns is favored by -1.93 kcal/mol per peptide, corresponding to a reversible equilibrium that is clearly driven towards β-sheet formation (Figure 4B).

Figure 4. Interaction energies among T7s, between T7 and Pt surfaces, and between T7 and Pt nanocrystals involved in the assembly process according to molecular dynamics simulation. (A) The coordinate system used in assembly. Pt nanocrystals align in the y direction, T7 β-sheet extends in x-y plane and stack in z direction. (B) Incorporation of peptides from ST-turns into βsheets at high concentration. (C and D) Adsorption preferences of (C) perpendicular and (D) parallel β-sheets on Pt{100} extended surface. (E) The docking of two nanocrystals with sandwiched peptides in close-packed assembly. Water molecules are hidden for visual clarity. NC stands for nanocrystal.

The interaction of the β-sheets with Pt {100} surfaces was tested in different orientations (Figure S11), whereby the simulations involved assemblies up to 36 T7 peptides in

solution. The best binding propensity with -6.53 kcal/mol per T7 peptide was found in a perpendicular orientation (β-sheet plane perpendicular to {100} facet) (Figure 4C). In



this binding configuration, the side chains of T7 point parallel to the surface in the z direction (Figure 1), which facilitates better peptide-Pt nanocrystal surface interactions through polarizable atoms in the backbone (C, N, O), and hydrogen bonds between peptide backbones vertical to the surface in the x direction are maintained (Figure 1 and 4C). Interestingly, the T7 peptide at the bottom layer of the β-sheets on the Pt{100} surface spontaneously changes from the initially given β-sheet structure to ST-turn structure after relaxation (Figure S12), which is consistent with the preference for ST-turns of individual peptides on the Pt{100} surface (Figure 2E). Hydrogen bonds with T7 peptides in the perpendicularly oriented β-sheets are thereby not affected. The perpendicular orientation of the β-sheets in the x direction with respect to the Pt nanocrystal surface, which corresponds to the parallel orientation of the side chains in the z direction, is in good consistency with our HRTEM observation that the 1D organization of the Pt nanocrystals is in the direction of the β-sheet strips (Figure 3B-E). In contrast, adsorption of the β-sheets onto Pt{100} surfaces in parallel orientation (β-sheet plane parallel to {100} facet) was less favored with -1.13 kcal/mol per peptide (Figure 4D). The reason for reduced attraction is that in this parallel orientation the side chains of the T7 have less soft epitaxial contacts for favorable binding on Pt {100} (Figure S11).35

Figure 5. Schematic illustration of the proposed assembly mechanism. The proposed assembly mechanism of cubic Pt nanocrystal in the presence of T7 peptides in solution and their driving force according to the computed interaction energies agree well with experimental observations. ST-turns on nanocrystal surfaces are hidden for visual clarity. NC stands for nanocrystal. The scale bars are 20 nm.

The assembly behaviors of cubic Pt nanocrystals can be explained by their specific interactions with the secondary structures of T7 peptide molecules (Figure 4 and 5). When T7 concentration in solution is low, the peptide molecules are distributed and their intermolecular interactions become negligible due to excessive water, hence T7 adopt ST-turns featuring intramolecular H-bonds, instead of extended β-sheets featuring intermolecular H-bonds. STturns of T7 bind specifically to {100} and lead to the cubic crystal formation (0D) (Figure 5A). As T7 concentration increases, intermolecular H-bonds start to dominate due to the favored energy reduction of -1.93 kcal/mol, leading to β-sheets. (Figure 4B). The orientation specific interaction between β-sheets and Pt {100} in the thermodynamically favorable perpendicular orientation (Figure 4C and S11), drives 0D Pt nanocrystals to assemble into 1D lines along [010] in the y direction (Figure 5B,C). We note that both close-packed 1D assembly and nonclose-packed 1D assembly of the cubic crystals are observed. The TEM observation shows an average cubecube distance of 12.2±0.9 Å in the close-packed assembly (Figure 3F,G), which agrees well with the simulated distance between the two cubes with a layer of ST-turns packed in between (12.6±0.1 Å). Among various possible conformations investigated (Figure S13 and S14), the packing of two cubic nanocrystals with a layer of ST-turns is also found to be the most stable (Figure 4E, 5C, and S15) with a docking energy of -6.72±0.79 kcal/mol per peptide (or -14.22±1.67 mJ/m2, normalized by the facet area of the cubic nanocrystal). Nevertheless, non-close-packed assembly is also observable due to kinetic reason (Figure 5B). Interestingly, in case of non-close-packed nanocrystals, long-range linear assembly is still maintained, which is a direct result of the orientationspecific interactions between the β-sheets and the cube surface. As the pointing orientation (β-strand pointing to {100} facet) interaction between β-sheets and Pt {100} is not preferred (Figure S11), an empty space between two adjacent nanocrystals is created as the pointing-orientated β-sheets on Pt {100} would usually disintegrate, allowing the non-close-packed nanocrystals to move in the y (assembly) direction (Figure S7). Furthermore, 2D alignment of Pt nanocrystals is realized by juxtaposition of β-sheets and 1D nanocrystal arrays (Figure 5D). Consequently, a 2D grid of uni-directionally assembled Pt nanocrystals is accomplished. The results clearly indicate that both the HOS control of T7 into β-sheets and the specific interactions between the Pt{100} surfaces and T7 peptide molecules determine the long-range Pt nanocrystal self-assembly.

3.

CONCLUSIONS

In summary, we have revealed that the secondary structures of T7 is responsible for the anisotropic growth and the subsequent long-range anisotropic and unidirectional assembly of Pt nanocrystals. The ST-turn has been identified and experimentally proven to be the effective motif in the recognition process toward Pt{100} leading to Pt cube formation. At higher concentrations, T7


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Journal of the American Chemical Society will spontaneously transform from ST-turn to β-sheet. Importantly, this self-assembly process in conjunctions with the specific interaction between T7 and cubic Pt nanocrystal can be used to organize the synthesized Pt nanocrystals into 2D sheets consists of unidirectional 1D assemblies along specific [100] direction over a large scale. The demonstration that one can indeed understand and hence explore the HOSs of biomolecules to guide the hierarchical assembly of nanocrystals from nano to macro scale opens up vast opportunities for creating complex material structures like those observed in nature in benign and environmentally harmonious ways.

ASSOCIATED CONTENT Supporting Information. Materials and methods, as well as supplementary data (PDF); Movie S1 (WMV). This material is available free of charge via the Internet at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding Author * [email protected], * [email protected]

Author Contributions ⊥

E. Z. and S. W. contributed equally.

Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT E.Z., X.Y., L.R. and Y.H. acknowledge the Electron Imaging Center of Nanomachines for TEM support. E.Z. acknowledges W.H.H. and Y.C. for cryo-TEM support. E.Z. acknowledge N.O.W. for software support. Y.H. acknowledge support from the Office of Naval Research under Grant number N000141512146. S.W. and H.H. acknowledge the allocation of computational resources at the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory, which is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC0500OR22725, the Argonne Leadership Computing Facility, which is a DOE Office of Science User Facility supported under Contract DE-AC02-06CH11357, and the Janus supercomputer, which is supported by the National Science Foundation (award number CNS-0821794) is acknowledged.

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Journal of the American Chemical Society SYNOPSIS TOC:


Long-Range Hierarchical Nanocrystal Assembly Driven by Molecular

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