Dynamics of DNA Origami Lattice Formation at SolidâLiquid Interfaces

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Surfaces, Interfaces, and Applications

Dynamics of DNA Origami Lattice Formation at Solid-Liquid Interfaces Charlotte Kielar, Saminathan Ramakrishnan, Sebastian Fricke, Guido Grundmeier, and Adrian Keller ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b16047 • Publication Date (Web): 03 Dec 2018 Downloaded from http://pubs.acs.org on December 6, 2018

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ACS Applied Materials & Interfaces

Dynamics of DNA Origami Lattice Formation at Solid-Liquid Interfaces Charlotte Kielar,†,# Saminathan Ramakrishnan,†,# Sebastian Fricke,† Guido Grundmeier,† and Adrian Keller*,†

† Technical and Macromolecular Chemistry, Paderborn University, Warburger Str. 100, 33098 Paderborn, Germany

ABSTRACT The self-organized formation of regular patterns is not only a fascinating topic encountered in a multitude of natural and artificial systems, but also presents a versatile and powerful route towards large-scale nanostructure assembly and materials synthesis. The hierarchical, interface-assisted assembly of DNA origami nanostructures into regular, 2D lattices represents a particularly promising example, as the resulting lattices may exhibit an astonishing degree of order and can be further utilized as masks in molecular lithography. Here, we thus investigate the development of order in such 2D DNA origami lattices assembled on mica surfaces by employing in-situ highspeed atomic force microscopy (AFM) imaging. DNA origami lattice formation is found to resemble thin film growth in several aspects. In particular, the Na+/Mg2+ ratio controls DNA origami adsorption, surface diffusion, and desorption, and is thus equivalent in its effects to substrate temperature which controls adatom dynamics in thin film deposition. Consequently, we

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observe a pronounced dependence of lattice order on Na+ concentration. At low Na+ concentrations, lattice formation resembles random deposition and results in unordered monolayers, whereas very high Na+ concentrations are accompanied by rapid diffusion and especially DNA origami desorption, which prevent lattice formation. At intermediate Na+ concentrations, highly-ordered DNA origami lattices are obtained that display an intricate symmetry, stemming from the complex shape of the employed Rothemund triangle. Nevertheless, even under such optimized conditions, the lattices display a considerable number of defects, including grain boundaries, point and line defects, and screw-like dislocations. By monitoring the dynamics of selected lattice defects, we identify mechanisms that limit the obtainable degree of lattice order. Possible routes toward further increasing lattice order by post-assembly annealing are discussed.

KEYWORDS. DNA origami, lattices, self-assembly, pattern formation, high-speed atomic force microscopy

INTRODUCTION The self-organized formation of regular patterns is a ubiquitous phenomenon in nature that covers all length scales.1 Examples of self-organized pattern formation can be found in galaxies,2 clouds,3 sandy dunes,4 flames,5 crystals,6 quantum systems,7 and the wide variety of biological systems, ranging from sub-cellular entities8 to bacterial colonies9 to animal coats10 to whole ecosystems.11 However, self-organized pattern formation has also become an increasingly important aspect in materials science and nanotechnology,12–14 where the appearance of such patterns may result in drastically altered materials properties, especially for patterns with nanoscale dimensions. For


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instance, regular nanopatterns composed of facetted ripple or dot structures forming spontaneously during epitaxial growth have promising applications in nano- and optoelectronics, as well as magnetism and catalysis.15,16 Similar self-organized nanopatterns can also be produced on various surfaces by low-energy ion beam irradiation.17,18 Also pulsed laser irradiation of materials may result in regular surface and even bulk patterns.19,20 Other examples from the field of thin films include regular surface patterns induced by dewetting,21 wrinkling,22 and microphase separation.23 At a molecular level, ordered patterns of organic or biological molecules in the form of regular 2D lattices may develop at solid-vacuum, solid-liquid or liquid-vapor interfaces due to supramolecular self-assembly.24–29 The molecular building blocks of these patterns are usually rather small and consequently form lattices with periodicities typically of the order of few nanometers or less, which poses certain limits to their general applicability in materials science. However, several recent studies have demonstrated the self-assembly of large DNA nanostructures into regular 1D and 2D lattices at solid-liquid,30–33 lipid-liquid,34–37 and liquid-air interfaces.38 In these systems, lattice formation is a direct result of 2D diffusion of the nanostructures at the interface in combination with either specific intermolecular interactions such as blunt-end stacking30,31,33,35–37 and sticky-end hybridization,32,34 or simple surface energy minimization by increasing the packing density.33,36 Different DNA nanostructures have been employed in this approach ranging from comparatively small DNA tile motifs31,32,37 to large DNA origami nanostructures ~ 100 nm in size,30,33–36 with their shape and intermolecular connectivity governing the symmetry of the forming lattices. Especially for larger DNA origami nanostructures assembling into close-packed lattices, regular patterns spanning several microns in size can be obtained that display an astonishing degree of order.33,36 This is a clear advantage over directing DNA origami adsorption via substrate prepatterning, which not only requires tedious substrate preparation steps but


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typically also results only in rather limited order.39–45 Most intriguingly, such lattices have periodicities in the 100 nm range and may exhibit cavities large enough to be filled with other molecular entities such as various proteins46 or smaller DNA nanostructures,47 resulting in highlyordered hierarchical patterns. Furthermore, such regular 2D DNA origami lattices can potentially be transferred into various inorganic materials using molecular lithography48–51 and for instance enable the fabrication of metamaterials and plasmonic sensor arrays.52 In this work, we have investigated the development of order in such 2D DNA origami lattices assembled on mica surfaces by employing in-situ high-speed atomic force microscopy (AFM) imaging. Adsorption of the anionic DNA origami nanostructures on the negatively charged mica surface is enabled by so-called salt bridges, i.e., shared Mg2+ counterions mediating electrostatic attraction.30,33,53 Adsorption strength can be controlled by addition of monovalent Na+ ions which compete with the Mg2+ ions for the DNA phosphates and the mica surface, resulting in weaker electrostatic attraction.30,33,53 The Na+/Mg2+ ratio thus has an equivalent effect on DNA origami surface diffusion as temperature on adatom diffusion in thin film growth, and affects lattice formation and order in a similar way. Therefore, we first quantitatively assess the effect of Na+ concentration on lattice formation and order, after which we analyze the multifold symmetry of the lattice obtained under optimized conditions in the asymptotic limit. Finally, we monitor the dynamics of selected lattice defects in order to identify mechanisms that limit the obtainable degree of lattice order. MATERIALS AND METHODS DNA origami assembly


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Rothemund triangles54 were assembled as described previously55 by folding the M13mp18 scaffold (Tilibit) via hybridization to 208 staple strands (Metabion). The staple-scaffold mixture was annealed in 1 x TAE buffer (Carl Roth) containing 10 mM MgCl2 (Sigma-Aldrich) using a thermocycler Primus 25 advanced (PEQLAB). The folded DNA origami triangles were purified by spin filtering using Amicon Ultra filters with 100 kDa MWCO (Millipore). DNA origami concentrations were determined by UV-Vis absorption measurements using an IMPLEN NanoPhotometer P 330. High-speed AFM imaging High-speed AFM imaging was performed using a JPK NanoWizard ULTRA Speed and USCF0.3-k0.3 cantilevers (NanoWorld). Measurements were performed in a liquid cell filled with 1 ml of 1xTAE buffer containing 10 mM MgCl2 and NaCl concentrations ranging from 0 mM to 125 mM. The DNA origami concentration was 3 nM in all experiments. For most conditions, AFM images with a scan size of 3 x 3 µm² were recorded at 512 px x 512 px and 10 Hz line rate, corresponding to 51.5 sec per frame. Only for the 125 mM NaCl sample, images were recorded at 256 px x 256 px and 4 sec per frame (65 Hz line rate) to account for the drastically enhanced surface diffusion. For all conditions, the first image of the time series was recorded approximately 4 min after injection of the DNA origami sample. The images were analyzed using Gwyddion open source software.56 RESULTS AND DISCUSSION Influence of Na+ concentration on lattice order


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In DNA origami assembly, Mg2+ concentrations between 10 and 20 mM are typically employed in order to compensate electrostatic repulsion between staples and scaffold. After assembly, the DNA origami can be transferred into selected buffers with much lower Mg2+ concentrations without loss of structural integrity.57–59 DNA origami immobilization on negatively charged surfaces such as mica or SiO2, however, requires the presence of divalent cations such as Mg2+ at concentrations between 10 and 200 mM, to facilitate the formation of salt bridges between the DNA backbone and the respective surface. Once adsorbed, the DNA origami can be exposed to different solutions and may withstand even harsher conditions than in bulk solution.60 On SiO2 surfaces, a reduction of the Mg2+ concentration after adsorption was found to disrupt some of the salt bridges due to Mg2+ desorption, which resulted in increased surface mobility of the DNA origami and enabled their post-adsorption manipulation.61 DNA origami lattice formation on mica surfaces, however, can be accomplished in a single step by exploiting the competition between Mg2+ and Na+ ions for the mica surface.33,46 While the Mg2+ ions form salt bridges and thus promote DNA origami immobilization, competing Na+ binding to the mica surface leads not only to a reduced number of salt bridges but also to partial charge neutralization of the surface. The ratio of Na+ ions to Mg2+ ions thus determines the number of intact salt bridges and thereby the surface mobility of the DNA origami. In the first set of experiments, we therefore investigated the influence of the Na+ concentration in the 10 mM Mg2+-containing DNA origami adsorption buffer on DNA origami lattice assembly by in-situ high-speed AFM. As can be seen in the AFM images in Figure 1 and especially the corresponding 2D Fast Fourier Transforms (FFTs) in the insets, the Na+ concentration has a remarkably strong influence on pattern regularity and order. In the absence of any Na+, surface diffusion of the DNA origami is so low that a mostly unordered monolayer with many pattern


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defects is forming, resulting in an almost circular ring in the FFT that shows only very weak indications of hexagonal symmetry as would be expected for a close-packed 2D lattice of equilateral triangles. This situation is thus similar to random deposition in thin film growth,62 in which each incoming particle firmly attaches to the first surface site it reaches without any subsequent hopping to neighboring sites. At a Na+ concentration of 25 mM, i.e., 2.5-fold excess over Mg2+, however, the attractive interaction between DNA origami and solid surface is sufficiently decreased to allow for some surface diffusion. After 2 524 sec of incubation, the corresponding AFM image in Figure 1 reveals that the formed DNA origami monolayer consists of small domains exhibiting hexagonal order that are separated from each other by defect-rich regions. Compared again to thin film growth, this scenario is equivalent to the formation of a polycrystalline film in which the grains display different orientations and are separated by defect-rich grain boundaries. Nevertheless, the FFT clearly shows a ring of hexagonal shape, indicating the appearance of a hexagonal symmetry in the lattice.


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Figure 1. High-speed AFM images and corresponding FFTs of 2D DNA origami lattice formation at different Na+ concentrations. Scale bars are 500 nm.


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Increasing the Na+ concentration leads to stronger surface diffusion and thus to a lower defect density and larger grains. At 75 mM, the FFT at 2 524 sec exhibits six well-resolved peaks that form the corners of a hexagon and several weaker higher-order peaks at larger wavenumbers, indicating a high degree of order and a multi-fold lattice symmetry. Further increase of the Na+ concentration to 100 mM, however, results in more visible defects and in particular holes in the assembled lattice, and consequently in the FFT appearing blurrier. This decrease of lattice order can be attributed to the low attractive interaction between the DNA origami triangles and the mica surface due to an insufficient number of Mg2+ salt bridges at this concentration, which results in high surface diffusion and also desorption of once adsorbed DNA origami. At an even higher Na+ concentration of 125 mM, the surface interactions become so weak, that no monolayer is forming at all due to the rapid desorption of onceadsorbed DNA origami (see Figure 2). Furthermore, surface diffusion became so fast, that we had to increase the frame rate by more than a factor of 10 in order to resolve the rapidly diffusing DNA origami triangles.

Figure 2. High-speed AFM images of rapid DNA origami diffusion at 125 mM Na+. The arrows highlight single DNA origami nanostructures. The green and blue arrows indicate DNA origami that remain at their


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rough positions but undergo rapid diffusive motions which makes it difficult to identify the triangular shape. The black arrows indicate a DNA origami triangle that desorbs between 252 and 256 sec. Scale bars are 500 nm.

To analyze the development of order under above conditions more quantitatively, we have calculated the radial power spectral density (PSD) functions of the AFM images shown in Figure 1. The resulting plots are shown in Figure 3. For all Na+ concentrations, the diffuse intensity at low k values decreases with increasing incubation time. Furthermore, all the PSD curves show a peak at k ~ 0.1 nm-1, corresponding to a characteristic length of about 65 nm, which appears to be characteristic for the DNA origami triangles. For Na+ concentrations between 0 and 75 mM, this peak slightly decreases in intensity with time, which can be attributed to a continuous reduction of the underlying broad noise peak with an intensity maximum below 0.05 nm-1. Although this decrease in noise hints at the formation of ordered patterns, the fact that the 0.1 nm-1 peak maintains a comparatively low intensity indicates a low degree of pattern order. At a Na+ concentration of 75 mM, however, the situation suddenly changes. Here, the intensity of the 0.1 nm-1 peak increases drastically with assembly time, indicating a strong increase in order, which agrees with the results shown in Figure 1. For a Na+ concentration of 100 mM, no increase in peak intensity is observed, reflecting the lower degree of order.

PSD (nm3)

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Figure 3. Radial PSD functions of the AFM images shown in Figure 1.


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The full width at half maximum (fwhm) of the characteristic peak in the PSD function is a measure of the correlation length of the formed pattern, i.e., the average domain size.63 The so determined correlation length ξ after 2 524 sec of incubation is shown for all Na+ concentrations in Figure 4. Obviously, similar correlation lengths are observed under all conditions, with the exception of 75 mM Na+, where ξ has a value about twice as high as for the other concentrations. This again is in agreement with the observation above, that this particular Na+ concentration of 75 mM results in highly regular DNA origami lattices with an exceptional degree of order. These results thus demonstrate the importance of a precise tuning of the attractive forces acting between the DNA origami and the mica surface for obtaining highly-ordered DNA origami lattices. At too low Na+ concentrations (indicated in yellow in Figure 4), a large number of Mg2+ salt bridges efficiently immobilize the DNA origami on the surface and prevent them from freely diffusing on the surface which, however, is an important prerequisite for the formation of a close-packed monolayer. At too high Na+ concentrations (indicated in red in Figure 4), the Mg2+-mediated attraction between DNA origami and mica surface becomes so low that their high lateral diffusivity and the increasing occurrence of desorption events hinder the formation of a static, densely-packed monolayer. The combination of these competing mechanisms results only in a rather narrow concentration window (indicated in green in Figure 4) in which the DNA origami are adsorbed through an optimal number of salt bridges and undergo just the right amount of diffusive motion to enable formation of a highly ordered lattice with maximum domain size.


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Figure 4. Correlation lengths ξ obtained for the different Na+ concentrations after 2 524 sec of incubation. Colors indicate the strength of the attractive interactions between DNA origami and mica surface: too strong (yellow), too weak (red), and optimal (green) for the formation of highly ordered lattices.

Lattice symmetry and periodicity Above analyses revealed some peculiar features of the assembled lattices. First, the lattice periodicity λ as determined from the radial PSD functions is only about 65 nm, which does not agree with the outer edge length of the DNA origami triangle of nominally 120 nm. The Rothemund triangle is composed of three trapezoids about 30 nm in width and thus features an internal triangular cavity with an inner edge length of nominally 50 nm. However, neither of these dimensions agree with the observed characteristic length λ of 65 nm. Second, the determined correlation length for the 75 mM case of ξ ~ 350 nm is surprisingly small as well, considering the dimensions of the DNA origami triangles. On the other hand, taking into account the periodicity λ ~ 65 nm, this value corresponds to an average domain size of more than 5λ, which is comparable to other self-organized isotropic nanopatterns.64,65 Third, closer inspection of the FFT obtained for the 75 mM sample after 2 524 sec of incubation reveals a more complex intensity distribution than


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what would be expected for a purely hexagonal pattern. Therefore, we have next set out to analyze the symmetry of the lattice assembled at this concentration in the asymptotic limit of long incubation time. Figure 5 shows an AFM image and the corresponding 2D FFT recorded after 4 120 sec. It is rather obvious from the AFM image in Figure 5 that even for such a long incubation time, there is still a significant number of defects. Nevertheless, the corresponding FFT exhibits a well-developed intensity distribution with clearly resolved minima and maxima. The complexity and multi-fold symmetry of the FFT, however, is rather stunning. In order to develop a better understanding of the symmetry of the formed DNA origami lattice, Fourier filtering has been employed.

Figure 5. AFM image and corresponding 2D FFT of a 2D DNA origami lattice assembled for 4 120 sec at a Na+ concentration of 75 mM. The scale bar is 500 nm. The colored boxes indicate the areas corresponding to the zoomed images shown in Figures 9 (green) and 10 (blue).


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As can be seen in Figure 6 (left panel), the inverse transform of the FFT region that includes the inner ring with the six well-defined peaks located at the points of the star-shaped central minimum yields a hole pattern with hexagonal symmetry. However, closer inspection of the resulting hole pattern reveals a hierarchical symmetry with the central hole in the hexagonal unit cell having a smaller diameter, a more circular shape, and a lower depth than the six outer holes. This smaller hole thus corresponds to the center of the hexagonal arrangement where the corners of the six triangles meet. The formation of a hole in the center results directly from the shape of the DNA origami triangles which feature rounded corners instead of pointy ones.

Figure 6. Inverse Fourier transforms of selected regions of the FFT shown in Figure 5. The insets show the corresponding FFT regions (left) and zooms of a single unit cell of the resulting pattern (right).

The inverse transform of the second, hexagonally shaped ring structure of the FFT with its six circular minima, on the other hand, obviously corresponds to the shapes of the individual DNA origami triangles (see Figure 6, central panel). Interestingly, these triangles exhibit a particularly deep triangular hole. This is due to the close arrangement of the DNA origami triangles which are separated only by a very narrow groove that cannot be fully penetrated by the AFM tip.


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The inverse transform of the central FFT region up to and including the second ring consequently results in the superposition of the two patterns discussed above (see Figure 6, right panel). The unit cell of this pattern now consists of a ring of six well-defined triangular holes with a smaller hole of much lower depth in the center. The presence of this central hole provides an explanation of the peculiar pattern periodicity λ of about 65 nm, as in this particular unit cell, the periodicity does not correspond to the distance from the center of mass of one triangle to the next, but rather to the distance from its center of mass to its corner where the central hole of the unit cell is located. For an equilateral triangle such as the Rothemund triangle, this distance corresponds roughly to the altitude of the triangle h minus the radius of the inscribed circle r. For a nominal edge length of 120 nm, h – r = 69 nm, which is in excellent agreement with the periodicity λ of about 65 nm determined from the radial PSD functions in Figure 2. Dynamics of lattice defects Despite the optimized Na+ concentration and the long assembly time, the DNA origami lattice shown in Figure 5 still exhibits many defects, including grain boundaries, dislocations, and missing triangles. It is the persistence of such defects even in the asymptotic limit which is responsible for the comparatively small domain size observed under these optimized conditions. Therefore, we next analyzed the dynamics of selected lattice defects that either were annealed during assembly or prevailed until the end of the experiment. Figure 7 shows high-speed AFM images of the formation and annealing of a point defect that results from the incorporation of a broken DNA origami triangle into the lattice. This occurs already rather early during lattice formation. In the AFM image corresponding to 670 sec, a DNA origami triangle with two incomplete trapezoids appears on the mica surface (indicated by the


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white arrow) and is subsequently incorporated into the lattice, which is otherwise mostly free of any defects in the vicinity (see images at 1 957 sec and 3 348 sec). Despite the pronounced stability of this defect which persists for more than 45 min, however, it is suddenly annealed and replaced by an intact DNA origami (see green arrows in Figure 7). In particular, it appears that the intact DNA origami triangle first partially adsorbs in the small free surface area provided by the internal cavity and the missing trapezoid parts of the damaged triangle and then stimulates its desorption. The intact triangle then fully occupies the available space and the lattice displays perfect order.

Figure 7. Schematic representation (a) and high-speed AFM images (b) of the formation (white arrows) and annealing (green arrows) of a point defect, i.e., an incorporated damaged DNA origami triangle. The


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continuous time series in (b) was recorded with intervals of 51.5 sec between images. The Na+ concentration was 75 mM.

The formation and annealing dynamics of a more complex line defect, reminiscent of a stacking fault, is monitored in Figure 8. Here, a defect-rich region is shown which undergoes significant rearrangements, resulting in the annealing of most of the present dislocations. However, these rearrangements result in the formation of a line defect (indicated by the broken lines in Figure 8) in a largely undisturbed region of the lattice. Despite the large number of rearrangements necessary for its annealing, this line defect does not persist. As can be seen in Figure 8, shortly after formation of the defect, one DNA origami triangle in its close vicinity spontaneously desorbs from the mica surface. Less than a minute later, a second DNA origami desorbs that was part of the right boundary of the line defect (see the white arrow in Figure 8). Consequently, it is the desorption of this second triangle that effectively reduces the lateral confinement of the remaining DNA origami along the defect, which can then start to rearrange their positions and anneal the defect. This rearrangement quickly spreads from the actual defect and involves many DNA origami triangles in the vicinity since annealing requires the whole domain to adjust its lattice orientation to match that of the neighboring domain. This rapid collapse of the imperfect lattice may be further accelerated by the interaction of the DNA origami with the AFM tip. Only 4 min after desorption of the second triangle, the last remaining holes in the lattice have already been filled with new DNA origami from solution and a perfect hexagonal lattice is obtained. The above observations demonstrate that even small and comparatively stable point defects can be annealed at sufficiently long assembly times. Similarly, also large line defects can be annealed by the concerted rearrangement of many DNA origami nanostructures. However, as is obvious from Figure 5, even after more than 1 h incubation, there are still defects present. These defects may


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either be extraordinarily stable and resist annealing, or form rather late during lattice assembly, so that they just have not been annealed yet. As we show below, the persistent defects observed in Figure 5 appear to be both, late-forming and comparatively stable.

Figure 8. Schematic representation (a) and high-speed AFM images (b) of the formation and annealing of a line defect (indicated by the broken lines). The white arrow in (b) indicates a desorbing DNA origami triangle at the right boundary of the line defect. The continuous time series in (b) was recorded with intervals of 51.5 sec between images. The Na+ concentration was 75 mM.


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Figure 9 shows high-speed AFM images that follow the partial annealing of the area indicated in blue in Figure 5. At 3 399 sec, this area exhibits a number of defects, resulting in a moderate rearrangement of the DNA origami triangles. In the course of this rearrangement, however, one DNA origami triangle in the center of the region (white arrows in Figure 9) is getting damaged. In particular, the connection between two trapezoids in the left corner of the triangle appears to be severed. The corners of the triangles have previously been identified as preferential damage sites, resulting from the fact that the connecting bridging staples are the shortest staples in the whole design and thus have rather low melting temperatures.66 The loss of the connection between the two trapezoids compromises the mechanical stability and rigidity of the triangle, which is reflected by the repeated desorption and re-adsorption of one of the trapezoids in Figure 9. While this partial desorption of the triangle seems to stimulate a more substantial rearrangement of the neighboring DNA origami and thus enables a more thorough annealing of the immediate surrounding, the point defect itself is not getting annealed in the time course of the experiment. This is in agreement with the observations made in Figure 7, which revealed that point defects are comparatively stable and may survive for a long time before they are eventually getting annealed. This particular point defect, however, may be even more stable as it occupies the same surface area as an intact triangle, so that it is not as easily displaced by an incoming or neighboring DNA origami. Such a displacement can only happen in the short period during which one of the triangle’s trapezoids is dangling into solution. Furthermore, since the defect formed rather late, most of the earlier defects have already been annealed, resulting in lower dynamics in the vicinity of the point defect and thus in fewer lateral interactions that might stimulate desorption. Therefore, we may expect that this particular point defect will persist for an extended period of time.


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Figure 9. High-speed AFM images showing the late-stage formation of a point defect (white arrows) in the area indicated in blue in Figure 5. The continuous time series was recorded with intervals of 51.5 sec between images. The Na+ concentration was 75 mM.

Another example for a late-forming, comparatively stable defect is shown in Figure 10. Again, the area is quite rich in defects and undergoes substantial rearrangements, until a rather ordered lattice is obtained. However, the selected area does not exhibit perfect order but features a small yet complex defect in its center (broken lines) that resembles the 2D equivalent of a screw dislocation. This screw-like dislocation appears to be more stable than the line defect shown in Figure 8, probably due to its smaller size and the higher degree of order of the surrounding lattice. Especially the latter may be expected to contribute significantly to the increased stability of the defect because most DNA origami found in the final image of the time series in Figure 10 show almost full


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connectivity to their neighbors with only little deviation from a perfect lattice. Disrupting this almost perfect lattice thus requires a rather large amount of energy. Consequently, this screw-like dislocation can be considered kinetically trapped and hard to anneal.

Figure 10. Schematic representation (a) and high-speed AFM images (b) of the late-stage formation of a rather stable screw-like dislocation (indicated by the broken lines in b) in the area indicated in green in Figure 5. The continuous time series in (b) was recorded with intervals of 51.5 sec between images. The Na+ concentration was 75 mM.


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CONCLUSION In summary, we have employed in-situ high-speed AFM to monitor the assembly of triangular DNA origami nanostructures into close-packed 2D lattices on mica surfaces. DNA origami lattice formation is found to resemble surface growth in several aspects. In particular, since the Na+/Mg2+ ratio controls DNA origami adsorption, surface diffusion, and desorption, it is in its effects equivalent to temperature in thin film deposition, which controls adatom dynamics. This is reflected in the Na+ dependence of lattice order. In the absence of any Na+, the situation resembles random deposition in which DNA origami randomly arrive at the surface and remain at their adsorption site. The result is an unordered monolayer. Increasing the Na+ concentration results in increased surface diffusion and thereby the growth of crystallites at the surface. When the growth fronts of two crystallites touch each other, defect rich grain boundaries form and the resulting monolayer resembles a polycrystalline film. At a Na+ concentration of 75 mM, corresponding to a Na+/Mg2+ ratio of 7.5, a highly ordered regular lattice is obtained, which displays an intricate hierarchical multi-fold symmetry, owing to the particular shape of the Rothemund triangle which features not only an internal triangular cavity but also rounded corners. At even higher Na+ concentrations, DNA origami desorption becomes more and more relevant, resulting in decreased lattice order. At 125 mM Na+, the residence time of a DNA origami at the mica surface is too short to facilitate monolayer formation. Even under optimized assembly conditions, i.e., 75 mM Na+ and long assembly times exceeding 1 h, however, the obtained DNA origami lattice still exhibits a considerable number of defects, including grain boundaries, point and line defects, and screw-like dislocations. Therefore, we have monitored the dynamics of selected lattice defects. While large line defects are not very stable and can rapidly be annealed by a massive concerted rearrangement of a large number of DNA origami


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in the surrounding, smaller point defects appear surprisingly stable. Such point defects consist of a damaged DNA origami incorporated into the lattice and can survive for extended periods of time before they are annealed due to replacement with an intact DNA origami from solution. Therefore, even longer incubation times of the order of several hours should result in lower defect densities. This is, however, hindered by the fact that some of the persistent defects form in the course of the annealing of larger, less stable defects. This in particular concerns screw-like dislocations which are embedded in an almost perfect surrounding lattice and thus require a large amount of energy for annealing. Based on our observations, it appears unlikely that lattices with significantly improved lattice order can be obtained simply by increasing the incubation time. Rather, and again in analogy to thin film growth, more complex post-assembly annealing protocols should be investigated. For instance, cycling the Na+ concentration between values that are higher and lower than the optimized one used for lattice assembly may enable the annealing of kinetically trapped screw-like dislocations by temporarily providing sufficient thermal motion to overcome the energy barrier for lattice rearrangement. Since this, however, would require a tedious, repeating exchange of the assembly buffer, which in itself might cause disturbances of the assembled lattices and induce the formation of defects, it may be worth exploring the possibility of a classic thermal cycling. On the other hand, increasing the substrate temperature may result in the adsorbed DNA origami getting more easily damaged during rearrangement and thus in the induction of point defects. All this points toward the necessity of delicately balancing defect annealing and defect induction mechanisms in order to further increase the already astonishing degree of order in these DNA origami lattices. This may for instance be achieved by photon-induced thermal annealing strategies which have shown great potential for directing the self-assembly of other macromolecular systems.67,68


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Finally, the assembly mechanism investigated in this work relies on the rather specific interactions between the Mg2+ ions and the mica surface.30,33,53 Assembling similar DNA origami lattices on other, more relevant substrates such as SiO2, is thus not straightforward. However, since DNA origami desorption from the mica surface can be induced by completely replacing the surfacebound Mg2+ ions by Na+ ions,46 it may be possible to transfer the assembled lattice from the mica substrate to another material, after suitable crosslinking of the individual DNA origami tiles, e.g., via sticky-end hybridization.34 This may enable the application of such highly ordered DNA origami lattices as large-area masks in molecular lithography.48–51 ASSOCIATED CONTENT Supporting Information: High-speed AFM movies of 2D DNA origami lattice assembly AUTHOR INFORMATION Corresponding Author *[email protected] Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. # These authors contributed equally. Notes The authors declare no competing financial interest. REFERENCES


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GRAPHICAL ABSTRACT


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Dynamics of DNA Origami Lattice Formation at SolidâLiquid Interfaces

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Dynamics of DNA Origami Lattice Formation at SolidâLiquid Interfaces