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Toward Dense Biotemplated Magnetic Nanoparticle Arrays: Probing the Particle-Template Interaction Ute Queitsch,*,† Christine Hamann,† Franziska Scha¨ffel,† Bernd Rellinghaus,† Ludwig Schultz,† Anja Blu¨her,‡ and Michael Mertig*,‡ IFW Dresden, P.O. Box 270016, D-01171 Dresden, Germany, and BioNanotechnology and Structure Formation Group, Max Bergmann Center of Biomaterials and Institute of Materials Science, Technische UniVersita¨t Dresden, D-01062 Dresden, Germany ReceiVed: March 9, 2009
We report on experiments to elucidate the underlying mechanism of the recently observed template-directed organization of gas phase deposited FePt nanoparticles into regular two-dimensional (2D) arrays on the bacterial surface protein layer (S-layer) of Bacillus sphaericus NCTC 9602. To this end, the size and charge state of the particles have been tuned prior to their deposition onto the S-layer, and the preferred particle deposition sites have been identified and correlated to the protein template lattice by means of statistical analysis of transmission electron microscopy images of the obtained hybrid structures. The experiments reveal that the match between the nanoparticle geometry and the regularly patterned template surface morphology is most important to achieve a high degree of nanoparticle ordering. Deposited nanoparticles were preferentially located at those sites where the S-layer surface exhibits hollows of appropriate size, so that the particle can reduce its surface free energy by maximizing its contact area with the exposed S-layer surface. Particular sites at the protein layer possessed a bimodal occupation frequency distribution. This can be explained by characteristic differences in the morphologies of the inner and outer faces of the S-layer sheets immobilized at the substrate surface. Experiments with nanoparticles of different charge states did not show significant variations in the particle distribution, indicating that the occurrence of a periodic surface charge modulation at the 2D protein crystal, which is often claimed to be the origin for the self-organization of particles deposited from solution, was not the relevant driving force under the chosen experimental conditions. Introduction Nanoparticles are the subject of intense research due to their outstanding properties and numerous applications in nanoelectronics,1,2 biological detection and sensing,3-5 catalysis,6,7 and magnetic data storage.8,9 In many cases, the key to the successful application of nanoparticles is the simultaneous control of both their synthesis and interparticle interactions at the nanometer scale, i.e., the fabrication of particles with controlled morphology and their simultaneous organization into highly ordered arrays. At present there is a broad variety of top-down fabrication methods that are capable of creating periodically structured arrays, e.g., electron-beam,10,11 ion-based,12,13 and imprint14,15 lithography. However, most of them are serial techniques and, therefore, not suitable for high-throughput manufacturing technologies. Therefore, to develop fast and cost-efficient parallel manipulation techniques, there has emerged intense research on bottom-up strategies for the fabrication of periodic nanoparticle arrays such as nanoparticle-based self-assembly of monolayers,16 large-scale transfer printing techniques,17 or the use of regularly patterned biotemplates, e.g., artificially designed DNA lattices or regular bacterial surface layers (S-layers).18 S-layers are two-dimensional (2D) protein crystals which constitute the outermost cell envelopes of many bacteria and archaea.19,20 They exhibit oblique, square, or hexagonal lattice symmetry with unit cell dimensions in the range 3-30 nm and * Corresponding authors. E-mail:
[email protected] (U.Q.);
[email protected] (M.M.). † IFW Dresden. ‡ Technische Universita¨t Dresden.
regular arrangements of pores with diameters of 2-8 nm. The typical layer thickness is 5-10 nm. S-layers are composed of single protein or glycoprotein units with a molecular weight of 40-200 kDa. The regular arrangement of the single monomer unit in the protein crystal implies that S-layers possess a regular surface charge pattern which arises from protonation/deprotonation of surface-exposed amino acid residues in solution.19,21,22 The morphologies and physicochemical properties of the inner and outer faces of S-layers are different.23-25 In order to use them as large-scale templates, S-layers can be recrystallized in vitro at liquid-air interfaces or substrates.26-28 Taking advantage of their spatially well-defined physical and chemical surface properties, S-layers have extensively been used for the templatedirected synthesis of regular nanoparticle arrays by chemical29-33 or electron-beam-induced34 reduction of metal salts. In addition, S-layers have been utilized as crystalline protein masks for electrochemical deposition of metal cluster arrays.35 In these approaches, the S-layer template is used to control both particle size and arrangement. Alternatively, preformed nanoparticles can be directly deposited on the S-layer from colloidal solutions36-38 or from the gas phase.39,40 The latter class of methods allows precise control of particle properties such as composition, size, and charge before they are deposited onto the S-layer template. However, although S-layers have been widely used as templates for the organization of nanostructures in the past, there is only very limited information about the spatial distribution of the physicochemical properties and, thus, about preferred affinity or binding sites for nanocrystals at
10.1021/jp9020992 CCC: $40.75 2009 American Chemical Society Published on Web 05/13/2009
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TABLE 1: Relevant Preparation Parameters and Reproducibly Obtained Mean Particle Diameters together with According Standard Deviations sample
I (mA)
p (mbar)
fHe (sccm)
dp (nm)
σ (nm)
1 2 3
0.1 0.4 0.4
2 2.5 2.7
30 0 0
2.8 4.5 6.0
0.7 1.3 2.4
S-layer surfaces as well as on the relevant particle-template interactions.32,41,42 In previous investigations we have demonstrated that the S-layer of Bacillus sphaericus NCTC 9602 can act as a molecular template for the organization of gas phase deposited FePt nanoparticles into ordered arrays.39,40 In particular, staining of the S-layer with uranyl acetate before particle deposition allowed precise identification of their positions and relative occupation numbers at the 2D S-layer crystal. Here we used this technique to study the mechanism underlying this biomolecular templating effect in more detail. First, we investigated the impact of the FePt particle size on the spatial distribution of deposited particles. This allowed the derivation of local information about the “geometrically” defined part of the particle adsorption which is basically determined by the contact area between the particle and the S-layer and, thus, depends on the local morphology of the S-layer surface and particle size. Second, by depositing neutral, positively charged, or negatively charged FePt nanoparticles of equal size, we investigated to what extent the particle adsorption at the S-layer is caused by electrostatic interactions.
Figure 1. Particle-size distributions obtained for the parameter sets given in Table 1. dp denotes the mean particle diameter as determined from fitting a log-normal distribution function to the experimental data.
Figure 2. Left: Experimental setup for the deposition of charge-selected particles. An electrostatic field of 330 V/m is generated between the deflector plates and the substrate is moved accordingly along the field axis to deposit either neutral, positively charged, or negatively charged particles. Right: Current to the sample holder as a function of the substrate position during the deposition of charge-selected particles.
Experimental Section The used S-layer was isolated from the bacterium B. sphaericus NCTC 9602. The conditions for cell cultivation and purification of the S-layer sheets are described elsewhere.24,34 The S-layer sheets were adsorbed with random orientation on carbon-coated copper grids and subsequently negatively stained with 2.5% uranyl acetate as described before.34 Transmission electron microscopy (TEM) was performed using a Philips CM20 microscope (200 kV, FEG). The used S-layer exhibits a p4 symmetry with a lattice constant of 12.5 nm and a thickness of 5 nm when dried in air.33 FePt nanoparticles were prepared in a commercially available nanoparticle deposition system (Nanodep 60, Oxford Applied Research Ltd.). The particles nucleated and grew from a supersaturated metal vapor obtained by dc sputtering from a stoichiometric FePt target in an Ar atmosphere of 1 mbar. The particles were then ejected through a combination of apertures into a high vacuum chamber (10-6 mbar e p e 10-4 mbar) where they were deposited onto substrates. A quadrupole mass spectrometer was integrated in the system for in-flight sizing and filtering of particles. The mean particle size was adjusted by varying the sputter current I, the pressure in the nucleation and growth chamber p, and the He flow rate f. Particles were reproducibly prepared at three different parameter sets which are summarized in Table 1. The obtained particle sizes were determined by TEM investigations. The measured particle-size distributions are plotted in Figure 1. Under standard experimental conditions, the probabilities of generating neutral, positively charged, or negatively charged particles are equal. In order to investigate whether electrostatic interactions between the deposited FePt nanoparticles and the S-layer surface play a significant role in the arrangement of nanoparticles, particles with defined charge were deposited on the S-layer template. Charge selection was accomplished by using an electrostatic beam deflector (Figure 2). An electrostatic
Figure 3. Left: Indication of the positions of sites A, B, and C within the crystallographic unit cell of the S-layer with a size of 12.5 × 12.5 nm2. Right: Particles whose centers were located within the gray area, that is, deviated by more than 2 nm from the center positions of sites A, B, and C were considered as “undefined”, and therefore belonged to the particle fraction D.
field of 330 V/m was generated between the particle beam deflector plates, and the position of the substrate along the direction of the field axis was adjusted to deposit only neutral, or positively charged, or negatively charged particles. The concurrent charging of the substrate was controlled by measuring the current to the substrate (Figure 2). The degree of regularity of the arrangement of the deposited FePt nanoparticles was determined by statistical evaluation of the particle positions. To provide statistically relevant data, depending on the particle density, up to 4000 particles on up to 100 S-layer sheets were evaluated for each data point. To accomplish the correlation between the particle positions and the underlying protein lattice, the S-layer structure was revealed by an uranyl acetate stain. In accordance with our previous work,39 the particles were assigned to three distinct sites of the protein lattice (Figure 3): Position “A” corresponds to the minor 4-fold symmetry axis, position “B” corresponds to the minor 2-fold symmetry axis, and position “C” corresponds to the major 4-fold symmetry axis of the S-layer lattice.24,25 Particles whose
Dense Biotemplated Magnetic Nanoparticle Arrays
Figure 4. Left: TEM micrograph of FePt nanoparticles with a mean particle diameter of dp ) 2.8 nm as deposited onto S-layer sheets of B. sphaericus NCTC 9602. Right: Site occupancies as obtained from the statistical analysis of such TEM images (depicted in hashed black bars). The gray bars indicate the site occupancy in case of a mere random particle distribution.
centers deviated by more than 2 nm from the center positions of sites A, B, and C or which could not be clearly recognized as single particles remained “undefined” and were assigned to the particle fraction “D”. In order to assess the quality of the templating effect, any measured site occupancy was compared to an according occupancy for a mere random distribution of particles on the substrate. Assuming an error of 2 nm for the identification of an S-layer site, one obtains statistical “background occupancies” of 8%, 16%, and 8% for the sites A, B, and C, respectively. Accordingly, for a random distribution, 68% of the deposited particles remain undefined and belong to the particle fraction D. These values are noted for comparison in all following site occupancy plots.
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Figure 5. Left: TEM micrograph of FePt nanoparticles with dp ) 4.5 nm on S-layer sheets. Right: Corresponding site occupancies. The color code is the same as in Figure 4.
Figure 6. Left: TEM micrograph of FePt nanoparticles of dp ) 6.0 nm on S-layer sheets. Right: Corresponding site occupancies. The color code is the same as in Figure 4.
Results and Discussion Influence of the Template Morphology. Previous studies on the deposition of gas phase prepared FePt nanoparticles onto S-layers revealed that the protein facilitated an ordered spatial arrangement of the otherwise statistically distributed nanoparticles on the substrate; i.e., the particle arrangement was directly determined by the symmetry and lattice periodicity of the 2D protein crystal. In particular, the occupation of the A site of the S-layer was found to be the largest enhanced compared to the pure statistical lateral distribution of nanoparticles. Here we have varied the size of FePt nanoparticles in a controlled manner prior to deposition, in order to investigate the influence of the template morphology on the particle assembly. With this aim, the particle size was varied in a range which corresponded to the size of specific topological features of the S-layer surface. As shown in Figure 4, for a mean particle diameter of dp ) 2.8 nm, the particles adsorbed almost randomly on the template. Upon increasing the particle size to a mean diameter of dp ) 4.5 nm, a large increase in the occupancy of site A over the value for a pure random particle distribution was observed (Figure 5) as now 25.7% of the particles were positioned there. Also a small increase of about 6% in the occupancy of position B was observed, indicating that, similarly to A, this site facilitated a preferred adsorption of nanoparticles, although its affinity seemed to be less pronounced. The fraction at position C remained constant. As a result of the enhanced occupation of sites A and B, the fraction of undefined particles decreased by roughly 24% with respect to statistically distributed particle deposition. Increasing the mean particle diameter to dp ) 6.1 nm led to a further increase of the occupancy of site A to 33.4% (Figure 6). The further changes in the occupancies of sites B and C compared to those obtained for the 4.5-nm-sized particles lie within the standard deviations. The undefined fraction D decreased to 37.9%.
Figure 7. Dependence of site occupancies on the mean particle diameter. The dashed horizontal lines indicated by open symbols denote the “background” occupancies of the accordant sites of the S-layer.
The results obtained for the different particle sizes are summarized in Figure 7. The derived experimental results clearly showed that the occupancy of site A increased with increasing the particle size. The occupation numbers for 4.5- and 6.1-nm particles were found to be significantly larger than the value of 8% derived for the mere random particle distribution. Furthermore, a smaller increase of the occupancy of site B with increasing particle size was observed, whereas the occupancy of site C was not affected by the variation of the particle size. Caused by the large increase of the specificity of the particle adsorption at site A and the less-pronounced increase of the occupancy of site B, the fraction of the unspecifically adsorbed particles D decreased with increasing particle diameter, resulting in a higher degree of regularity of the nanoparticle arrangement. Consequently, the highest degree of particle ordering at the protein template was obtained for the 6.1-nm particles. We suppose that the observed dependence can be directly explained by taking the three-dimensional (3D) structure of the S-layer protein into account, which determines the morphology of the protein crystal surface. From high-resolution TEM investigations, it is known that the 3D structures of the S-layers of B. sphaericus NCTC 9602, B. sphaericus P1, and Sporosarcina ureae ATCC 13881 and, thus, their surface morphologies are very similar.24,25,31,34 Figure 8 shows a schematic drawing of the basic features of the 3D structure of this type of S-layer as
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Figure 8. Schematic drawing of the S-layer structure according to the 3D reconstruction of the S-layers of B. sphaericus P1 and S. ureae ATCC 13881.24,25 The 3D model shows 2 × 2 unit cells of the protein crystal. The S-layer is presented with the inner face up.
derived from the 3D image reconstructions of the S-layers of B. sphaericus P1 and S. ureae ATCC 13881.24,25 The S-layer is depicted with its inner face up. The main protein domain, located around position C (marked in blue) is the highest, protruding structure. In its center, a pore of about 2 nm in diameter penetrating the whole S-layer is located. The main domains are interconnected by arm domains. The arm domains possess 2-3nm-wide trenches (marked in red), in the center of which position B is located. The surfaces of the arm domains are about 2-3 nm below the main domains. Each region between the four arm domains is covered by a cross-shaped minor protein domain (marked in yellow), in the center of which position A is located. The minor protein domain is closely located to the outer face of the S-layer and, therefore, forms a cavity-like structure at the inner face with a diameter of about 6 nm and a depth of about 4-6 nm. Assuming that the deposited particles are able to migrate over short distances at the protein surface, they will finally adsorb at high-affinity sites. Neglecting charge effects for a moment, a migrating particle will experience a high affinity at those sites where it can maximize its contact area with the underlying S-layer template and, thus, minimize its free surface energy. Immediately, from the structural S-layer features given above, it follows that the surface affinity probed by a migrating particle will depend on the size of the particle itself. Compared to “flat” regions of the S-layer surface, a larger affinity is expected when the particle size matches the characteristic sizes of hollows at the S-layer surface. In accordance with these simple geometric arguments, the smallest deposited particles with a diameter of dp ) 2.8 nm can enter all smaller or bigger hollows/cavities at the S-layer surface, i.e., the protein pores located at the A position, the trenches at the arm domains at B positions, and the larger cavity at site C (cf. Figure 8). Hence, there is no energetic advantage in binding at site A, and as a consequence, a more or less random particle distribution at the S-layer template was observed. In agreement with this model, increasing the particle size to dp ) 4.5 nm led to an increase of the adsorption at site A and less pronounced adsorption at the B sites. The highest specificity of nanoparticle adsorption and accordingly the highest A site occupation was observed for 6.1nm particles, since in this case the particle size equals the size of the S-layer surface cavity located there. Under these circumstances, the largest possible contact area was obtained. In contrast, compared to 4.5-nm particles, the occupation of B sites did not substantially increase for 6.1-nm particles because they are too large to fit into the trenches at the B sites.
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Figure 9. Site occupancies as obtained from the statistical analysis of the particle positions upon variation of the particle charge state for two different particle sizes. White bars: negatively charged particles. Gray bars: neutral particles. Black hatched bars: positively charged particles. The dashed horizontal lines denote the “background” occupancies of the accordant sites of the S-layer.
From here we can conclude that the geometric match between the nanoparticle size and the S-layer surface morphology as well as its accessibility for particles are crucial for the achievement of a high specificity of the nanoparticle adsorption and, thus, for the degree of regularity of the nanoparticle arrangement. Influence of Electrostatic Interactions. Due to protonation/ deprotonation of surface-exposed amino acid residues in solution, S-layers exhibit periodically arranged charge lattices which are different at the inner and outer faces of the protein layer.22,43,44 Usually, at the outer face positively and negatively charged groups nearly compensate, so that this face appears nearly neutral. This is different at the inner face, where one type of surface charge dominates, so that the net surface charge is either negative or positive. The periodic distribution of charge centers at S-layer surfaces has been used to arrange charged nanoparticles or protein cages such as polycationic ferritin on S-layer templates into periodic arrays.36,38,41,42,45 All these experiments have been carried out in liquid solution. So far, it is not thoroughly understood whether these charge lattices will remain, diminish partially, or vanish completely, when the S-layer is dried. Whereas it is usually accepted that dried biomolecules are charge neutral due to charge compensation with counterions, some indications for local charge differences, also depending on the actual extent of hydration, are reported in the literature.46-49 In order to investigate whether electrostatic interactions between gas phase deposited FePt nanoparticles and the S-layer surface play a role in the observed particle ordering, we have carried out experiments with charged nanoparticles using an electrostatic deflector (Figure 2) to sort the particles due to their charge prior to deposition. In the case of existing of effective charge centers at the dried protein layers, a redistribution of the particle positions upon changing the particle charge was expected. To account for morphological effects as discussed above, the experiments were carried out with charge-selected particles of 4.5- and 6.0-nm diameter. Figure 9 shows for these two particle sizes the results of the statistical evaluation of the relative occupancies of the positions A, B, and C as well as of the fraction D for negatively charged, positively charged, and neutral particles. The obtained results show that the influence of the charge state of the deposited FePt particles on the particle arrangement is small. Taking the calculated value for the fraction D to evaluate the particle arrangement, there was slightly more disorder observed for the neutral particles than for the charged ones. This effect, which was nearly equal for positively and negatively charged particles, was found to be more pronounced for the 4.5-nm particles. Notably, the obtained results are in full agreement with the results of the particle-size-dependency study. With 25-30% and 35-40% relative occupations for the particles with dp ) 4.5
Dense Biotemplated Magnetic Nanoparticle Arrays nm and dp ) 6.0 nm, respectively, also here a pronounced occupation of site A was found compared to randomly adsorbed particles. In conclusion, only a little redistribution of the specific site occupancies was observed for the different particle charge states. For 4.5-nm particles, the fraction of undefined particles D was about 10% larger for neutral particles than for positively and negatively charged particles. The observed effect diminished with increasing particle size. This result implies that, if electrostatic interactions played a role in the ordering of gas phase deposited FePt nanoparticles on the dried S-layer sheets, then the effect was small. Compared to perfect nanoparticle ordering achieved in solution by making use of the electrostatic interaction between gold nanoparticles and regular arranged HPI layers as demonstrated by Bergkvist et al.,41 our results indicate that charge lattices, if existing in the dried state, are at least strongly reduced in intensity. However, currently we cannot clearly conclude that this effect was solely caused by the effect of drying. The observed behavior could possibly also be explained by the fact that the presented statistical data were obtained for particles which were deposited onto negatively stained S-layers. Up to now the influence of staining on the templating properties of the S-layers has not been clarified. It may well be that the uranyl acetate treatment also leads to a saturation of the S-layer surface charges. More detailed investigations on this issue would require particle deposition onto native, i.e., unstained, S-layers. Yet, in this case the correlation of the particle positions with the underlaying S-layer lattice will become rather difficult. One way to tackle this problem in future would be the application of cryogenic TEM to allow for imaging of the unstained protein layer with high resolution. Side-Specific Adsorption of FePt Nanoparticles at S-layers. As discussed under Influence of the Template Morphology and Influence of Electrostatic Interactions, the structures of the inner and the outer faces of the used S-layer are different.25,24 The inner face appears more corrugated than the outer one, suggesting that the particle ordering effect will be more pronounced for particles deposited to the inner face. A direct way to investigate this issue would be the deposition of FePt particles onto S-layers which were assembled at the substrate surface with controlled orientation, that is, either with the inner face or with the outer face toward the surface. However, since we worked with S-layer sheets with arbitrary surface orientation, we have tackled the problem of side-specific particle ordering at the template in a different way. We deposited FePt particles of different sizes to arbitrarily oriented S-layer sheets and calculated the related frequency distribution of the occupancy of site A. In accordance with the simple model discussed in the Influence of the Template Morphology section, we expect the following behavior: Small particles will undergo a random distribution at both S-layer faces. Therefore, their frequency distribution will be near the 8% as calculated for a statistical occupation of site A. Larger particles will show a more pronounced occupancy of this site. However, if the ordering effect was different on both S-layer faces, then we would expect a bimodal frequency distribution. The results of the experiments are plotted in Figure 10. They reveal a monomodal A-site frequency distribution for the small particles (dp ) 2.8 nm) with a mean occupancy of about 10% which was close to the expected statistical “background” value of 8%. For particles with dp ) 4.5 nm, a bimodal frequency distribution was clearly observed. Two maxima were found at 24% and 30%. From the 3D S-layer structure25,24 one can infer that the adsorption affinity of site A is less for the outer face
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Figure 10. Frequency distribution of the occupancies of site A for 2.8- and 4.5-nm FePt nanoparticles.
than for the inner one. Therefore, the occupance maximum at 30% can be assigned to the inner S-layer face. The mean A-site occupancy was 26%, which is consistent with the above presented data for particles of this size. A pronounced bimodal distribution of the A-site occupancy was also observed for the 6.0-nm particles. In this case, it was shifted to higher values (results not shown). The occurrence of a bimodal frequency distribution of the A-site occupancy for adequately sized particles proved that the different morphologies of the two S-layer sides strongly influenced the specific particle adsorption. In turn, the A-site occupancy can be used to distinguish between the two S-layer faces. Conclusions Gas phase prepared FePt nanoparticles with tuned size and charge state have been used to investigate the origin for the template-directed arrangement of the particles into ordered arrays at the regular bacterial surface layer protein of B. sphaericus NCTC 9602. The deposited particles preferentially adsorbed at the A site, which corresponds to the minor 4-fold symmetry axis of the regular protein lattice. The experiments clearly showed that the geometric match between the nanoparticle and the exposed S-layer cavity located at the A site is critical for the achievable degree of nanoparticle ordering. This effect, which turned out to be the main driving force to achieve particle ordering, is mainly caused by the reduction of the surface free energy of the particles by maximizing the contact area between particles and the S-layer surface. Experiments with charged particles revealed that electrostatic interactions play only a minor role for the arrangement of the particles into regular arrays. Thus, by the performed experiments a better understanding of the general principles underlying the self-organization of nanoparticles on dried S-layer templates could be achieved. In addition, it could be shown that the particle ordering is different for the two faces of the S-layer. Particle deposition to the inner face, which exhibits the more corrugated structure, led to higher particle ordering. This finding implies that further improvement in the regularity of the particle arrangement may be achieved by utilizing large-scale recrystallization to assemble S-layer crystals where exclusively the inner face will be exposed to the nanoparticle beam. Acknowledgment. The authors thank Beate Katzschner for the isolation of the S-layer protein. Moreover, the financial support of this work by the DFG (Grant ME 1256/13-1), and the BMBF (Grant 03X0004A) is acknowledged. References and Notes (1) Li, J.; Qin, F.; Li, C. M.; Bao, Q.; Chan-Park, M. B.; Zhang, W.; Qin, J.; Ong, B. S. Chem. Mater. 2008, 20, 2057–2059.
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