Letter pubs.acs.org/NanoLett
Plasmonic DNA-Origami Nanoantennas for Surface-Enhanced Raman Spectroscopy Paul Kühler,† Eva-Maria Roller,‡ Robert Schreiber,‡ Tim Liedl,‡ Theobald Lohmüller,*,† and Jochen Feldmann† †
Photonics and Optoelectronics Group, Department of Physics and Center for NanoScience (CeNS), LMU München, Amalienstrasse 54, Munich, 80799, Germany ‡ Department of Physics and Center for NanoScience (CeNS), LMU München, Geschwister-Scholl- Platz 1, Munich, 80539, Germany S Supporting Information *
ABSTRACT: We report that plasmonic nanoantennas made by DNA origami can be used as reliable and efficient probes for surface-enhanced Raman spectroscopy (SERS). The nanoantenna is built up by two gold nanoparticles that are linked together by a three-layered DNA origami block at a separation distance of 6 nm in order to achieve plasmonic coupling and the formation of a plasmonic “hot spot”. The plasmonic properties of the hybrid structure are optically characterized by dark-field imaging and polarization-dependent spectroscopy. SERS measurements on molecules that are embedded in the DNA origami that bridges the nanoantenna gap were performed in order to demonstrate the excellent performance of these structures for enhancing spectroscopic signals. A strong enhancement of the Raman signal was recorded from measurements on single hot spots compared to measurements in bulk. Finally, we show that the laser polarization with respect to the dimer orientation has a strong impact on the SERS performance. KEYWORDS: DNA origami, plasmonic nanoantennas, SERS, nanoparticles
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sensors and for spectroscopy applications, and many examples have been shown in the past.20,21 Taking full advantage of the capabilities of plasmonic nanoantennas, however, is still experimentally challenging for several reasons. First, the two nanoparticles need to be brought closely together at a predefined and well-controlled distance of only a few nanometers. This is difficult to achieve, even with high-end methods such as electron beam lithography. Second, the observed molecules have to be precisely located at the hot spot region in order to benefit from the strongest field enhancement. Finally, the structures need to be stable and stay intact during the course of the measurement. It has been shown, for example, that laser light in resonance with the localized surface plasmon of two gold nanoparticles on a glass surface can already cause a change of the interparticle distance during a SERS measurement.22 In this work, we report on a strategy to overcome these experimental challenges by using DNA origami as a scaffold to build up plasmonic nanoantennas from gold nanoparticles that can be used as sensitive probes for SERS measurements. In recent years, DNA-based nanofabrication techniques that
lasmonic nanoantennas made from two gold nanoparticles that are brought close to each other are capable of confining far-field propagating light to the optical near-field.1−4 This is caused by coupling of the localized surface plasmons of both particles.5−7 The strong electromagnetic field that is generated between the particles upon irradiation with light at the resonance wavelength can be harnessed to enhance the fluorescence signal or the Raman scattering intensity from molecules that are located at the plasmonic hot spot in the nanoparticle gap.8−13 This is particularly true for fluorescent dyes with low quantum efficiency, which can experience an over thousand-fold enhancement of their fluorescence emission.12 Raman spectroscopy is advantageous compared to fluorescence for detecting and identifying chemical compounds because Raman signals arise from discrete vibrational energy levels of the molecules.14 Each spectrum contains a chemical fingerprint of the measured molecule. Raman signal intensities are very weak compared to fluorescence signals because most molecules have a very low scattering cross-section (∼10−29−10−30 cm2).15 At a plasmonic hot spot, however, the Raman scattering intensities from molecules are amplified by several orders of magnitude due to field-enhancement effects that render it possible to obtain a Raman signal from even single molecules.16−19 In light of these properties, it is obvious that plasmonically coupled gold nanoparticles have a great potential as optical © 2014 American Chemical Society
Received: March 14, 2014 Revised: April 16, 2014 Published: April 23, 2014 2914
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enhancement within the plasmonic hot spot which is along the axis of the nanoparticle dimer. The origamis were prepared and purified following published procedures.34 The final solution was then drop-cast on a clean glass coverslip and incubated for 10 min to let the origaminanoantennas adsorb on the substrate. Finally, the sample was dried by spin-coating. Gel electrophoresis and transmission electron microscopy (TEM) revealed a high assembly yield of up to 72% of particle dimers with only a small fraction of single particles and particle aggregates present (Figure 1b and Supporting Information Figure S3 and S4). TEM measurements were also performed to analyze the distance between the gold particles in the assembled dimers (Supporting Information Figure S5). The average gap of a dried DNA-nanoantenna was 6 ± 1 nm, which is even smaller than the expected thickness of the DNA origami block in solution (∼8 nm). This can be explained by a flattening of the DNA origami layers during the drying process.39 We would like to emphasize that the separation distance is only depending on the origami design and even smaller distances are possible, for example, by reducing the number of DNA sheets to two instead of three. In principle, a smaller gap would be desirable because the enhancement of the electromagnetic field between two opposing gold particles is strongly increased toward shorter distances.40 A thinner DNA block, however, leads to a reduced rigidity of the overall nanoantenna structure that may cause larger gap size distribution and a reduced synthesis yield. The origami design shown here and the separation distance of 6 nm was therefore chosen on purpose as it provides a good balance in terms of DNA-origami yield, sample stability, and a high SERS enhancement. The plasmonic properties of individual AuNP assemblies were characterized by dark-field microscopy. A real-color photograph of the randomly distributed, individual origami antennas on the surface of a glass coverslip is shown in Figure 2a. A difference in brightness and color between individual features of the substrate can be noticed already by the naked eye. Scanning electron microscopy measurements were performed to identify the structures as single gold particles (Figure 2a, (v)), or coupled dimers (Figure 2a, (i−iv)) as shown in Figure 2b. The optical differences between monomers and dimers were also quantified in detail by measuring the dark-field scattering spectra of individual structures. A mean red shift of the scattering maximum from 558 ± 6 to 570 ± 3 nm was observed for a dimer structure compared to the spectrum of a single particle due to plasmonic coupling (Figure 2c). The scattered light polarized parallel and perpendicular to the dimer long axis was measured independent from each other in order to disentangle the contributions from the attractive and repulsive dipole coupling in the dimer (Figure 2d). Both components add up to the unpolarized response that is governed by the coupled mode, indicating that the overall red shift of the unpolarized spectrum is a good measure for the coupling strength of the dimer. The relatively narrow distribution of the dimer scattering peak positions illustrates the homogeneity of the hybrid structures given that the red shift due to plasmonic coupling is strongly dependent on the interparticle distance. Furthermore, the optical properties and the polarization dependence of the dimer spectra were found to be in good agreement with theoretical values obtained by Mie calculations (Supporting Information Figure S6)). The applicability of the DNA-assembled AuNP dimers as a sensitive probe for Raman spectroscopy was tested in the next step. Molecules that served as a Raman dye were therefore
employ nanoscale folding and hybridization of DNA oligomer strands have developed into a powerful tool for the synthesis of three-dimensional nanomaterials by self-assembly.23−26 Incorporation of functional groups or labels at the oligomer chains allows binding of certain molecules or metallic nanoparticles to the DNA template with nanoscale accuracy.27−30 In this context, plasmonic nanostructures such as particle dimers as well as chiral plasmonic nanostructures prepared by DNA origami have been reported recently.31−36 DNA nanopillars that are modified with plasmonically coupled gold nanoparticles have been used to increase the fluorescence signal of molecules that were delivered to the plasmonic hot spot.37,38 In this report, we take the next step forward and demonstrate how DNA origami can be used as a template to generate plasmonic nanoparticle dimers that can be used as sensitive probes for SERS. The system we investigated is a hybrid structure consisting of two 40 nm gold nanoparticles (AuNPs) that are functionalized on two sides of a rigid DNA origami block (Figure 1a). The
Figure 1. Schematic illustration and TEM images of a DNA origamiassembled AuNP hybrid structure used for SERS measurements. (a) Schematic of the gold nanoparticle dimer structure that is separated by the DNA structure. The probe consists of two 40 nm Au nanoparticles that are hybridized to a rigid DNA origami block with dimensions of 58 nm × 30 nm and a thickness of 6 nm (dry). The DNA origami block is composed of a scaffolding DNA strand (8064 nucleotides (nt) long) that is folded into shape by 200 short DNA strands (∼40 nt long). The Au nanoparticles are functionalized with thiolated singlestranded DNA (ssDNA) and hybridized to the origami structure by three 15-nucleotide-long linking strands. When illuminated at proper wavelength, a plasmonic “hot spot” is formed in the gap between the AuNPs that can be used for enhancing fluorescence or Raman signals. (b) TEM micrograph of AuNP dimers adsorbed on a carbon-coated Formvar TEM grid. (c) Close-up of two origami probes. The separation distance between the gold nanoparticles is defined by the thickness of the DNA sheet that spans the entire nanoparticle gap. At the same time, the DNA origami acts as a scaffold to incorporate molecules for Raman detection. The shell surrounding the nanoparticles originates from the ssDNA molecules which are bound to the particle surface.
origami is built up by a stack of three layers of DNA and has a side length of 58 nm × 30 nm in solution. The AuNPs are closely apposed on each side of the origami block with a separation distance that is defined by the thickness of the origami sheet and the linking DNA molecules (Supporting Information, Figures S1 and S2). Because the origami block spans the gap between the particles it can be employed as a scaffold to incorporate or bind any molecule of interest directly to the DNA sheet. This configuration offers the advantage that the analyte is located precisely at the region of highest field 2915
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Figure 2. Characterization and SERS spectra of individual origami-AuNP dimers. (a) Real-color photograph of individual nanoparticle dimers (i−iv) and single gold nanoparticles (v) taken in dark-field illumination. (b) SEM images of particles marked in panel (a). (c) Unpolarized scattering spectra of the individual dimers and the monomer marked in panel a. The maxima of single particle (v) and a gold nanoparticle dimer (i) are located at 565.5 and 575.4 nm, respectively. (d) Comparison between the unpolarized and the polarization dependent scattering spectra of the AuNP dimer (iv) with respect to the dimer axis. The perpendicular polarized scattered light intensity is at maximum at 562.2 nm and the horizontally polarized part at 572.9 nm. (e) Unpolarized Raman spectra of individual dimers with intercalated SYBR Gold molecules (spectra (i−iv)) and the highly concentrated bulk solution (black curve) of SYBR-Gold. The peaks are located at ΛBG = 920 cm−1, Λ1 = 1250 cm−1, Λ2 = 1365 cm−1, Λ3 = 1490 cm−1, and Λ4 = 1550 cm−1. Spectrum (v) shows a measurement taken from a single gold nanoparticle at position (v) shown in panel a for comparison with the SERS spectra obtained from nanoparticle dimers.
of 2 × 106 in the center. Additionally, the calculations reveal that the |E|4 enhancement varies by a factor of 2 for a gap size between 5 and 7 nm (which is expected for individual nanoparticle dimers according to TEM analysis). This factor of 2 agrees very well with the experimentally observed variation of the peak intensities between SERS measurements on different dimer structures as shown in Figure 2e. Using DNA origami as a method to generate plasmonic nanoantennas for Raman spectroscopy bears the risk that an unwanted background peak from the DNA might contribute to the measured spectrum. We therefore performed control experiments on origami-antennas that were not labeled with any dye to analyze the level of background contribution and its potential limitation for the DNA origami approach. An example for a spectrum of a plain origami dimer is shown in Figure S8a in the Supporting Information. Three main peaks at 998, 1087, and 1587 cm−1 and smaller Raman shifts at 759, 1028, and 1129 cm−1 were observed. These spectral bands can be assigned to the thymine nucleotides of the ssDNA strand that is bound to the nanoparticles (759, 998, 1029 cm−1),42 the conjugate Adenine binding sequence on the origami sheet (1587 cm−1),43 and the phosphodioxy- (PO2−) band of the DNA backbone (1087 cm−1).42,43 The main occurrence of thymine peaks is likely observed because the poly-T strands covering the complete nanoparticle surface where the |E4| enhancement is also strong (Supporting Information Figure S7). Notably, none of the Raman bands of the DNA background were observed in the SYBR Gold spectra shown in Figure 2. This can be explained because the measurements on the dye were performed with lower laser intensity. A Raman signal from DNA was only observed when the laser power was increased by at least a factor of 4 which corresponds to a laser power density of ∼9 kW/cm2. The dye analyte therefore showed a much stronger enhancement, likely because of a larger scattering cross
selectively incorporated into the origami block between the particles. We used SYBR Gold, a minor groove-binding fluorescent nucleic acid stain that has a high affinity to double-stranded DNA. In our experiments, we expect a ratio of at least 1 molecule per 20 base pairs to label the DNA block if it is incubated with stoichiometric amounts of dye molecules. The measurement was performed using an excitation laser wavelength of 568 nm in order to match the plasmon resonance of the gold nanoparticle dimers. The SERS spectra obtained from the individual AuNP dimers shown in Figure 2a are displayed in Figure 2e. We could clearly attribute the Raman peaks Λ1−Λ4 to the SYBR Gold molecules by comparing the data with the spectrum of a highly concentrated bulk solution. A spectrum taken from a single particle (Figure 2e (v)) shows that the SYBR Gold peaks that are observed for the dimer structure are missing. Only a small peak at Λ2 = 1365 cm−1 and a broad peak at ΛBG = 920 cm−1 are observed. The broad 920 cm−1 peak was found also for control measurements that were done on the same substrate but far away from any particles. A Raman band at this wavenumber, however, is characteristic of phosphate and thus likely originates from molecular residuals from the buffer solution which was mainly phosphate buffer saline (PBS).41 As already mentioned, the strongest SERS enhancement is expected from molecules that are located precisely at the hot spot between the two gold nanoparticles. We performed finitedifference time-domain (FDTD) calculations to estimate both, the size of the hot spot region and the expected |E|4 enhancement (Supporting Information Figure 7). From the estimated size of the hot spot, we concluded that approximately 25 dye molecules are located in the gap region. This yields to a mean SERS enhancement factor (EF) of 3.1 × 105 for the 1365 cm−1 peak. This value also compares well to FDTD calculations that yield an averaged |E|4 enhancement of 1.4 × 105 over the whole hot spot region and an enhancement 2916
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Figure 3. The SERS intensity of the 1365 cm−1 Raman peak is depending on the polarization orientation of the exciting laser. (a) SEM images of individual DNA-assembled AuNP dimers. (b) SERS peak height at 1365 cm−1 extracted from Raman spectra that were taken at different relative polarization orientations of the exciting laser. (c) SERS spectra taken at a laser polarization parallel and perpendicular to the gold dimer axis.
the analyte with respect to the dimer axis48 (Supporting Information Figure S9). A SERS spectrum of SYBR Gold for both, parallel and perpendicular orientation of the laser light with respect to the nanoparticle dimer axis is shown in Figure 3c. When the laser polarization is aligned to the dimer, the field enhancement in the particle gap, and accordingly the SERS enhancement, reaches its maximum. On the opposite, at perpendicular orientation the SERS effect is at a minimum. These results agree well with the picture of the polarization-dependent plasmonic response of the coupled dimer, which was found in the scattering spectra (Figure 2d). This illustrates the importance of aligning the exciting laser polarization with the dimer long axis in order to achieve the maximum field enhancement and the strongest SERS signal intensity. Also, the signal intensity was reaching its initial values after a full measurement over 180°, which again confirms the long-term stability of the origami structure. Overall, the strategy to use DNA origami for the synthesis of plasmon coupled nanoantennas expands the applicability for sensor applications based on SERS detection. DNA selfassembly represents a reliable fabrication method to create probes of strongly coupled nanoparticle dimers with a wellcontrolled geometry and separation distance at the nanoscale. A DNA-nanoantenna design that spans the nanoparticle gap as demonstrated here also provides an addressable scaffold for delivering functional molecules precisely to the hot spot region located at the center between the two closely apposed particles and at the same time improves the rigidity and stability of the origami structure to prevent sample degradation during the measurement. Importantly, the sequence-specific addressability of DNA origami itself may be used as a template to locate certain molecules of interest via specific binding precisely at the hot spot region. DNA origami structures potentially carry multiple, sequence-defined binding sites where a wide variety of (bio)molecules can be attached. This may allow to specifically target molecules in solution or potentially inside living cells. This feature marks a clear advantage compared to other methods that rely on random adsorption of molecules to the nanoantenna gap.
section of the dye molecules compared to DNA. No background signal was observed when the unlabeled origami was measured with the same integration time and laser power density that were used for the measurements of SYBR Gold. For measurements conducted with sufficiently high laser intensities, however, the DNA background peaks might appear in the spectrum which makes a further peak analysis necessary. This has been tested for two other dyes (POPO3-Iodide and SYBR green) and is exemplarily shown in the Supporting Information, Figure S8b,c. In general, the use of low laser intensities is favorable for any Raman measurement on nanoparticle-origami samples because light absorbed by plasmonic particles is very efficiently converted into heat and temperature elevations of several hundred degrees Celsius can be reached within a few picoseconds. A strong heating could cause DNA melting and thus lead to a disassembly of the DNA origami.44,45 We observed that throughout the measurements on the origami dimer structures the SERS signal was homogeneous and stable. This indicates that the laser power used in our experiments is sufficiently low to prevent thermal degradation of the nanoantennas due to plasmonic heating. Only a small bleaching was observed after several minutes of laser exposure but SEM analysis of the sample afterward showed that the dimer structure was still intact and that the bleaching was solely caused by dye degradation. For a coupled gold nanoparticle dimer, Raman scattering is expected to be strongest along the dimer axis due to the strongest field enhancement in the particle gap. We investigated the impact of the polarization dependence of the SERS signal for the AuNP dimers in more detail as shown in Figure 3. The Λ2 = 1365 cm−1 peak height was evaluated for different excitation laser polarization orientations with respect to the dimer axis (Figure 3a,b). Each polarization-dependent measurement was performed on a single dimer structure with an integration time of 100 s for each data point. When comparing the absolute values of the peak height among the different hybrid structures for nonpolarized light, only small differences were observed. The polarization dependency of a SERS peak can be understood in the frame of the E4 model, which is a widely accepted explanation for the SERS effect.46,47 According to this model, the data in Figure 3b can be described by ISERS ∼ I⊥ cos4(α) + I∥ cos2(α)sin2(α), where α is the angle between the excitation light polarization and the dimer axis, and I⊥ and I∥ depend on the orientation of the associated Raman dipole of
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ASSOCIATED CONTENT
S Supporting Information *
Materials and methods and information about the DNA origami block structure, the gold nanoparticle attachment, 2917
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(17) Willets, K. A.; Van Duyne, R. P. Localized Surface Plasmon Resonance Spectroscopy and Sensing. Annu. Rev. Phys. Chem. 2007, 58, 267−297. (18) Camden, J. P.; et al. Probing the Structure of Single-Molecule Surface-Enhanced Raman Scattering Hot Spots. J. Am. Chem. Soc. 2008, 130, 12616−12617. (19) Kleinman, S. L.; Frontiera, R. R.; Henry, A.-I.; Dieringer, J. A.; Van Duyne, R. P. Creating, characterizing, and controlling chemistry with SERS hot spots. Phys. Chem. Chem. Phys. 2013, 15, 21. (20) Lal, S.; Link, S.; Halas, N. J. Nano-optics from sensing to waveguiding. Nat. Photonics 2007, 1, 641−648. (21) Anker, J. N.; et al. Biosensing with plasmonic nanosensors. Nat. Mater. 2008, 7, 442−453. (22) Ringler, M.; et al. Moving Nanoparticles with Raman Scattering. Nano Lett. 2007, 7, 2753−2757. (23) Chen, J. H.; Seeman, N. C. Synthesis from DNA of a molecule with the connectivity of a cube. Nature 1991, 350, 631−633. (24) Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 2006, 440, 297−302. (25) Douglas, S. M.; et al. Self-assembly of DNA into nanoscale three-dimensional shapes. Nature 2009, 459, 414−418. (26) Seeman, N. C. Nanomaterials Based on DNA. Annu. Rev. Biochem. 2010, 79, 65−87. (27) Nykypanchuk, D.; Maye, M. M.; Van der Lelie, D.; Gang, O. DNA-guided crystallization of colloidal nanoparticles. Nature 2008, 451, 549−552. (28) Alivisatos, A. P.; et al. Organization of “nanocrystal molecules” using DNA. Nature 1996, 382, 609−611. (29) Xu, X.; Rosi, N. L.; Wang, Y.; Huo, F.; Mirkin, C. A. Asymmetric Functionalization of Gold Nanoparticles with Oligonucleotides. J. Am. Chem. Soc. 2006, 128, 9286−9287. (30) Zheng, J.; et al. Two-Dimensional Nanoparticle Arrays Show the Organizational Power of Robust DNA Motifs. Nano Lett. 2006, 6, 1502−1504. (31) Chen, Y.; Cheng, W. DNA-based plasmonic nanoarchitectures: from structural design to emerging applications. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology 2012, 4, 587−604. (32) Ding, B.; et al. Gold Nanoparticle Self-Similar Chain Structure Organized by DNA Origami. J. Am. Chem. Soc. 2010, 132, 3248−3249. (33) Fan, J. A.; et al. Self-Assembled Plasmonic Nanoparticle Clusters. Science 2010, 328, 1135−1138. (34) Kuzyk, A.; et al. DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response. Nature 2012, 483, 311− 314. (35) Mastroianni, A. J.; Claridge, S. A.; Alivisatos, A. P. Pyramidal and Chiral Groupings of Gold Nanocrystals Assembled Using DNA Scaffolds. J. Am. Chem. Soc. 2009, 131, 8455−8459. (36) Shen, X.; et al. Rolling Up Gold Nanoparticle-Dressed DNA Origami into Three-Dimensional Plasmonic Chiral Nanostructures. J. Am. Chem. Soc. 2012, 134, 146−149. (37) Schmied, J. J.; et al. DNA Origami Nanopillars as Standards for Three-Dimensional Superresolution Microscopy. Nano Lett. 2013, 13, 781−785. (38) Acuna, G. P.; et al. Fluorescence Enhancement at Docking Sites of DNA-Directed Self-Assembled Nanoantennas. Science 2012, 338, 506−510. (39) Stein, I. H.; Schüller, V.; Böhm, P.; Tinnefeld, P.; Liedl, T. Single-Molecule FRET Ruler Based on Rigid DNA Origami Blocks. ChemPhysChem 2011, 12, 689−695. (40) McMahon, J. M.; et al. Gold nanoparticle dimer plasmonics: finite element method calculations of the electromagnetic enhancement to surface-enhanced Raman spectroscopy. Anal. Bioanal. Chem. 2009, 394, 1819−1825. (41) Pye, C. C.; Rudolph, W. W. An ab Initio, Infrared, and Raman Investigation of Phosphate Ion Hydration. J. Phys. Chem. A 2003, 107, 8746−8755. (42) Movileanu, L.; Benevides, J. M.; Thomas, G. J. Temperature dependence of the raman spectrum of DNA. Part IRaman
nanogap size, gel electrophoresis data, Mie and FDTD calculations, and further SERS measurements of additional analytes. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail: [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. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors thank Dr. Lidiya Osinkina and Dr. Frank Jäckel for helpful discussions. Financial support by the ERC through the Advanced Investigator Grant HYMEM, by the DFG through the Nanosystems Initiative Munich (NIM) and through the Sonderforschungsbereich (SFB1032), project A6 and A8, and by the Volkswagen Foundation is gratefully acknowledged.
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Plasmonic DNA-Origami Nanoantennas for Surface-Enhanced Raman Spectroscopy Paul Kühler,† Eva-Maria Roller,‡ Robert Schreiber,‡ Tim Liedl,‡ Theobald Lohmüller,*,† and Jochen Feldmann† †
Photonics and Optoelectronics Group, Department of Physics and Center for NanoScience (CeNS), LMU München, Amalienstrasse 54, Munich, 80799, Germany ‡ Department of Physics and Center for NanoScience (CeNS), LMU München, Geschwister-Scholl- Platz 1, Munich, 80539, Germany S Supporting Information *
ABSTRACT: We report that plasmonic nanoantennas made by DNA origami can be used as reliable and efficient probes for surface-enhanced Raman spectroscopy (SERS). The nanoantenna is built up by two gold nanoparticles that are linked together by a three-layered DNA origami block at a separation distance of 6 nm in order to achieve plasmonic coupling and the formation of a plasmonic “hot spot”. The plasmonic properties of the hybrid structure are optically characterized by dark-field imaging and polarization-dependent spectroscopy. SERS measurements on molecules that are embedded in the DNA origami that bridges the nanoantenna gap were performed in order to demonstrate the excellent performance of these structures for enhancing spectroscopic signals. A strong enhancement of the Raman signal was recorded from measurements on single hot spots compared to measurements in bulk. Finally, we show that the laser polarization with respect to the dimer orientation has a strong impact on the SERS performance. KEYWORDS: DNA origami, plasmonic nanoantennas, SERS, nanoparticles
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sensors and for spectroscopy applications, and many examples have been shown in the past.20,21 Taking full advantage of the capabilities of plasmonic nanoantennas, however, is still experimentally challenging for several reasons. First, the two nanoparticles need to be brought closely together at a predefined and well-controlled distance of only a few nanometers. This is difficult to achieve, even with high-end methods such as electron beam lithography. Second, the observed molecules have to be precisely located at the hot spot region in order to benefit from the strongest field enhancement. Finally, the structures need to be stable and stay intact during the course of the measurement. It has been shown, for example, that laser light in resonance with the localized surface plasmon of two gold nanoparticles on a glass surface can already cause a change of the interparticle distance during a SERS measurement.22 In this work, we report on a strategy to overcome these experimental challenges by using DNA origami as a scaffold to build up plasmonic nanoantennas from gold nanoparticles that can be used as sensitive probes for SERS measurements. In recent years, DNA-based nanofabrication techniques that
lasmonic nanoantennas made from two gold nanoparticles that are brought close to each other are capable of confining far-field propagating light to the optical near-field.1−4 This is caused by coupling of the localized surface plasmons of both particles.5−7 The strong electromagnetic field that is generated between the particles upon irradiation with light at the resonance wavelength can be harnessed to enhance the fluorescence signal or the Raman scattering intensity from molecules that are located at the plasmonic hot spot in the nanoparticle gap.8−13 This is particularly true for fluorescent dyes with low quantum efficiency, which can experience an over thousand-fold enhancement of their fluorescence emission.12 Raman spectroscopy is advantageous compared to fluorescence for detecting and identifying chemical compounds because Raman signals arise from discrete vibrational energy levels of the molecules.14 Each spectrum contains a chemical fingerprint of the measured molecule. Raman signal intensities are very weak compared to fluorescence signals because most molecules have a very low scattering cross-section (∼10−29−10−30 cm2).15 At a plasmonic hot spot, however, the Raman scattering intensities from molecules are amplified by several orders of magnitude due to field-enhancement effects that render it possible to obtain a Raman signal from even single molecules.16−19 In light of these properties, it is obvious that plasmonically coupled gold nanoparticles have a great potential as optical © 2014 American Chemical Society
Received: March 14, 2014 Revised: April 16, 2014 Published: April 23, 2014 2914
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enhancement within the plasmonic hot spot which is along the axis of the nanoparticle dimer. The origamis were prepared and purified following published procedures.34 The final solution was then drop-cast on a clean glass coverslip and incubated for 10 min to let the origaminanoantennas adsorb on the substrate. Finally, the sample was dried by spin-coating. Gel electrophoresis and transmission electron microscopy (TEM) revealed a high assembly yield of up to 72% of particle dimers with only a small fraction of single particles and particle aggregates present (Figure 1b and Supporting Information Figure S3 and S4). TEM measurements were also performed to analyze the distance between the gold particles in the assembled dimers (Supporting Information Figure S5). The average gap of a dried DNA-nanoantenna was 6 ± 1 nm, which is even smaller than the expected thickness of the DNA origami block in solution (∼8 nm). This can be explained by a flattening of the DNA origami layers during the drying process.39 We would like to emphasize that the separation distance is only depending on the origami design and even smaller distances are possible, for example, by reducing the number of DNA sheets to two instead of three. In principle, a smaller gap would be desirable because the enhancement of the electromagnetic field between two opposing gold particles is strongly increased toward shorter distances.40 A thinner DNA block, however, leads to a reduced rigidity of the overall nanoantenna structure that may cause larger gap size distribution and a reduced synthesis yield. The origami design shown here and the separation distance of 6 nm was therefore chosen on purpose as it provides a good balance in terms of DNA-origami yield, sample stability, and a high SERS enhancement. The plasmonic properties of individual AuNP assemblies were characterized by dark-field microscopy. A real-color photograph of the randomly distributed, individual origami antennas on the surface of a glass coverslip is shown in Figure 2a. A difference in brightness and color between individual features of the substrate can be noticed already by the naked eye. Scanning electron microscopy measurements were performed to identify the structures as single gold particles (Figure 2a, (v)), or coupled dimers (Figure 2a, (i−iv)) as shown in Figure 2b. The optical differences between monomers and dimers were also quantified in detail by measuring the dark-field scattering spectra of individual structures. A mean red shift of the scattering maximum from 558 ± 6 to 570 ± 3 nm was observed for a dimer structure compared to the spectrum of a single particle due to plasmonic coupling (Figure 2c). The scattered light polarized parallel and perpendicular to the dimer long axis was measured independent from each other in order to disentangle the contributions from the attractive and repulsive dipole coupling in the dimer (Figure 2d). Both components add up to the unpolarized response that is governed by the coupled mode, indicating that the overall red shift of the unpolarized spectrum is a good measure for the coupling strength of the dimer. The relatively narrow distribution of the dimer scattering peak positions illustrates the homogeneity of the hybrid structures given that the red shift due to plasmonic coupling is strongly dependent on the interparticle distance. Furthermore, the optical properties and the polarization dependence of the dimer spectra were found to be in good agreement with theoretical values obtained by Mie calculations (Supporting Information Figure S6)). The applicability of the DNA-assembled AuNP dimers as a sensitive probe for Raman spectroscopy was tested in the next step. Molecules that served as a Raman dye were therefore
employ nanoscale folding and hybridization of DNA oligomer strands have developed into a powerful tool for the synthesis of three-dimensional nanomaterials by self-assembly.23−26 Incorporation of functional groups or labels at the oligomer chains allows binding of certain molecules or metallic nanoparticles to the DNA template with nanoscale accuracy.27−30 In this context, plasmonic nanostructures such as particle dimers as well as chiral plasmonic nanostructures prepared by DNA origami have been reported recently.31−36 DNA nanopillars that are modified with plasmonically coupled gold nanoparticles have been used to increase the fluorescence signal of molecules that were delivered to the plasmonic hot spot.37,38 In this report, we take the next step forward and demonstrate how DNA origami can be used as a template to generate plasmonic nanoparticle dimers that can be used as sensitive probes for SERS. The system we investigated is a hybrid structure consisting of two 40 nm gold nanoparticles (AuNPs) that are functionalized on two sides of a rigid DNA origami block (Figure 1a). The
Figure 1. Schematic illustration and TEM images of a DNA origamiassembled AuNP hybrid structure used for SERS measurements. (a) Schematic of the gold nanoparticle dimer structure that is separated by the DNA structure. The probe consists of two 40 nm Au nanoparticles that are hybridized to a rigid DNA origami block with dimensions of 58 nm × 30 nm and a thickness of 6 nm (dry). The DNA origami block is composed of a scaffolding DNA strand (8064 nucleotides (nt) long) that is folded into shape by 200 short DNA strands (∼40 nt long). The Au nanoparticles are functionalized with thiolated singlestranded DNA (ssDNA) and hybridized to the origami structure by three 15-nucleotide-long linking strands. When illuminated at proper wavelength, a plasmonic “hot spot” is formed in the gap between the AuNPs that can be used for enhancing fluorescence or Raman signals. (b) TEM micrograph of AuNP dimers adsorbed on a carbon-coated Formvar TEM grid. (c) Close-up of two origami probes. The separation distance between the gold nanoparticles is defined by the thickness of the DNA sheet that spans the entire nanoparticle gap. At the same time, the DNA origami acts as a scaffold to incorporate molecules for Raman detection. The shell surrounding the nanoparticles originates from the ssDNA molecules which are bound to the particle surface.
origami is built up by a stack of three layers of DNA and has a side length of 58 nm × 30 nm in solution. The AuNPs are closely apposed on each side of the origami block with a separation distance that is defined by the thickness of the origami sheet and the linking DNA molecules (Supporting Information, Figures S1 and S2). Because the origami block spans the gap between the particles it can be employed as a scaffold to incorporate or bind any molecule of interest directly to the DNA sheet. This configuration offers the advantage that the analyte is located precisely at the region of highest field 2915
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Figure 2. Characterization and SERS spectra of individual origami-AuNP dimers. (a) Real-color photograph of individual nanoparticle dimers (i−iv) and single gold nanoparticles (v) taken in dark-field illumination. (b) SEM images of particles marked in panel (a). (c) Unpolarized scattering spectra of the individual dimers and the monomer marked in panel a. The maxima of single particle (v) and a gold nanoparticle dimer (i) are located at 565.5 and 575.4 nm, respectively. (d) Comparison between the unpolarized and the polarization dependent scattering spectra of the AuNP dimer (iv) with respect to the dimer axis. The perpendicular polarized scattered light intensity is at maximum at 562.2 nm and the horizontally polarized part at 572.9 nm. (e) Unpolarized Raman spectra of individual dimers with intercalated SYBR Gold molecules (spectra (i−iv)) and the highly concentrated bulk solution (black curve) of SYBR-Gold. The peaks are located at ΛBG = 920 cm−1, Λ1 = 1250 cm−1, Λ2 = 1365 cm−1, Λ3 = 1490 cm−1, and Λ4 = 1550 cm−1. Spectrum (v) shows a measurement taken from a single gold nanoparticle at position (v) shown in panel a for comparison with the SERS spectra obtained from nanoparticle dimers.
of 2 × 106 in the center. Additionally, the calculations reveal that the |E|4 enhancement varies by a factor of 2 for a gap size between 5 and 7 nm (which is expected for individual nanoparticle dimers according to TEM analysis). This factor of 2 agrees very well with the experimentally observed variation of the peak intensities between SERS measurements on different dimer structures as shown in Figure 2e. Using DNA origami as a method to generate plasmonic nanoantennas for Raman spectroscopy bears the risk that an unwanted background peak from the DNA might contribute to the measured spectrum. We therefore performed control experiments on origami-antennas that were not labeled with any dye to analyze the level of background contribution and its potential limitation for the DNA origami approach. An example for a spectrum of a plain origami dimer is shown in Figure S8a in the Supporting Information. Three main peaks at 998, 1087, and 1587 cm−1 and smaller Raman shifts at 759, 1028, and 1129 cm−1 were observed. These spectral bands can be assigned to the thymine nucleotides of the ssDNA strand that is bound to the nanoparticles (759, 998, 1029 cm−1),42 the conjugate Adenine binding sequence on the origami sheet (1587 cm−1),43 and the phosphodioxy- (PO2−) band of the DNA backbone (1087 cm−1).42,43 The main occurrence of thymine peaks is likely observed because the poly-T strands covering the complete nanoparticle surface where the |E4| enhancement is also strong (Supporting Information Figure S7). Notably, none of the Raman bands of the DNA background were observed in the SYBR Gold spectra shown in Figure 2. This can be explained because the measurements on the dye were performed with lower laser intensity. A Raman signal from DNA was only observed when the laser power was increased by at least a factor of 4 which corresponds to a laser power density of ∼9 kW/cm2. The dye analyte therefore showed a much stronger enhancement, likely because of a larger scattering cross
selectively incorporated into the origami block between the particles. We used SYBR Gold, a minor groove-binding fluorescent nucleic acid stain that has a high affinity to double-stranded DNA. In our experiments, we expect a ratio of at least 1 molecule per 20 base pairs to label the DNA block if it is incubated with stoichiometric amounts of dye molecules. The measurement was performed using an excitation laser wavelength of 568 nm in order to match the plasmon resonance of the gold nanoparticle dimers. The SERS spectra obtained from the individual AuNP dimers shown in Figure 2a are displayed in Figure 2e. We could clearly attribute the Raman peaks Λ1−Λ4 to the SYBR Gold molecules by comparing the data with the spectrum of a highly concentrated bulk solution. A spectrum taken from a single particle (Figure 2e (v)) shows that the SYBR Gold peaks that are observed for the dimer structure are missing. Only a small peak at Λ2 = 1365 cm−1 and a broad peak at ΛBG = 920 cm−1 are observed. The broad 920 cm−1 peak was found also for control measurements that were done on the same substrate but far away from any particles. A Raman band at this wavenumber, however, is characteristic of phosphate and thus likely originates from molecular residuals from the buffer solution which was mainly phosphate buffer saline (PBS).41 As already mentioned, the strongest SERS enhancement is expected from molecules that are located precisely at the hot spot between the two gold nanoparticles. We performed finitedifference time-domain (FDTD) calculations to estimate both, the size of the hot spot region and the expected |E|4 enhancement (Supporting Information Figure 7). From the estimated size of the hot spot, we concluded that approximately 25 dye molecules are located in the gap region. This yields to a mean SERS enhancement factor (EF) of 3.1 × 105 for the 1365 cm−1 peak. This value also compares well to FDTD calculations that yield an averaged |E|4 enhancement of 1.4 × 105 over the whole hot spot region and an enhancement 2916
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Figure 3. The SERS intensity of the 1365 cm−1 Raman peak is depending on the polarization orientation of the exciting laser. (a) SEM images of individual DNA-assembled AuNP dimers. (b) SERS peak height at 1365 cm−1 extracted from Raman spectra that were taken at different relative polarization orientations of the exciting laser. (c) SERS spectra taken at a laser polarization parallel and perpendicular to the gold dimer axis.
the analyte with respect to the dimer axis48 (Supporting Information Figure S9). A SERS spectrum of SYBR Gold for both, parallel and perpendicular orientation of the laser light with respect to the nanoparticle dimer axis is shown in Figure 3c. When the laser polarization is aligned to the dimer, the field enhancement in the particle gap, and accordingly the SERS enhancement, reaches its maximum. On the opposite, at perpendicular orientation the SERS effect is at a minimum. These results agree well with the picture of the polarization-dependent plasmonic response of the coupled dimer, which was found in the scattering spectra (Figure 2d). This illustrates the importance of aligning the exciting laser polarization with the dimer long axis in order to achieve the maximum field enhancement and the strongest SERS signal intensity. Also, the signal intensity was reaching its initial values after a full measurement over 180°, which again confirms the long-term stability of the origami structure. Overall, the strategy to use DNA origami for the synthesis of plasmon coupled nanoantennas expands the applicability for sensor applications based on SERS detection. DNA selfassembly represents a reliable fabrication method to create probes of strongly coupled nanoparticle dimers with a wellcontrolled geometry and separation distance at the nanoscale. A DNA-nanoantenna design that spans the nanoparticle gap as demonstrated here also provides an addressable scaffold for delivering functional molecules precisely to the hot spot region located at the center between the two closely apposed particles and at the same time improves the rigidity and stability of the origami structure to prevent sample degradation during the measurement. Importantly, the sequence-specific addressability of DNA origami itself may be used as a template to locate certain molecules of interest via specific binding precisely at the hot spot region. DNA origami structures potentially carry multiple, sequence-defined binding sites where a wide variety of (bio)molecules can be attached. This may allow to specifically target molecules in solution or potentially inside living cells. This feature marks a clear advantage compared to other methods that rely on random adsorption of molecules to the nanoantenna gap.
section of the dye molecules compared to DNA. No background signal was observed when the unlabeled origami was measured with the same integration time and laser power density that were used for the measurements of SYBR Gold. For measurements conducted with sufficiently high laser intensities, however, the DNA background peaks might appear in the spectrum which makes a further peak analysis necessary. This has been tested for two other dyes (POPO3-Iodide and SYBR green) and is exemplarily shown in the Supporting Information, Figure S8b,c. In general, the use of low laser intensities is favorable for any Raman measurement on nanoparticle-origami samples because light absorbed by plasmonic particles is very efficiently converted into heat and temperature elevations of several hundred degrees Celsius can be reached within a few picoseconds. A strong heating could cause DNA melting and thus lead to a disassembly of the DNA origami.44,45 We observed that throughout the measurements on the origami dimer structures the SERS signal was homogeneous and stable. This indicates that the laser power used in our experiments is sufficiently low to prevent thermal degradation of the nanoantennas due to plasmonic heating. Only a small bleaching was observed after several minutes of laser exposure but SEM analysis of the sample afterward showed that the dimer structure was still intact and that the bleaching was solely caused by dye degradation. For a coupled gold nanoparticle dimer, Raman scattering is expected to be strongest along the dimer axis due to the strongest field enhancement in the particle gap. We investigated the impact of the polarization dependence of the SERS signal for the AuNP dimers in more detail as shown in Figure 3. The Λ2 = 1365 cm−1 peak height was evaluated for different excitation laser polarization orientations with respect to the dimer axis (Figure 3a,b). Each polarization-dependent measurement was performed on a single dimer structure with an integration time of 100 s for each data point. When comparing the absolute values of the peak height among the different hybrid structures for nonpolarized light, only small differences were observed. The polarization dependency of a SERS peak can be understood in the frame of the E4 model, which is a widely accepted explanation for the SERS effect.46,47 According to this model, the data in Figure 3b can be described by ISERS ∼ I⊥ cos4(α) + I∥ cos2(α)sin2(α), where α is the angle between the excitation light polarization and the dimer axis, and I⊥ and I∥ depend on the orientation of the associated Raman dipole of
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ASSOCIATED CONTENT
S Supporting Information *
Materials and methods and information about the DNA origami block structure, the gold nanoparticle attachment, 2917
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(17) Willets, K. A.; Van Duyne, R. P. Localized Surface Plasmon Resonance Spectroscopy and Sensing. Annu. Rev. Phys. Chem. 2007, 58, 267−297. (18) Camden, J. P.; et al. Probing the Structure of Single-Molecule Surface-Enhanced Raman Scattering Hot Spots. J. Am. Chem. Soc. 2008, 130, 12616−12617. (19) Kleinman, S. L.; Frontiera, R. R.; Henry, A.-I.; Dieringer, J. A.; Van Duyne, R. P. Creating, characterizing, and controlling chemistry with SERS hot spots. Phys. Chem. Chem. Phys. 2013, 15, 21. (20) Lal, S.; Link, S.; Halas, N. J. Nano-optics from sensing to waveguiding. Nat. Photonics 2007, 1, 641−648. (21) Anker, J. N.; et al. Biosensing with plasmonic nanosensors. Nat. Mater. 2008, 7, 442−453. (22) Ringler, M.; et al. Moving Nanoparticles with Raman Scattering. Nano Lett. 2007, 7, 2753−2757. (23) Chen, J. H.; Seeman, N. C. Synthesis from DNA of a molecule with the connectivity of a cube. Nature 1991, 350, 631−633. (24) Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 2006, 440, 297−302. (25) Douglas, S. M.; et al. Self-assembly of DNA into nanoscale three-dimensional shapes. Nature 2009, 459, 414−418. (26) Seeman, N. C. Nanomaterials Based on DNA. Annu. Rev. Biochem. 2010, 79, 65−87. (27) Nykypanchuk, D.; Maye, M. M.; Van der Lelie, D.; Gang, O. DNA-guided crystallization of colloidal nanoparticles. Nature 2008, 451, 549−552. (28) Alivisatos, A. P.; et al. Organization of “nanocrystal molecules” using DNA. Nature 1996, 382, 609−611. (29) Xu, X.; Rosi, N. L.; Wang, Y.; Huo, F.; Mirkin, C. A. Asymmetric Functionalization of Gold Nanoparticles with Oligonucleotides. J. Am. Chem. Soc. 2006, 128, 9286−9287. (30) Zheng, J.; et al. Two-Dimensional Nanoparticle Arrays Show the Organizational Power of Robust DNA Motifs. Nano Lett. 2006, 6, 1502−1504. (31) Chen, Y.; Cheng, W. DNA-based plasmonic nanoarchitectures: from structural design to emerging applications. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology 2012, 4, 587−604. (32) Ding, B.; et al. Gold Nanoparticle Self-Similar Chain Structure Organized by DNA Origami. J. Am. Chem. Soc. 2010, 132, 3248−3249. (33) Fan, J. A.; et al. Self-Assembled Plasmonic Nanoparticle Clusters. Science 2010, 328, 1135−1138. (34) Kuzyk, A.; et al. DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response. Nature 2012, 483, 311− 314. (35) Mastroianni, A. J.; Claridge, S. A.; Alivisatos, A. P. Pyramidal and Chiral Groupings of Gold Nanocrystals Assembled Using DNA Scaffolds. J. Am. Chem. Soc. 2009, 131, 8455−8459. (36) Shen, X.; et al. Rolling Up Gold Nanoparticle-Dressed DNA Origami into Three-Dimensional Plasmonic Chiral Nanostructures. J. Am. Chem. Soc. 2012, 134, 146−149. (37) Schmied, J. J.; et al. DNA Origami Nanopillars as Standards for Three-Dimensional Superresolution Microscopy. Nano Lett. 2013, 13, 781−785. (38) Acuna, G. P.; et al. Fluorescence Enhancement at Docking Sites of DNA-Directed Self-Assembled Nanoantennas. Science 2012, 338, 506−510. (39) Stein, I. H.; Schüller, V.; Böhm, P.; Tinnefeld, P.; Liedl, T. Single-Molecule FRET Ruler Based on Rigid DNA Origami Blocks. ChemPhysChem 2011, 12, 689−695. (40) McMahon, J. M.; et al. Gold nanoparticle dimer plasmonics: finite element method calculations of the electromagnetic enhancement to surface-enhanced Raman spectroscopy. Anal. Bioanal. Chem. 2009, 394, 1819−1825. (41) Pye, C. C.; Rudolph, W. W. An ab Initio, Infrared, and Raman Investigation of Phosphate Ion Hydration. J. Phys. Chem. A 2003, 107, 8746−8755. (42) Movileanu, L.; Benevides, J. M.; Thomas, G. J. Temperature dependence of the raman spectrum of DNA. Part IRaman
nanogap size, gel electrophoresis data, Mie and FDTD calculations, and further SERS measurements of additional analytes. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail: [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. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors thank Dr. Lidiya Osinkina and Dr. Frank Jäckel for helpful discussions. Financial support by the ERC through the Advanced Investigator Grant HYMEM, by the DFG through the Nanosystems Initiative Munich (NIM) and through the Sonderforschungsbereich (SFB1032), project A6 and A8, and by the Volkswagen Foundation is gratefully acknowledged.
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