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Fluorescence and Energy Transfer in Dye-Labeled DNA Crystals Joseph S. Melinger, Ruojie Sha, Chengde Mao, Nadrian C. Seeman, and Mario G. Ancona J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.6b09385 • Publication Date (Web): 07 Nov 2016 Downloaded from http://pubs.acs.org on November 10, 2016

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The Journal of Physical Chemistry

Fluorescence and Energy Transfer in Dye-Labeled DNA Crystals

Joseph S. Melinger1,*, Ruojie Sha2, Chengde Mao3, Nadrian C. Seeman2, and Mario G. Ancona1,**

1

Electronics Science and Technology Division, Naval Research Laboratory, Washington DC, 20375

2

Department of Chemistry, New York University, New York, NY 10003

3

Department of Chemistry, Purdue University, West Lafayette, IN 47907

Supporting Information ABSTRACT: DNA crystals make it possible to organize guest molecules into specific periodic 3D patterns at the nanoscale, and thereby to create novel macroscopic objects with potentially useful functionality. Here, we describe the fluorescence and energy transfer properties of DNA crystals that are self assembled from DNA tensegrity triangles with covalently attached Cy3 and Cy5 dyes. When compared to reference DNA strands in solution, the fluorescence measurements indicate that the dyes in the crystal experience a more homogenous environment, resulting in a two-fold increase in Cy3 quantum yield and single-exponential Cy3 fluorescence decays. Energy transfer in a network of coupled Cy3 and Cy5 dyes in the DNA crystal is demonstrated experimentally. Numerical simulation finds the experiments to be consistent with a Förster model of the dyes in the periodic crystalline environment, and particularly if the transition dipoles are assumed random in orientation but static on the time scale of the excitation decay.

Introduction Structural DNA nanotechnology has demonstrated the ability to control the structure of matter on the nanometer scale and is anticipated to help create new nanomaterials for di1 verse applications . As one area of potential use, DNA nanostructures can provide addressable scaffolds for organizing chromophores (e.g., organic dyes) into networks that mimic biological light harvesting complexes. Recent examples of such DNA-organized dye networks are photonic 2,3 4,5 wires , stars and dendritic assemblies , and DNA con6 7 structs including 7-helix bundles and other structures . While all of these designs show promise for synthetic light harvesting, they tend to be inefficient because of “disorder”

arising from the flexibility of the DNA scaffold, variations in the dye positions and orientations, poor formation efficiency, etc. In hopes of combating these deficiencies, we consider here the use of a more rigid scaffold in the form of a DNA self assembled crystal based on the tensegrity triangle DNA mo8 tif . We focus on measuring, modeling, and understanding the fluorescence and energy transfers that occur in these crystal-based dye networks, but it might well be that such assemblies could ultimately have value for photonic applica9 tions, especially given their large size . Results and Discussion In 2010, Wang et al. reported on the self-assembly of DNA crystals containing the cyanine dyes, Cy3 and Cy5, covalently 10 attached to the DNA scaffold . The underlying unit cell consisted of a pair of tensegrity triangles A and B as shown in Fig. 1, and these self-assembled to form a rhombohedral lattice, with an A triangle on one end of each edge of the unit cell and a B triangle on the other end. When the A and B triangles were functionalized (or not) with Cy3 and Cy5 dyes, respectively, the crystals were found to be colored, with pink crystals produced from the Cy3-A+B design; blue crystals from A+Cy5-B, and purple crystals from A-Cy3+B-Cy5. Synchrotron X-ray diffraction of these crystals verified their rhombohedral arrangement as well as determined various 10 structural properties . In the present paper we build on the earlier work by characterizing the fluorescence properties of dye-labeled DNA crystals when just a single dye type is present, and looking at the fluorescence resonance energy transfer (FRET) that occurs in crystals containing both Cy3 and Cy5 dyes. The DNA crystals used here are much like those in Ref. 10 and are again based on tensegrity triangle pairs as shown in Fig. 1a. Each triangle

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is composed of seven DNA strands that intertwine as double helices in an “over and under” motif to provide a comparatively rigid building block. The triangles are paired using sticky ends designed so that an A triangle can bind only to a B triangle and vice versa, thus producing the A-B pairs of Fig. 1a. In the original work, a “symmetric” design was used with each side of the triangle having identical sequences so that of the seven component strands only three were unique. This arrangement improves yield (and lowers cost), but it also implies that if some strands are dye-labeled, the crystal will form a random “alloy” with no control over which side of any given triangle is functionalized with the dye. In order to avoid this type of disorder, here we employed an “asymmetric” design in which all seven strands have unique sequences so that the dye locations become fully specified. One other difference from the earlier work is that previously the dyes were covalently attached to the central DNA strand of the triangle at the 5’ end via a 6-carbon linker. Instead, here we attach the dyes internally to the central strand using double phosphate linkage chemistry (Fig. S1a). When Cy3 is included in a given crystal, it is always in triangle A while Cy5 is always in triangle B, as shown in Fig. 1a. And because of the “asymmetric” design these dye locations are unique.

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fluorescence and picosecond time-resolved fluorescence. The fluorescent properties of crystals containing only a single dye type are discussed first. Fig. 2a compares steady state fluorescence spectra of the crystal Cy3-A+B with that of the central DNA triangle strand labeled with Cy3 in solution at ca. 1µM. The latter provides a reference spectrum corresponding to an “isolated” Cy3. In each case the excitation wavelength was 515 nm which selectively excites the Cy3. The fluorescence band shapes for the reference and crystal are similar, though the crystal spectrum is red-shifted by 6-7 nanometers. This red shift is due to partial re-absorption of the blue edge of the crystal fluorescence that overlaps with the optically dense Cy3 absorption band. To substantiate this explanation, a dilute Cy3-A+B crystal with only 1 in 64 unit cells containing a Cy3, was found to produce a spectrum nearly co-incident with the reference spectrum (see Fig. 2a). Thus, this basic experiment gives a first indication that the DNA crystal does not contain dyes that are aggregated, nor are they interacting in any way that distorts the fluorescence band shape.

Figure 1. a) Schematic of the two-triangle tensegrity unit showing the sequences for the seven unique DNA strands in each triangle and the placement of the dyes. Each arm of a triangle is terminated with sticky ends to bind only to the complementary triangle. b) Optical micrographs of the two types of crystals studied: Cy3-A+B and Cy3A+Cy5-B. The white scale bar indicates 100 microns.

As in Ref. 10, when the dye-labeled DNA is self-assembled into crystals, those containing only Cy3 dyes (Cy3-A+B) are colored pink, while those containing both dyes, Cy3-A+Cy5B, are purple, as shown in the optical micrographs of Fig. 1b and Fig. S1b. The size of the Cy3-A+Cy5-B crystals varied between 25-50µm, which is smaller than the ca. 100-200 µm crystals produced in Ref. 10. This is presumed due to the more complicated asymmetric design and to possible perturbations to the triangle geometry introduced by the internal double phosphate linkage of the dyes.

Figure 2. a) Steady state fluorescence spectra of the central DNA strand of a triangle molecule containing Cy3 (black curve), the Cy3A+B crystal (blue curve), and a diluted Cy3-A+B crystal, where 1 of 64 triangle units contains a Cy3 (red curve). b) Time resolved fluorescence of the central DNA strand containing Cy3 (gray curve) and the Cy3-A+B crystal with full labeling (black curve). The red curves are fits to the data described in the text. In each case the χ2 value was less than 1.2.

The spectroscopic characterization of the dye-labeled DNA crystals was performed using a combination of steady state

Fig. 2b shows time-resolved Cy3 fluorescence following excitation with a 532 nm picosecond (8 ps, FWHM) laser pulse,


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and the time constants are collected in Table 1. The fluorescence decay of the Cy3 doubly linked to a DNA oligo is highly 11, 12 non-exponential as has been reported previously . As in Ref. 11, fitting the response requires a sum of three exponential functions, with the longest time constant being 2.0 ns and the average being 0.90 ns (see Table S1). This behavior is believed to originate from a non-radiative pathway associated with Cy3 photo-isomerization and that varies with the 11-13 local environment . In contrast, the Cy3 fluorescence decay from the Cy3-A+B crystal is found to be well described by a single exponential function (see Fig. 2b) with a decay constant (2.0 ns, see Table 1 and Table S1) that is approximately double that for the Cy3-labeled DNA strand. This implies a fluorescence quantum yield that is correspondingly doubled (see Table 1), assuming that the Cy3 radiative lifetime in the crystal is the same as in solution. That a pure exponential decay is seen implies that the Cy3 experiences a more uniform environment in the crystal, and that the lifetime is approximately the same as the longest decay component of the Cy3-DNA oligo case (see Table S1) suggests that the crystal environment is suppressing the photo-isomerization pathway. In keeping with the modeling of Ref. 11, it is likely that this results from the DNA in the crystal being much more constrained and less able to bend or accommodate dye intercalation. In contrast, the Cy5 decay is nearly pure exponential whether in solution or in the crystal, and in both cases has essentially the same time constant (Fig. S2), findings that are consistent with a slower photo-isomerization pathway for 14 this dye . Lastly, these observations support the idea that both the Cy3 and Cy5 crystals are small enough in their critical dimension to still be considered optically thin. Based on the DNA design, the closest Cy3-Cy5 separations in our crystals are approximately 50Å. This distance is close to 12,15 reported Förster radii in the 54-60 Å range , and so we expect significant energy transfer between these dyes via the Förster mechanism (dipole-dipole coupling). FRET from a single Cy3-A+Cy5-B crystal is shown in Fig. 3a. In the steady state, selective excitation of Cy3 at 515 nm produces strong Cy5 fluorescence which suggests energy transfer from the initially excited Cy3 to Cy5. One way of quantifying the energy transfer efficiency is to compare with a calibrated Cy3A+B crystal under identical conditions of excitation, dye concentration, and fluorescence collection. However, this is difficult to achieve and so we instead rely on the fluorescence decays of a control Cy3-A+B sample, the Cy3 donor in Cy3A+Cy5-B (detection at 575 nm), and the Cy5 induction in Cy3-A+Cy5-B (detection at 675 nm) as shown in Fig. 3b. The time constants based on fitting the curves to a multiexponential function are collected in Table 1 and Table S1. The Cy3 decay shortens from 2.0 ns in Cy3-A+B to 0.55 ns in Cy3A+Cy5-B, and the complementary induction of Cy5 fluorescence (rise time ~ 0.34 ns; decay time ~ 1.6ns) confirms that the observed dynamics are due to FRET and not some other photophysical process. Using the relationship 1 ⁄ , where is the lifetime of the donor in the presence of the acceptor (in Cy3-A+Cy5-B), and is the lifetime of the donor in the donor-only control (Cy3-A+B), the FRET efficiency of the Cy3-A+Cy5-B crystal is then estimated to be 0.72, using values from Table 1.

Figure 3. a) Fluorescence spectrum of a single Cy3-A+Cy5B crystal from selective excitation of Cy3 at 515 nm. b) Time resolved fluorescence of Cy3-A+Cy5-B crystals following selective excitation of Cy3 with a picosecond laser at 532 nm. The blue curve is the donor Cy3 response from Cy3-A+B. The black curve is the Cy3 donor decay in Cy3-A+Cy5-B. The green curve is the Cy5 acceptor in Cy3-A+Cy5-B. The red curves are fits to the data using a multiexponential function. In each case the χ2 value was less than 1.2.

To aid in understanding the energy transfers in the Cy3A+Cy5-B DNA crystals we performed simulations that considered the periodic network of coupled dyes in the crystal (Figs. S3a and S3b) and assumed Förster coupling (see the SI for complete details). These simulations (Figs. S4-S8) included both homoFRET (between like dyes) and heteroFRET (between Cy3s and Cy5s). Also, since the simulations were necessarily finite in size whereas the experiment is effectively infinite, care had to be taken to ensure that the simulations are large enough that edge effects are negligible. Initial simulations assumed ideal rhombohedral geometry, dynamic (i.e., 〈 〉 2⁄3) or static dipoles with an isotropic distribu16 tion , and with the Förster radii taken to be elevated over the values cited earlier by the enhanced donor quantum yield. Support for the static dipole assumption comes from measurements (see Fig. S9) on a Cy3-A + B crystal that find the fluorescence anisotropy levels off to a constant value following homoFRET, rather than relaxing to zero anisotropy, as would be the case if there were significant dye motion on the excited state timescale. Consistency of simulation and experiment was then assessed by seeing whether good agreement could be achieved with plausibly small adjustments of the model parameters.



Cy5) = 62Å, the static dipole model, and that in 10% of the crystal the Cy5 dye is absent.

SUMMARY AND CONCLUSIONS

Figure 4. Comparison of experiment (points) and simulation (lines) of FRET in the Cy3-A+Cy5-B crystal. The simulation assumes R0(Cy3Cy5) = 62Å and the dipoles are treated in the dynamic (dashed) or static (solid) limits. The inset gives a semi-long version of the plot.

Figure 4 compares the experimental time-resolved fluorescence shown in Fig. 3b with Förster simulations assuming R0(Cy3-Cy5)= 62Å. Both the dynamic and static dipole limits do well in matching the Cy5 emission, but as emphasized by the inset neither is adequate with regard to the donor emission, though clearly the static dipole treatment does better. Significantly improved agreement (Figs. S5 and S6) for the Cy3 emission is obtained in the static limit if one lowers R0 to 52Å, however, the Cy5 agreement is less good and the long Cy3 emission tail is still inadequately captured This circumstance led us to consider alternative scenarios, and one that does quite well (see Fig. 5) is to assume that there are small regions (~10%) of the Cy3-A+Cy5 crystal, perhaps at the surfaces, that are missing most of the Cy5 dyes. While obviously speculative, this scenario seems plausible in that regions of missing Cy5 near the crystal surface could occur during the crystal growth or as a result of photobleaching, (see the SI and Fig. S10 for further discussion).

In summary, we have characterized the fluorescence and FRET properties of DNA crystals with dyes that are covalently attached to DNA tensegrity triangle building blocks. Timeresolved fluorescence experiments show that the Cy3 dyes in the crystal exist in a more homogeneous environment than when attached to the same DNA strand, but in random solution. The Cy3 fluorescence intensity increased two-fold in the crystal, and we argue that this is because the crystal environment holds the dye rigidly thereby suppressing excitedstate isomerization. It seems likely that other cyanine dyes that undergo efficient excited state isomerization about the methine bridge would also show similarly elevated fluorescence in DNA crystals, whereas more rigid dyes (e.g., rhodamines) would not be expected to show this behavior. FRET between the Cy3 and Cy5 dyes in the full network was demonstrated with an efficiency of 0.72. Using numerical simulation, these experiments were shown to be consistent with a Forster model, and particularly if the dipoles are assumed randomly oriented but static (at least on the FRET timescale). Overall, the ability of the DNA tensegrity crystals to control dye placement, density, attachment chemistry, and, possibly, orientation make them attractive for research and engineering on dye assemblies for photonics applications such as to light-harvesting. *

Table 1. Fluorescence and FRET Constants.

1

static dipoles Emission Cy3, Cy5 (norm)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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R = 62Å

QY

τCy3 (ns)

τCy5 rise/decay (ns)

EFRET

Cy3-DNA oligo

0.28

0.90

-

-

Cy3-A+B xtal

0.60

2.0

-

-

Cy5-DNA oligo

0.27

-

2.0

-

A+Cy5-B xtal

0.27

-

2.0

-

Cy3-A+Cy5-B xtal

-

0.55

0.34/1.8

0.72

†

†

*

The time constants are based on the multiexponential fitting parameters collected in Table S1.

0

**

0.1

EFRET is the FRET efficiency based on the donor decay.

Cy5

†

The values of QY from the crystals are determined by comparison to the measured QY of the dye attached to dsDNA in solution, and assuming that the radiative decay rate of the dye in solution and in the crystal is the same.

Cy3 0.01

Experimental Methods

10% Cy3 only 0.001

**

Sample

0

1

2

3

4

5

6

7

time (ns) Figure 5. Comparison of experiment (points) and simulation (lines) of FRET in the Cy3-A+Cy5-B crystal. The simulation assumes R0(Cy3-

Synthesis, Purification and Crystallization. DNA sequences were designed using the program in Ref. 10, including Cy3 and Cy5 (Glen Research) derivatives (see Fig. S1a), and were synthesized by standard phosphoramidite techniques on an Applied Biosystems 394 DNA synthesizer. The strands were purified by denaturing PAGE. The asymmetric triangles A and B were separately annealed at 6 µM concentration in 1X TAE/Mg buffer by an established annealing pro-


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cedure (5 min at 90 °C, 15 min at 65 °C, 15 min at 37 °C and 20 min at RT). A volume of 6 µL of each of the annealed Triangle A and B complexes were mixed with 8 µL buffer containing 125 mM magnesium acetate, 50 mM HEPES (pH 7.0), and 10% 2-methyl-2,4-pentanediol (MPD) to form a 20 µL sitting drop, equilibrated against a 0.5 ml reservoir of 1.4 M ammonium sulphate for two weeks at RT, during which the volume of the drop diminished by about 90%. Native, Cy3 & Cy5derivative crystals (see Fig. 1b and Fig. S1b) were all produced under identical conditions. The native crystals can be quite large, but when dyes are incorporated their sizes tend to be no larger than about 100µm in their largest dimension and take the form of “flat” rhombohedra. In no instances were any macroscopic-sized crystals without color observed in setups of A and B molecules derivatized with either Cy3 and/or Cy5. Steady State Fluorescence. Fluorescence spectra of individual single DNA crystals were measured by coupling the 515 nm line of an argon-ion laser into the back port of a Zeiss Axiovert microscope and focusing the light onto the crystal surface with a 100 X objective (NA = 1.3). This wavelength excites the first absorption shoulder to the blue side of the Cy3 absorption maximum near 555 nm. The Cy5 absorption is relatively small at this wavelength. DNA crystals were extracted from their mother liquor using a micro loop and then placed into one of the sample wells of an eight-chamber tray (Lab-Tek) containing the same buffer used to grow the crystals. Care was taken to attenuate the laser sufficiently so that significant photobleaching, taken as a reduction in fluorescence intensity of more than 10% of the cyanine dyes, was not observed over the course of the measurement. The cyanine dye fluorescence that emerged from the microscope exit port was focused into an optical fiber spectrometer (Ocean Optics). Fluorescence spectra were then acquired over an integration time of 10 seconds. Typically, the crystals would be resting on the floor of the well with the light path crossing the thinnest dimension; uniformity was verified by collecting a set of fluorescence spectra with the laser focused at different points on the crystal surface. Fluorescence spectra were collected for both Cy3-A+B and Cy3-A+Cy5-B crystals. As references, the same microscope and spectrometer setup were also used to obtain spectra for dilute solutions of the central DNA strand labeled with either the Cy3 or Cy5 dye (~1 µM concentration in buffer solution). The fluorescence quantum yield (QY) of the DNA strand containing the Cy3 was measured using a Varian Eclipse spectrometer in a 90 degree excitation/detection geometry, and with a peak optical density smaller than 0.1. The Cy3 fluorescence intensity was referenced to Rhodamine B in 17 ethanol (QY = 0.68) . This procedure led to a QY = 0.28±0.02 for the Cy3-labeled DNA strand in buffer solution. Time Resolved Fluorescence. The fluorescence lifetimes and FRET dynamics of the dye-labeled DNA crystals were measured using the time-correlated single photon counting (TCSPC) technique. The experiment employed either a frequency-doubled diode-pumped Nd:YVO4 laser (High-Q picoTRAIN) at 532 nm (to selectively excite Cy3), with a pulsewidth of 7ps (FWHM) and a repetition rate of 80MHz, or a cavity-dumped dye laser operating near 600 nm with a pulse width of 1 ps, and at a repetition rate of 8 MHz. For this measurement a collection of crystals (typically more than 20) were extracted from the mother liquor and then

transferred into a column of buffer solution residing at the bottom of a glass pipet tube (approximately 1mm in diameter) such that the crystals were suspended in the buffer. The pipet tube was sealed at the top to prevent the liquid containing the crystals at the bottom from leaking out. The laser beam was defocused to fully illuminate the glass tube containing the suspended crystals. The laser was sufficiently attenuated to avoid significant photobleaching effects, as mentioned above. The fluorescence from the crystals passed through a polarizer set to the magic angle and then filtered using a monochromator. Fluorescence dynamics for Cy3 and Cy5 were measured at 575 nm and 675 nm, respectively. A micro channel plate photomultiplier tube (Hamamatsu) was used to detect the fluorescence and the single photon counting was performed using a Becker-Hickl SPC-630 card. An instrument response function (IRF) of approximately 45 ps (FWHM) was measured using scattered light from a scattering solution in the fluorescence cell. The reference solution of the central DNA strand containing Cy3 was measured in the same manner.

ASSOCIATED CONTENT Supporting Information Additional information and examples of dye-labeled DNA crystals are provided. Details related to the fitting and theoretical modeling of experimental measurements are also given.

AUTHOR INFORMATION Corresponding Author * **

[email protected] [email protected]

ACKNOWLEDGMENT J.S.M. and M.G.A. acknowledge support from the Naval Research Laboratory Nanoscience Institute, the Office of Naval Research, and the Laboratory-University Collaborative Initiative (LUCI). N.S. and R.S. acknowledge support from NSF/AFOSR ODISSEI-1332411, CCF-1526650 from the NSF, MURI W911NF-11-1-0024 from ARO, N000141110729 from ONR, DE-SC0007991 from DOE for DNA synthesis and partial salary support, and grant GBMF3849 from the Gordon and Betty Moore Foundation.

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Seeman, N. C. Structural DNA Nanotechnology. Cambridge University Press: Cambridge, U.K., 2016. (2) Hannestad, J. K.;, Sandin, P.; Albinsson, B. Self-Assembled DNA Photonic Wire for Long-Range Energy Transfer. J. Am. Chem. Soc. 2008, 130, 15889-15895. (3) Díaz, S. A.; Buckhout-White, S.; Ancona, M. G.; Spillmann C. M.; Goldman, E. R.; Melinger, J. S.; Medintz, I. L. FRET: Extending DNA-Based Molecular Photonic Wires with Homogeneous Förster Resonance Energy Transfer. Adv. Opt. Mat. 2016, 4, 339339. (4) Hemmig, E. A.; Creatore, C.; Wänsch, B.; Hecker, L.; Mair, P.; Parker, M. A.; Emmott, S.; Tinnefeld, P.; Keyser, U. F.; Chin, A. W. Programming Light-Harvesting Efficiency Using DNA Origami. Nano Lett. 2016, 16, 2369-2374. (5) Buckhout-White, S; Spillmann, C. M.; Algar, W. R.; Khachatrian, A.; Melinger, J. S.; Goldman, E. R.; Ancona, M. G.; Medintz,



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