DOI: 10.1002/chem.201501213
Communication
& Light Harvesting
DNA-Based Oligochromophores as Light-Harvesting Systems Philipp Ensslen,[a] Fabian Brandl,[b] Sabrina Sezi,[a] Reji Varghese,[a] Roger-Jan Kutta,[b] Bernhard Dick,[b] and Hans-Achim Wagenknecht*[a] Abstract: The chromophores ethynyl pyrene as blue, ethynyl perylene as green and ethynyl Nile red as red emitter were conjugated to the 5-position of 2’-deoxyuridine via an acetylene bridge. Using phosphoramidite chemistry on solid phase labelled DNA duplexes were prepared that bear single chromophore modifications, and binary and ternary combinations of these chromophore modifications. The steady-state and time-resolved fluorescence spectra of all three chromophores were studied in these modified DNA duplexes. An energy-transfer cascade occurs from ethynyl pyrene over ethynyl perylene to ethynyl Nile red and subsequently an electron-transfer cascade in the opposite direction (from ethynyl Nile red to ethynyl perylene or ethynyl pyrene, but not from ethynyl perylene to ethynyl pyrene). The electron-transfer processes finally provide charge separation. The efficiencies by these energy and electron-transfer processes can be tuned by the distances between the chromophores and the sequences. Most importantly, excitation at any wavelength between 350 and 700 nm finally leads to charge separated states which make these DNA samples promising candidates for light-harvesting systems.
The development of artificial antenna systems for collecting UV/Vis light requires the hierarchical organization of chromophores at the supramolecular level.[1–7] The arrangement of synthetic building blocks by self-assembly into structures with well-defined molecular geometries and chromophore distances allows control over various photophysical interactions.[1, 2, 5, 6] The regular topology of DNA including the double helical structure and the typical distance of approximately 3.4 æ between the base pairs offers a promising structural scaffold. Hence, it is not surprising that an increasing number of examples for DNA-based organization of p-conjugated chromophores have been published over recent years.[8–12] [a] Dipl.-Chem. P. Ensslen, Dr. S. Sezi, Dr. R. Varghese, Prof. Dr. H.-A. Wagenknecht Institute of Organic Chemistry, Karlsruhe Institute of Technology (KIT) Fritz-Haber-Weg 6, 76131 Karlsruhe (Germany) E-mail: [email protected] [b] F. Brandl, Dr. R.-J. Kutta, Prof. Dr. B. Dick Institute of Physical and Theoretical Chemistry, University of Regensburg Universittsstr. 31, 93053 Regensburg (Germany) Supporting information for this article is available on the WWW under http://dx.doi.org/10.1002/chem.201501213. Chem. Eur. J. 2015, 21, 9349 – 9354
Complex photophysical interactions of oligofluorosides that have been elucidated by a combinatorial approach yield a remarkable variety of emission colours at a single excitation wavelength.[9] The potential of energy-transfer cascades has successfully been demonstrated in the development of DNAbased photonic wires.[13] The key for success of such assemblies is the precise control of energy-transfer processes. DNAbased architectures offer the possibility to organize chromophores with spatial resolution on the nanometer scale so that artificial light-harvesting antennas should be obtainable.[14–17] It has been shown that excimer- and exciton-forming multichromophores based on the double-helical DNA scaffold are able to harvest photons.[15] In a recent approach, a self-assembled nanoscale DNA–porphyrin complex was embedded in membranes which allows light harvesting, too.[16] More complex structures including proteins have been achieved.[17] Based on the combination of two different fluorophores as DNA base modifications we presented a few years ago a white-light emitting DNA.[15] Moreover, we showed that pyrene- and Nile red-type DNA base modifications allow both the DNA-based (covalent)[18, 19] and the DNA-templated (noncovalent)[20] self-assembly to oligochromophoric structures. Herein, we show how to use the DNA-based architecture for the covalent arrangement of three different chromophores covering nearly the whole UV-A/Vis absorption range and provide the principal photophysical characteristics of a light-harvesting system. The major advantage of this approach is that the energy transfer (EnT) between the three chromophores is followed by electron-transfer (ElT) steps yielding a charge-separated state that is potentially useful for photocatalytic and other applications. The chromophores applied were ethynyl pyrene (Py) as the blue, ethynyl perylene (Pe) as the green and ethynyl Nile red (Nr) as the red emitter (Scheme 1). All three chromophores were conjugated to the 5-position of 2’-deoxyuridine via an acetylene bridge in order to maintain, at least partially, the canonical dU–A base pairing. Our recent results from the noncovalent, DNA-templated chromophore arrangements showed that specific binding between chromophore-modified 2’-deoxyuridines and 2’-deoxyadenosines as part of the counter-strand is required.[20] The phosphoramidites of 2’-deoxyuridine with Py or Pe are commercially available. The DNA building block of 2’deoxyuridine modified with ethynyl Nile red was synthesized according to our published procedure.[18, 19, 21] DNA1–DNA3 contain one of each chromophore as single modifications. In DNA4–DNA6 two of the chromophores were combined. Finally, all three chromophores are combined and placed either adjacent to each other in DNA7 and DNA10 or separated by one
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Communication (DNA8, DNA11) or two intervening A–T base pair (DNA9, DNA12). The two DNA sets differ only in the order of the chromophores which is either Py-Pe-Nr (DNA7–DNA9) or Py-Nr-Pe (DNA10–DNA12). All double-stranded DNA samples were characterized by their melting temperature, UV/Vis absorption (including melting temperatures), steady-state fluorescence spectroscopy and fluorescence lifetimes.
Table 1. Sequences and melting temperatures (Tm) of DNA1–DNA12; general sequence: 5’-GCAGTCAA-X-AACACTGA-3’. Sample
X
Tm [8C][a]
DTm [8C][b]
DNA1 DNA2 DNA3 DNA4 DNA5 DNA6 DNA7 DNA8 DNA9 DNA10 DNA11 DNA12
Py Pe Nr Py-Pe Py-Nr Pe-Nr Py-Pe-Nr Py-A-Pe-A-Nr Py-A-A-Pe-A-A-Nr Py-Nr-Pe Py-A-Nr-A-Pe Py-A-A-Nr-A-A-Pe
57.9 58.3 57.2 55.2 55.7 55.2 57.2 53.4 53.6 57.2 53.8 52.3
¢3.6 ¢3.2 ¢4.3 ¢6.9 ¢6.3 ¢6.8 ¢6.8 ¢8.7 ¢9.9 ¢6.1 ¢8.3 ¢11.2
[a] l = 260 nm, 20–90 8C, interval: 0.7 8C min¢1, 2.5 mm double-stranded DNA in 10 mm NaPi buffer (pH 7.0), 250 mm NaCl. [b] In comparison to the corresponding unmodified DNA duplex that contained thymines (T) instead of Py, Pe or Nr.
Scheme 1. Structures of modified nucleosides Py, Pe and Nr.
The melting temperatures of the single-modified double strands DNA1–DNA3 reflect a loss of stability of 3–4 8C that is typical for modifications at the 5-position of 2’-deoxyuridines in DNA (Table 1).[19] Accordingly, the melting temperatures of the twofold labelled DNA4–DNA6 decrease by 6–7 8C. In case of the threefold modified samples an additional DTm of ¢3– 4 8C for the third DNA base modification is only observed if the chromophores are separated by two intervening base pairs (DNA9 and DNA12). The loss of Tm is less than 3–4 8C per modification with only one intervening A–T base pair (DNA8 and DNA11) or even less in case of the duplexes with directly adjacent chromophores (DNA7 and DNA10). The latter result indicates stabilizing interactions between chromophores regaining some of the loss of thermal stability. The reference duplexes with single modifications, DNA1– DNA3, showed the characteristic optical behaviour of the corresponding chromophores (Figure 1, top). The major absorption bands at 380/400, 450/480 and 620 nm can be assigned to the presence of the chromophores Py, Pe or Nr, respectively, and should in principle allow selective excitation. A careful look, however, reveals that excitation of Py at 380 nm and Pe at 450 nm will not occur absolutely selectively since mainly Nr has a broad absorption in these ranges, too. This needs to be taken into consideration when steady-state and time-resolved fluorescence data are interpreted. Another careful look on the absorption of the threefold-modified DNA samples with directly adjacent chromophores (DNA7, Figure 1, bottom, and DNA10, Figure S13 in the Supporting Information) shows reduced extinction, red-shifted maxima for Py and Pe and a blue-shifted maximum for Nr, compared to the correspondChem. Eur. J. 2015, 21, 9349 – 9354
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ing duplexes with two intervening A–T base pairs, DNA9 and DNA12, respectively. Assuming that the chromophores in the latter two duplexes are well separated from each other, the mentioned absorption differences of DNA7 and DNA10 must be assigned to excitonic interactions between the chromophores. This interpretation tracks well with the previously described interpretation of the Tm results where we showed that the loss of duplex stability for DNA7 and DNA10 is less than three single modifications. In order to support the idea of excitonic interactions between the chromophores as DNA base modifications circular dichroism (CD) spectra of all duplexes were recorded between 200 and 700 nm, which includes the absorption range of DNA and of the three different chromophores (Figure 2). The CD spectra of all 12 duplexes between 200 and 300 nm can be assigned to the typical B-conformation. Obviously, the overall conformation of double-helical DNA is not significantly altered due to the attached chromophores. Significant CD signals in the chromophore absorption range (between 300 and 700 nm) can be observed only with those duplexes that bear two or three chromophores directly adjacent to each other, that means DNA4–DNA6, DNA7 and DNA10, and to a certain extent also DNA11. These CD signals can be assigned to excitonic interactions between the chromophores in these double strands. In contrast, the duplexes with one intervening base pair (DNA8) or with even two intervening base pairs (DNA9 and DNA12) between the chromophores serve as negative controls since they do not exhibit any significant CD signal between 350 and 700 nm. The same can be observed with the single-modified reference double strands DNA1–DNA3. In conclusion, the occurrence of excitonic interactions between directly adjacent chromophores was: 1) indicated in the Tm measurements, 2) observed in the absorption spectra, and 3) supported by the CD spectra. Interestingly, the two duplexes with one intervening base pair reveal a sequence dependence of these interactions since they behave quite differently; DNA11 shows excitonic interactions whereas DNA8 does not.
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Figure 1. UV/Vis absorption of DNA1–DNA3 (top) and DNA7–DNA9 (bottom); 2.5 mm double-stranded DNA in 10 mm NaPi buffer (pH 7.0), 250 mm NaCl. For DNA4–DNA6 and DNA10–DNA12 see Figure S13 in the Supporting Information.
All steady-state fluorescence was recorded under identical experimental conditions, in order to obtain full comparability. Fluorescence lifetimes were determined with time-resolved photon counting using a streak camera with a time resolution of about 50–70 ps and analysed by global lifetime analysis (Table 2, for the methodology, see the Supporting Information).[22] The single chromophores in DNA1–DNA3 exhibit their typical emissions at 445 (Py), 489/522 (Pe) and 668 nm (Nr) when excited at their characteristic wavelengths (as discussed above). The lifetime of Py* (in DNA1) is 0.52 ns and hence shorter compared to that of Pe* (in DNA2, 0.89 ns) and Nr* (in DNA3, 0.97 ns). The mono-exponential decays rules out the possibility of multiple conformations of these chromophores as covalent DNA modifications. DNA4–DNA6 allow the study of the three possible binary combinations of Py, Pe, and Nr (Figure 3, left), which is an important prerequisite for the subsequent interpretation of the spectroscopic data of threefold modified DNA7–DNA12. When DNA4 is excited at the Py-typical wavelength (380 nm), the steady-state fluorescence exhibits nearly quantitative quenching of the Py emission and significant Pe emission with a lifetime of 1.01 ns is obtained. Accordingly, we propose an efficient EnT from the Py to the Pe moiety in DNA4. The resulting Pe* lifetime is nearly the same as in the single-labelled reference DNA2 (0.89 ns) and rules out the possibility of an ElT from Pe* back to Py (that would quench the Pe* fluorescence). Chem. Eur. J. 2015, 21, 9349 – 9354
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Figure 2. CD spectra of DNA7–DNA9 (top) and DNA10–DNA12 (bottom); 2.5 mm double-stranded DNA in 10 mm NaPi buffer (pH 7.0), 250 mm NaCl. For DNA1–DNA3 and DNA4–DNA6, see Figure S15 in the Supporting Information.
Table 2. Fluorescence lifetime data from decay-associated spectra of DNA1–DNA12.
DNA1 DNA2 DNA3 DNA4 DNA5 DNA6 DNA7 DNA8 DNA9 DNA10 DNA11 DNA12
lexc = 380 nm (Py) t2 [ns] t1 [ns]
lexc = 450 nm (Pe) t1 [ns] t2 [ns]
lexc = 600 nm (Nr) t1 [ns]
0.52 – – 1.01 0.35 – 0.79 1.07 1.20 0.84 0.51 1.05
– 0.89 – 0.95 – 0.49 1.15 1.12 1.33 0.56 0.52 1.16
– – 0.97 – 0.60 – – 0.69 1.33 – 0.50 0.82
– – – – – – – 0.05 0.09 0.04 0.05 0.07
– – – – – – – – – – 0.05 0.05
In DNA5 and DNA6, however, the situation is different. When excited at the Py-typical wavelength (380 nm) or Pe-typical wavelength (455 nm), respectively, only small amounts of Nr emission are observed. Hence, at first glance an EnT from Py or
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Communication Pe to Nr in DNA5 or DNA6, respectively, seems to be unlikely. But the lifetime of Py* in DNA5 is shortened to 0.35 ps (compared to that of DNA1) and a weak dual fluorescence of Py* and Nr* is obtained which can only be explained by an EnT from Py* to Nr. The situation is comparable and only slightly different in DNA6. Upon excitation of Pe, the Pe* lifetime is shortened to 0.49 ns (compared to DNA2) due to an EnT to Nr, but the Nr* fluorescence is completely quenched indicating an efficient ElT back to Pe. Thus, the photophysical situation in both DNA5 and DNA6 could be explained in such a way that EnT occurs from Py* or Pe*, respectively, to Nr and is followed by an ElT from Nr back to Py or Pe, respectively. In order to support this interpretation, we compared DNA3 bearing the single Nr modification with DNA5 and DNA6. When excited at the Nrtypical wavelength 610 nm, the Figure 3. Fluorescence spectra of DNA1–DNA6 and DNA7—DNA9; 2.5 mm double-stranded DNA in 10 mm NaPi steady-state fluorescence of buffer (pH 7.0), 250 mm NaCl; top lexc = 380 nm, middle: lexc = 455 nm, bottom: lexc = 610 nm. For DNA10–DNA12 DNA5 is nearly completely see Figure S14 in the Supporting Information. quenched by ElT and that of DNA6 is completely quenched. The time-resolved data support this result. When excited at The Pe* lifetime is shortened in DNA10 and DNA11 (Py-Nr-Pe the Nr-typical wavelength, the Nr* lifetime in DNA5 is shortsequence) but not in DNA7–DNA9 (Py-Pe-Nr sequence). The ened by ElT to 0.60 ns (compared to 0.97 ns in the reference latter, unshortened lifetimes clearly rule out the occurrence of DNA3). In DNA6, the Nr* is too weak and does not allow the EnT from Pe* to Nr in these sequences. Moreover, it is known determination of a lifetime. In conclusion, for the binary chrofrom the binary Py-Pe combination in DNA4 (as described mophore combinations in DNA4–DNA6, the fluorescence studabove) that there is no ElT from Pe* to Py, hence the shorties revealed that EnT processes are occurring from Py!Pe, ened Pe* lifetimes in DNA10 and DNA11 can be assigned to Py!Nr and Pe!Nr, and ElT processes in the other direction, EnT processes from Pe* to Nr. The second Pe* lifetimes that from Nr!Pe and Nr!Py but not from Pe!Py. were observed especially in DNA11 and DNA12 reveal the rate With this knowledge about the binary chromophore combiof 0.05 ns for the EnT process from Pe* to Nr. These observed nations and the involved photophysical processes, the interdifferences between the sequences (Py-Pe-Nr vs. Py-Nr-Pe) pretation of the steady-state fluorescence and lifetime data of cannot be explained sufficiently here but must have their threefold labelled DNA7–DNA12 is very straightforward origin in the different relative orientation of the chromophores (DNA7–DNA9, Figure 3, right; DNA10–DNA12, Figure S14 in (as the differences in the CD spectra already implied). the Supporting Information). The EnT from Py* to Pe and to Nr It is important to mention that EnT processes (Py!Pe, Pe! in DNA7 and DNA10 is reflected by the shortened lifetime of Nr and Py!Nr) occur by a distance dependence that is proportional to r¢6, whereas ElT (from Nr!Pe and Nr!Py) exhibit Py* (upon excitation at 380 nm). Depending on the distance between Py* and Pe/Nr (vide infra) these EnT processes occur an exponential and thereby stronger distance dependence. with rates between 0.04 (DNA10) and 0.09 ns (DNA9). The Hence, the increasing distance between the three chromolonger lifetimes that were observed in these samples (around phores in the series DNA7-DNA8-DNA9 and DNA10-DNA111 ns) can probably be associated to a DNA conformation in DNA12 should primarily reflect these differences by increased which the chromophore does not undergo an EnT transfer effiacceptor fluorescence intensities of Pe and Nr in the steadyciently. With respect to Pe excitation at 450 nm a more destate spectra and less shortened lifetimes of Pe* and Nr* in the tailed look at the lifetime data reveals sequence differences. time-resolved data (Figure 4). In fact, the Nr* fluorescence inChem. Eur. J. 2015, 21, 9349 – 9354
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Communication pendence can also be observed by comparison of the Pe* lifetimes in the different series of duplexes, DNA7!DNA9 versus DNA10!DNA12. The EnT process from Pe* to Nr can only be seen over distances where the ElT in the opposite direction becomes too slow to compete and thereby does not quench the resulting Nr* emission. The occurrence of an increasing amount of acceptor (Nr*) emission intensity (in the steadystate spectra) as a result of EnT again indicates that (after EnT) the ElT processes from Nr* back to Pe becomes less inefficient with increasing distance. The combination of the chromophores Py, Pe and Nr attached to the DNA bases (rigidly attached by acetylene bridges) and the double helix of DNA as structural architecture yields multichromophore systems with promising photophysical properties. The absorption of the three combined chromophores covers nearly the whole UV-A/Vis range. An EnT cascade occurs from Py over Pe to Nr and ElT in the opposite direction (from Nr to Pe or Py) subsequently provides charge separation. The efficiencies by these processes can be tuned by the distance between the chromophores. Most importantly, excitation at any wavelength between 350 and 700 nm leads finally to charge-separated states that can be used potentially for chemical photocatalysis or other applications. Hence, we conclude that especially DNA7–DNA12 represents a proof-of concept that light-harvesting systems can be designed astonishingly simply by helical arrangement in DNA-based architectures. Figure 4. Top: representative spectrum showing the time-resolved fluorescence of DNA12. The most intense signal (380 nm) comes from the scattered laser light (and its reflection from the rear of the cuvette ~ 100 ps later). Py* shows a short fluorescence lifetime, Pe* and Nr* show a much longer fluorescence lifetime. Bottom: decay-associated spectra of DNA12. Positive amplitudes correspond to decay, negative amplitudes to a rise. The spectrum associated with the short lifetime (0.07 ns) shows a positive signal in the range of Py* emission, and a negative signal in range of Nr* emission. Thus, the EnT from Py can be easily seen. In contrast, the longer lifetime (1.05 ns, as documented in Table 2) does not correspond to the fluorescence of Py* (although this chromophore has been excited at 380 nm) but to the fluorescence of Pe* and Nr*, as evidenced by the positive signals of this decay-associated spectrum.
tensity increases significantly in both series of duplexes when the Nr chromophore is excited directly at 600 nm. Upon excitation of Nr (600 nm) in DNA7 and DNA10, the Nr* fluorescence is quenched completely as a result of an efficient ElT from Nr* to Pe over such short distances. This interpretation is supported by the Nr* fluorescence lifetimes of the DNA samples in which Pe is separated from Nr by one or two intervening A–T base pairs. In fact, with increasing distance in DNA8!DNA9 and DNA11!DNA12 the Nr* fluorescence lifetime increases. A more detailed look reveals that the Nr* lifetimes are shorter in DNA11/DNA12 compared to DNA8/DNA9 due to the neighbourhood of Py next to Nr in the sequence Py-Nr-Pe which opens an additional ElT channel. In the other direction, the Pe* fluorescence as an intermediate emission in the EnT cascades Py!Pe!Nr and acceptor emission in the row Py!Nr is intensified if DNA8/DNA9 and DNA11/DNA12 are excited at the Pytypical wavelength (380 nm). This difference in distance deChem. Eur. J. 2015, 21, 9349 – 9354
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Experimental Section All experimental details, including the syntheses and spectroscopy, are described in the Supporting Information.
Acknowledgements Financial support by the Karlsruhe School of Optics and Photonics (KSOP), Deutsche Forschungsgemeinschaft/GRK 1626 “Chemical Photocatalysis” and KIT is gratefully acknowledged. Keywords: electron transfer · energy transfer · fluorescence · helix · oligonucleotides
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Received: March 27, 2015 Published online on June 9, 2015
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& Light Harvesting
DNA-Based Oligochromophores as Light-Harvesting Systems Philipp Ensslen,[a] Fabian Brandl,[b] Sabrina Sezi,[a] Reji Varghese,[a] Roger-Jan Kutta,[b] Bernhard Dick,[b] and Hans-Achim Wagenknecht*[a] Abstract: The chromophores ethynyl pyrene as blue, ethynyl perylene as green and ethynyl Nile red as red emitter were conjugated to the 5-position of 2’-deoxyuridine via an acetylene bridge. Using phosphoramidite chemistry on solid phase labelled DNA duplexes were prepared that bear single chromophore modifications, and binary and ternary combinations of these chromophore modifications. The steady-state and time-resolved fluorescence spectra of all three chromophores were studied in these modified DNA duplexes. An energy-transfer cascade occurs from ethynyl pyrene over ethynyl perylene to ethynyl Nile red and subsequently an electron-transfer cascade in the opposite direction (from ethynyl Nile red to ethynyl perylene or ethynyl pyrene, but not from ethynyl perylene to ethynyl pyrene). The electron-transfer processes finally provide charge separation. The efficiencies by these energy and electron-transfer processes can be tuned by the distances between the chromophores and the sequences. Most importantly, excitation at any wavelength between 350 and 700 nm finally leads to charge separated states which make these DNA samples promising candidates for light-harvesting systems.
The development of artificial antenna systems for collecting UV/Vis light requires the hierarchical organization of chromophores at the supramolecular level.[1–7] The arrangement of synthetic building blocks by self-assembly into structures with well-defined molecular geometries and chromophore distances allows control over various photophysical interactions.[1, 2, 5, 6] The regular topology of DNA including the double helical structure and the typical distance of approximately 3.4 æ between the base pairs offers a promising structural scaffold. Hence, it is not surprising that an increasing number of examples for DNA-based organization of p-conjugated chromophores have been published over recent years.[8–12] [a] Dipl.-Chem. P. Ensslen, Dr. S. Sezi, Dr. R. Varghese, Prof. Dr. H.-A. Wagenknecht Institute of Organic Chemistry, Karlsruhe Institute of Technology (KIT) Fritz-Haber-Weg 6, 76131 Karlsruhe (Germany) E-mail: [email protected] [b] F. Brandl, Dr. R.-J. Kutta, Prof. Dr. B. Dick Institute of Physical and Theoretical Chemistry, University of Regensburg Universittsstr. 31, 93053 Regensburg (Germany) Supporting information for this article is available on the WWW under http://dx.doi.org/10.1002/chem.201501213. Chem. Eur. J. 2015, 21, 9349 – 9354
Complex photophysical interactions of oligofluorosides that have been elucidated by a combinatorial approach yield a remarkable variety of emission colours at a single excitation wavelength.[9] The potential of energy-transfer cascades has successfully been demonstrated in the development of DNAbased photonic wires.[13] The key for success of such assemblies is the precise control of energy-transfer processes. DNAbased architectures offer the possibility to organize chromophores with spatial resolution on the nanometer scale so that artificial light-harvesting antennas should be obtainable.[14–17] It has been shown that excimer- and exciton-forming multichromophores based on the double-helical DNA scaffold are able to harvest photons.[15] In a recent approach, a self-assembled nanoscale DNA–porphyrin complex was embedded in membranes which allows light harvesting, too.[16] More complex structures including proteins have been achieved.[17] Based on the combination of two different fluorophores as DNA base modifications we presented a few years ago a white-light emitting DNA.[15] Moreover, we showed that pyrene- and Nile red-type DNA base modifications allow both the DNA-based (covalent)[18, 19] and the DNA-templated (noncovalent)[20] self-assembly to oligochromophoric structures. Herein, we show how to use the DNA-based architecture for the covalent arrangement of three different chromophores covering nearly the whole UV-A/Vis absorption range and provide the principal photophysical characteristics of a light-harvesting system. The major advantage of this approach is that the energy transfer (EnT) between the three chromophores is followed by electron-transfer (ElT) steps yielding a charge-separated state that is potentially useful for photocatalytic and other applications. The chromophores applied were ethynyl pyrene (Py) as the blue, ethynyl perylene (Pe) as the green and ethynyl Nile red (Nr) as the red emitter (Scheme 1). All three chromophores were conjugated to the 5-position of 2’-deoxyuridine via an acetylene bridge in order to maintain, at least partially, the canonical dU–A base pairing. Our recent results from the noncovalent, DNA-templated chromophore arrangements showed that specific binding between chromophore-modified 2’-deoxyuridines and 2’-deoxyadenosines as part of the counter-strand is required.[20] The phosphoramidites of 2’-deoxyuridine with Py or Pe are commercially available. The DNA building block of 2’deoxyuridine modified with ethynyl Nile red was synthesized according to our published procedure.[18, 19, 21] DNA1–DNA3 contain one of each chromophore as single modifications. In DNA4–DNA6 two of the chromophores were combined. Finally, all three chromophores are combined and placed either adjacent to each other in DNA7 and DNA10 or separated by one
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Communication (DNA8, DNA11) or two intervening A–T base pair (DNA9, DNA12). The two DNA sets differ only in the order of the chromophores which is either Py-Pe-Nr (DNA7–DNA9) or Py-Nr-Pe (DNA10–DNA12). All double-stranded DNA samples were characterized by their melting temperature, UV/Vis absorption (including melting temperatures), steady-state fluorescence spectroscopy and fluorescence lifetimes.
Table 1. Sequences and melting temperatures (Tm) of DNA1–DNA12; general sequence: 5’-GCAGTCAA-X-AACACTGA-3’. Sample
X
Tm [8C][a]
DTm [8C][b]
DNA1 DNA2 DNA3 DNA4 DNA5 DNA6 DNA7 DNA8 DNA9 DNA10 DNA11 DNA12
Py Pe Nr Py-Pe Py-Nr Pe-Nr Py-Pe-Nr Py-A-Pe-A-Nr Py-A-A-Pe-A-A-Nr Py-Nr-Pe Py-A-Nr-A-Pe Py-A-A-Nr-A-A-Pe
57.9 58.3 57.2 55.2 55.7 55.2 57.2 53.4 53.6 57.2 53.8 52.3
¢3.6 ¢3.2 ¢4.3 ¢6.9 ¢6.3 ¢6.8 ¢6.8 ¢8.7 ¢9.9 ¢6.1 ¢8.3 ¢11.2
[a] l = 260 nm, 20–90 8C, interval: 0.7 8C min¢1, 2.5 mm double-stranded DNA in 10 mm NaPi buffer (pH 7.0), 250 mm NaCl. [b] In comparison to the corresponding unmodified DNA duplex that contained thymines (T) instead of Py, Pe or Nr.
Scheme 1. Structures of modified nucleosides Py, Pe and Nr.
The melting temperatures of the single-modified double strands DNA1–DNA3 reflect a loss of stability of 3–4 8C that is typical for modifications at the 5-position of 2’-deoxyuridines in DNA (Table 1).[19] Accordingly, the melting temperatures of the twofold labelled DNA4–DNA6 decrease by 6–7 8C. In case of the threefold modified samples an additional DTm of ¢3– 4 8C for the third DNA base modification is only observed if the chromophores are separated by two intervening base pairs (DNA9 and DNA12). The loss of Tm is less than 3–4 8C per modification with only one intervening A–T base pair (DNA8 and DNA11) or even less in case of the duplexes with directly adjacent chromophores (DNA7 and DNA10). The latter result indicates stabilizing interactions between chromophores regaining some of the loss of thermal stability. The reference duplexes with single modifications, DNA1– DNA3, showed the characteristic optical behaviour of the corresponding chromophores (Figure 1, top). The major absorption bands at 380/400, 450/480 and 620 nm can be assigned to the presence of the chromophores Py, Pe or Nr, respectively, and should in principle allow selective excitation. A careful look, however, reveals that excitation of Py at 380 nm and Pe at 450 nm will not occur absolutely selectively since mainly Nr has a broad absorption in these ranges, too. This needs to be taken into consideration when steady-state and time-resolved fluorescence data are interpreted. Another careful look on the absorption of the threefold-modified DNA samples with directly adjacent chromophores (DNA7, Figure 1, bottom, and DNA10, Figure S13 in the Supporting Information) shows reduced extinction, red-shifted maxima for Py and Pe and a blue-shifted maximum for Nr, compared to the correspondChem. Eur. J. 2015, 21, 9349 – 9354
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ing duplexes with two intervening A–T base pairs, DNA9 and DNA12, respectively. Assuming that the chromophores in the latter two duplexes are well separated from each other, the mentioned absorption differences of DNA7 and DNA10 must be assigned to excitonic interactions between the chromophores. This interpretation tracks well with the previously described interpretation of the Tm results where we showed that the loss of duplex stability for DNA7 and DNA10 is less than three single modifications. In order to support the idea of excitonic interactions between the chromophores as DNA base modifications circular dichroism (CD) spectra of all duplexes were recorded between 200 and 700 nm, which includes the absorption range of DNA and of the three different chromophores (Figure 2). The CD spectra of all 12 duplexes between 200 and 300 nm can be assigned to the typical B-conformation. Obviously, the overall conformation of double-helical DNA is not significantly altered due to the attached chromophores. Significant CD signals in the chromophore absorption range (between 300 and 700 nm) can be observed only with those duplexes that bear two or three chromophores directly adjacent to each other, that means DNA4–DNA6, DNA7 and DNA10, and to a certain extent also DNA11. These CD signals can be assigned to excitonic interactions between the chromophores in these double strands. In contrast, the duplexes with one intervening base pair (DNA8) or with even two intervening base pairs (DNA9 and DNA12) between the chromophores serve as negative controls since they do not exhibit any significant CD signal between 350 and 700 nm. The same can be observed with the single-modified reference double strands DNA1–DNA3. In conclusion, the occurrence of excitonic interactions between directly adjacent chromophores was: 1) indicated in the Tm measurements, 2) observed in the absorption spectra, and 3) supported by the CD spectra. Interestingly, the two duplexes with one intervening base pair reveal a sequence dependence of these interactions since they behave quite differently; DNA11 shows excitonic interactions whereas DNA8 does not.
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Figure 1. UV/Vis absorption of DNA1–DNA3 (top) and DNA7–DNA9 (bottom); 2.5 mm double-stranded DNA in 10 mm NaPi buffer (pH 7.0), 250 mm NaCl. For DNA4–DNA6 and DNA10–DNA12 see Figure S13 in the Supporting Information.
All steady-state fluorescence was recorded under identical experimental conditions, in order to obtain full comparability. Fluorescence lifetimes were determined with time-resolved photon counting using a streak camera with a time resolution of about 50–70 ps and analysed by global lifetime analysis (Table 2, for the methodology, see the Supporting Information).[22] The single chromophores in DNA1–DNA3 exhibit their typical emissions at 445 (Py), 489/522 (Pe) and 668 nm (Nr) when excited at their characteristic wavelengths (as discussed above). The lifetime of Py* (in DNA1) is 0.52 ns and hence shorter compared to that of Pe* (in DNA2, 0.89 ns) and Nr* (in DNA3, 0.97 ns). The mono-exponential decays rules out the possibility of multiple conformations of these chromophores as covalent DNA modifications. DNA4–DNA6 allow the study of the three possible binary combinations of Py, Pe, and Nr (Figure 3, left), which is an important prerequisite for the subsequent interpretation of the spectroscopic data of threefold modified DNA7–DNA12. When DNA4 is excited at the Py-typical wavelength (380 nm), the steady-state fluorescence exhibits nearly quantitative quenching of the Py emission and significant Pe emission with a lifetime of 1.01 ns is obtained. Accordingly, we propose an efficient EnT from the Py to the Pe moiety in DNA4. The resulting Pe* lifetime is nearly the same as in the single-labelled reference DNA2 (0.89 ns) and rules out the possibility of an ElT from Pe* back to Py (that would quench the Pe* fluorescence). Chem. Eur. J. 2015, 21, 9349 – 9354
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Figure 2. CD spectra of DNA7–DNA9 (top) and DNA10–DNA12 (bottom); 2.5 mm double-stranded DNA in 10 mm NaPi buffer (pH 7.0), 250 mm NaCl. For DNA1–DNA3 and DNA4–DNA6, see Figure S15 in the Supporting Information.
Table 2. Fluorescence lifetime data from decay-associated spectra of DNA1–DNA12.
DNA1 DNA2 DNA3 DNA4 DNA5 DNA6 DNA7 DNA8 DNA9 DNA10 DNA11 DNA12
lexc = 380 nm (Py) t2 [ns] t1 [ns]
lexc = 450 nm (Pe) t1 [ns] t2 [ns]
lexc = 600 nm (Nr) t1 [ns]
0.52 – – 1.01 0.35 – 0.79 1.07 1.20 0.84 0.51 1.05
– 0.89 – 0.95 – 0.49 1.15 1.12 1.33 0.56 0.52 1.16
– – 0.97 – 0.60 – – 0.69 1.33 – 0.50 0.82
– – – – – – – 0.05 0.09 0.04 0.05 0.07
– – – – – – – – – – 0.05 0.05
In DNA5 and DNA6, however, the situation is different. When excited at the Py-typical wavelength (380 nm) or Pe-typical wavelength (455 nm), respectively, only small amounts of Nr emission are observed. Hence, at first glance an EnT from Py or
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Communication Pe to Nr in DNA5 or DNA6, respectively, seems to be unlikely. But the lifetime of Py* in DNA5 is shortened to 0.35 ps (compared to that of DNA1) and a weak dual fluorescence of Py* and Nr* is obtained which can only be explained by an EnT from Py* to Nr. The situation is comparable and only slightly different in DNA6. Upon excitation of Pe, the Pe* lifetime is shortened to 0.49 ns (compared to DNA2) due to an EnT to Nr, but the Nr* fluorescence is completely quenched indicating an efficient ElT back to Pe. Thus, the photophysical situation in both DNA5 and DNA6 could be explained in such a way that EnT occurs from Py* or Pe*, respectively, to Nr and is followed by an ElT from Nr back to Py or Pe, respectively. In order to support this interpretation, we compared DNA3 bearing the single Nr modification with DNA5 and DNA6. When excited at the Nrtypical wavelength 610 nm, the Figure 3. Fluorescence spectra of DNA1–DNA6 and DNA7—DNA9; 2.5 mm double-stranded DNA in 10 mm NaPi steady-state fluorescence of buffer (pH 7.0), 250 mm NaCl; top lexc = 380 nm, middle: lexc = 455 nm, bottom: lexc = 610 nm. For DNA10–DNA12 DNA5 is nearly completely see Figure S14 in the Supporting Information. quenched by ElT and that of DNA6 is completely quenched. The time-resolved data support this result. When excited at The Pe* lifetime is shortened in DNA10 and DNA11 (Py-Nr-Pe the Nr-typical wavelength, the Nr* lifetime in DNA5 is shortsequence) but not in DNA7–DNA9 (Py-Pe-Nr sequence). The ened by ElT to 0.60 ns (compared to 0.97 ns in the reference latter, unshortened lifetimes clearly rule out the occurrence of DNA3). In DNA6, the Nr* is too weak and does not allow the EnT from Pe* to Nr in these sequences. Moreover, it is known determination of a lifetime. In conclusion, for the binary chrofrom the binary Py-Pe combination in DNA4 (as described mophore combinations in DNA4–DNA6, the fluorescence studabove) that there is no ElT from Pe* to Py, hence the shorties revealed that EnT processes are occurring from Py!Pe, ened Pe* lifetimes in DNA10 and DNA11 can be assigned to Py!Nr and Pe!Nr, and ElT processes in the other direction, EnT processes from Pe* to Nr. The second Pe* lifetimes that from Nr!Pe and Nr!Py but not from Pe!Py. were observed especially in DNA11 and DNA12 reveal the rate With this knowledge about the binary chromophore combiof 0.05 ns for the EnT process from Pe* to Nr. These observed nations and the involved photophysical processes, the interdifferences between the sequences (Py-Pe-Nr vs. Py-Nr-Pe) pretation of the steady-state fluorescence and lifetime data of cannot be explained sufficiently here but must have their threefold labelled DNA7–DNA12 is very straightforward origin in the different relative orientation of the chromophores (DNA7–DNA9, Figure 3, right; DNA10–DNA12, Figure S14 in (as the differences in the CD spectra already implied). the Supporting Information). The EnT from Py* to Pe and to Nr It is important to mention that EnT processes (Py!Pe, Pe! in DNA7 and DNA10 is reflected by the shortened lifetime of Nr and Py!Nr) occur by a distance dependence that is proportional to r¢6, whereas ElT (from Nr!Pe and Nr!Py) exhibit Py* (upon excitation at 380 nm). Depending on the distance between Py* and Pe/Nr (vide infra) these EnT processes occur an exponential and thereby stronger distance dependence. with rates between 0.04 (DNA10) and 0.09 ns (DNA9). The Hence, the increasing distance between the three chromolonger lifetimes that were observed in these samples (around phores in the series DNA7-DNA8-DNA9 and DNA10-DNA111 ns) can probably be associated to a DNA conformation in DNA12 should primarily reflect these differences by increased which the chromophore does not undergo an EnT transfer effiacceptor fluorescence intensities of Pe and Nr in the steadyciently. With respect to Pe excitation at 450 nm a more destate spectra and less shortened lifetimes of Pe* and Nr* in the tailed look at the lifetime data reveals sequence differences. time-resolved data (Figure 4). In fact, the Nr* fluorescence inChem. Eur. J. 2015, 21, 9349 – 9354
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Communication pendence can also be observed by comparison of the Pe* lifetimes in the different series of duplexes, DNA7!DNA9 versus DNA10!DNA12. The EnT process from Pe* to Nr can only be seen over distances where the ElT in the opposite direction becomes too slow to compete and thereby does not quench the resulting Nr* emission. The occurrence of an increasing amount of acceptor (Nr*) emission intensity (in the steadystate spectra) as a result of EnT again indicates that (after EnT) the ElT processes from Nr* back to Pe becomes less inefficient with increasing distance. The combination of the chromophores Py, Pe and Nr attached to the DNA bases (rigidly attached by acetylene bridges) and the double helix of DNA as structural architecture yields multichromophore systems with promising photophysical properties. The absorption of the three combined chromophores covers nearly the whole UV-A/Vis range. An EnT cascade occurs from Py over Pe to Nr and ElT in the opposite direction (from Nr to Pe or Py) subsequently provides charge separation. The efficiencies by these processes can be tuned by the distance between the chromophores. Most importantly, excitation at any wavelength between 350 and 700 nm leads finally to charge-separated states that can be used potentially for chemical photocatalysis or other applications. Hence, we conclude that especially DNA7–DNA12 represents a proof-of concept that light-harvesting systems can be designed astonishingly simply by helical arrangement in DNA-based architectures. Figure 4. Top: representative spectrum showing the time-resolved fluorescence of DNA12. The most intense signal (380 nm) comes from the scattered laser light (and its reflection from the rear of the cuvette ~ 100 ps later). Py* shows a short fluorescence lifetime, Pe* and Nr* show a much longer fluorescence lifetime. Bottom: decay-associated spectra of DNA12. Positive amplitudes correspond to decay, negative amplitudes to a rise. The spectrum associated with the short lifetime (0.07 ns) shows a positive signal in the range of Py* emission, and a negative signal in range of Nr* emission. Thus, the EnT from Py can be easily seen. In contrast, the longer lifetime (1.05 ns, as documented in Table 2) does not correspond to the fluorescence of Py* (although this chromophore has been excited at 380 nm) but to the fluorescence of Pe* and Nr*, as evidenced by the positive signals of this decay-associated spectrum.
tensity increases significantly in both series of duplexes when the Nr chromophore is excited directly at 600 nm. Upon excitation of Nr (600 nm) in DNA7 and DNA10, the Nr* fluorescence is quenched completely as a result of an efficient ElT from Nr* to Pe over such short distances. This interpretation is supported by the Nr* fluorescence lifetimes of the DNA samples in which Pe is separated from Nr by one or two intervening A–T base pairs. In fact, with increasing distance in DNA8!DNA9 and DNA11!DNA12 the Nr* fluorescence lifetime increases. A more detailed look reveals that the Nr* lifetimes are shorter in DNA11/DNA12 compared to DNA8/DNA9 due to the neighbourhood of Py next to Nr in the sequence Py-Nr-Pe which opens an additional ElT channel. In the other direction, the Pe* fluorescence as an intermediate emission in the EnT cascades Py!Pe!Nr and acceptor emission in the row Py!Nr is intensified if DNA8/DNA9 and DNA11/DNA12 are excited at the Pytypical wavelength (380 nm). This difference in distance deChem. Eur. J. 2015, 21, 9349 – 9354
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Experimental Section All experimental details, including the syntheses and spectroscopy, are described in the Supporting Information.
Acknowledgements Financial support by the Karlsruhe School of Optics and Photonics (KSOP), Deutsche Forschungsgemeinschaft/GRK 1626 “Chemical Photocatalysis” and KIT is gratefully acknowledged. Keywords: electron transfer · energy transfer · fluorescence · helix · oligonucleotides
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Received: March 27, 2015 Published online on June 9, 2015
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