Efficient Long-range, Directional Energy Transfer through DNA

Subscriber access provided by CAL STATE UNIV BAKERSFIELD

Article

Efficient Long-range, Directional Energy Transfer through DNA-Templated Dye Aggregates Xu Zhou, Sarthak Mandal, Shuoxing Jiang, Su Lin, Jianzhong Yang, Yan Liu, David G. Whitten, Neal W. Woodbury, and Hao Yan J. Am. Chem. Soc., Just Accepted Manuscript • Publication Date (Web): 16 Apr 2019 Downloaded from http://pubs.acs.org on April 16, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 26 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

Journal of the American Chemical Society

Efficient Long-range, Directional Energy Transfer through DNA-Templated Dye Aggregates

Xu Zhou,1,3, $ Sarthak Mandal,2,5, $ Shuoxing Jiang, 1 Su Lin,2, 3 Jianzhong Yang, 4 Yan Liu, 1, 3 David G. Whitten, 4 Neal W. Woodbury2, 3* and Hao Yan1, 3*

1Center

for Molecular Design and Biomimetics at the Biodesign Institute, Arizona State University,

Tempe, Arizona, USA 2Center

for Innovations in Medicine at the Biodesign Institute, Arizona State University, Tempe,

Arizona, USA 3School

of Molecular Sciences, Arizona State University, Tempe, Arizona, USA

4Department

of Chemical and Biological Engineering, University of New Mexico, Albuquerque,

New Mexico, USA 5Department

of Chemistry, National Institute of Technology Tiruchirappalli, Tamil Nadu, India

*Corresponding

$ Both

Authors ([email protected], [email protected])

these authors contributed equally to this work

1 ACS Paragon Plus Environment

Journal of the American Chemical Society 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

Abstract The benzothiazole cyanine dye, K21, forms dye aggregates on double stranded DNA (dsDNA) templates. These aggregates exhibit a red-shifted absorption band, enhanced fluorescence emission and an increased fluorescence lifetime, all indicating strong excitonic coupling among the dye molecules. K21 aggregate formation on dsDNA is only weakly sequence dependent, providing a flexible approach that is adaptable to many different DNA nanostructures. Donor (D) – bridge (B) – Acceptor (A) complexes consisting of Alexa Fluor 350 as the donor, a 30 bp (9.7 nm) DNA templated K21 aggregate as the bridge and Alexa Fluor 555 as the acceptor show an overall donor to acceptor energy transfer efficiency of ~60%, with the loss of excitation energy being almost exclusively at the donor-bridge junction (63%). There was almost no excitation energy loss due to transfer through the aggregate bridge and the transfer efficiency from the aggregate to the acceptor was about 96%. By comparing the energy transfer in templated aggregates at several lengths up to 32 nm, the loss of energy per nanometer through the K21 aggregate bridge was determined to be 96%

42%

54%

>96%

50%

on essentially random sequences of dsDNA. Figure S10 shows the analysis of 2D-B-A complexes using a random DNA sequence with a length of 30 bp as a template and the results are very similar to those reported for poly(A)/poly(T) above. D-B-A Constructs with dsDNA lengths of 30 bp (9.7 nm), 60 bp (19.4 nm) and 100 bp (32.4 nm) using essentially random sequences were compared to



explore the length dependence of energy transfer through the aggregates. The persistence length of dsDNA is ~50 nm, so these sequences are nearly rigid spacers. The concentration of DNA base pairs was kept the same for each construct giving rise to final DNA strand concentrations of 4 µM, 2 µM and 1.2 µM, respectively. To maintain a similar ratio of absorption cross-section of the AF350 donor and the K21 dye at 350 nm for each construct, 2 donors, 4 donors and 7 donors were conjugated onto the DNA templates with lengths of 30 bp, 60 bp and 100 bp, respectively (Figure 5, SI Section 3). Multiple donors conjugated to the DNA were separated by 2 or 3 bps to avoid direct physical contact of the dyes minimize self-quenching. Steady state fluorescence spectra using 350 nm excitation were measured for the three D-BA systems with different lengths of the bridge aggregates. The aggregate bridge to acceptor energy transfer efficiencies in the three systems are in the range of 85%-93% (Figure 5a, Figure S1012). Note that the errors provided are errors in repeated measurements of a specific preparation of the construct, while the differences between preparations of different templated aggregates are apparently larger (exactly what DNA sequence was used and how the aggregate formed). Based on this it is difficult to detect much difference in energy transfer efficiency as a function of the bridge length. Since light can be absorbed anywhere within the aggregate, the bridge to acceptor energy transfer efficiency would be expected to drop with increasing length as light absorbed far from the acceptor should be subject to larger losses. The fact that there is little loss implies that at least up to 100 bp (32 nm), the losses are small. Taken at face value, an energy transfer efficiency within the aggregate of 88% over 100 bp results in a characteristic energy transfer length of ~370 bp or ~120 nm (the characteristic energy transfer length is the length that would result in an energy transfer efficiency of 1/e or 37%; this calculation is described in SI section 5) and an energy loss per nanometer of less than 1%. However this calculation assumes that the final transfer between 20 ACS Paragon Plus Environment

Page 20 of 26

Page 21 of 26 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


the bridge and the acceptor is 100% efficient and is thus a minimum value for the characteristic energy transfer length through the aggregate (if one assumed that the final transfer efficiency from the aggregate to the acceptor was 95%, then the characteristic length estimated would be ~620 bp or 200 nm and 90% would result in ~2000 bp or 650 nm).

Figure 5. Cyanine dye aggregates mediate donor-acceptor energy transfer over long distance. a. Schematic and fluorescence spectra of B-A constructs formed on 30 bp (30R), 60 bp (60R) and 100 bp (100R) DNA templates with random sequence. b. Schematic and fluorescence spectra of nD-B-A constructs formed on 30 bp (30R), 60 bp (60R) and 100 bp (100R) DNA templates with random sequence. Figure 5b shows the result of adding donors to the constructs in the length series. Note that the arrangement of donors and their conjugation (and thus efficiency of transfer) to the aggregate vary from construct to construct, thus one cannot compare overall efficiencies for each construct (the donor to aggregate energy transfer efficiency dominates the overall efficiency; the variation in donor to bridge efficiency in these constructs is shown in Figure S13 and S14). However, all constructs show substantial transfer from donor to acceptor through the aggregate bridge. For the 21 ACS Paragon Plus Environment


7D-B-A construct with a 100 bp (32 nm) aggregate bridge, the overall energy transfer efficiency is ~ 55% upon excitation of the donor at 350 nm. A detailed model with microscopic rate constants is provided in the supplementary material (SI, Section 6).

Conclusion K21 dye aggregates on dsDNA templates facilitate directional energy transfer over distances of at least tens and probably hundreds of nanometers, providing an effective means of incorporating energy transfer “wires” into photonic systems based on DNA nanostructures. The fact that the assembly of aggregates onto the DNA is only weakly dependent on DNA sequence allows considerable flexibility in DNA nanostructure design. The addressability and bio-compatibility of DNA nanostructures allows integration of functional components, such as enzymes46 and photosynthetic reaction centers47, for the construction of artificial light-harvesting and energy conversion systems.

Associated Content Supporting Information. Additional steady-state and time-resolved spectroscopic data, DNA sequences, DNA-dye conjugates synthesis and characterization, calculation and estimation of energy transfer efficiency, a simple kinetics model of D-B-A energy transfer construct.

Acknowledgements This work was supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Award No. DE-SC0016353. 22 ACS Paragon Plus Environment

Page 22 of 26

Page 23 of 26 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


References 1. Park, H.; Heldman, N.; Rebentrost, P.; Abbondanza, L.; Iagatti, A.; Alessi, A.; Patrizi, B.; Salvalaggio, M.; Bussotti, L.; Mohseni, M.; Caruso, F.; Johnsen, H. C.; Fusco, R.; Foggi, P.; Scudo, P. F.; Lloyd, S.; Belcher, A. M., Enhanced energy transport in genetically engineered excitonic networks. Nat Mater 2016, 15 (2), 211-6. 2. Yim, D.; Sung, J.; Kim, S.; Oh, J.; Yoon, H.; Sung, Y. M.; Kim, D.; Jang, W. D., Guest-Induced Modulation of the Energy Transfer Process in Porphyrin-Based Artificial Light Harvesting Dendrimers. J Am Chem Soc 2017, 139 (2), 993-1002. 3. Shi, Y.; Cao, X.; Hu, D.; Gao, H., Highly Branched Polymers with Layered Structures that Mimic Light-Harvesting Processes. Angew Chem Int Ed Engl 2018, 57 (2), 516-520. 4. Zhao, L.; Zou, H.; Zhang, H.; Sun, H.; Wang, T.; Pan, T.; Li, X.; Bai, Y.; Qiao, S.; Luo, Q.; Xu, J.; Hou, C.; Liu, J., Enzyme-Triggered Defined Protein Nanoarrays: Efficient Light-Harvesting Systems to Mimic Chloroplasts. ACS Nano 2017, 11 (1), 938-945. 5. Son, H. J.; Jin, S.; Patwardhan, S.; Wezenberg, S. J.; Jeong, N. C.; So, M.; Wilmer, C. E.; Sarjeant, A. A.; Schatz, G. C.; Snurr, R. Q.; Farha, O. K.; Wiederrecht, G. P.; Hupp, J. T., Light-harvesting and ultrafast energy migration in porphyrin-based metal-organic frameworks. J Am Chem Soc 2013, 135 (2), 862-9. 6. Williams, D. E.; Rietman, J. A.; Maier, J. M.; Tan, R.; Greytak, A. B.; Smith, M. D.; Krause, J. A.; Shustova, N. B., Energy transfer on demand: photoswitch-directed behavior of metal-porphyrin frameworks. J Am Chem Soc 2014, 136 (34), 11886-9. 7. Hannestad, J. K.; Sandin, P.; Albinsson, B., Self-assembled DNA photonic wire for long-range energy transfer. J Am Chem Soc 2008, 130 (47), 15889-95. 8. Teo, Y. N.; Kool, E. T., DNA-multichromophore systems. Chem Rev 2012, 112 (7), 4221-45. 9. Woller, J. G.; Hannestad, J. K.; Albinsson, B., Self-assembled nanoscale DNA-porphyrin complex for artificial light harvesting. J Am Chem Soc 2013, 135 (7), 2759-68. 10. Dutta, P. K.; Varghese, R.; Nangreave, J.; Lin, S.; Yan, H.; Liu, Y., DNA-directed artificial lightharvesting antenna. J Am Chem Soc 2011, 133 (31), 11985-93. 11. Stein, I. H.; Steinhauer, C.; Tinnefeld, P., Single-molecule four-color FRET visualizes energytransfer paths on DNA origami. J Am Chem Soc 2011, 133 (12), 4193-5. 12. Buckhout-White, S.; Spillmann, C. M.; Algar, W. R.; Khachatrian, A.; Melinger, J. S.; Goldman, E. R.; Ancona, M. G.; Medintz, I. L., Assembling programmable FRET-based photonic networks using designer DNA scaffolds. Nat Commun 2014, 5, 5615. 13. Hemmig, E. A.; Creatore, C.; Wunsch, 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 (4), 2369-74. 14. Melinger, J. S.; Khachatrian, A.; Ancona, M. G.; Buckhout-White, S.; Goldman, E. R.; Spillmann, C. M.; Medintz, I. L.; Cunningham, P. D., FRET from Multiple Pathways in Fluorophore-Labeled DNA. Acs Photonics 2016, 3 (4), 659-669. 15. Scholes, G. D.; Fleming, G. R.; Olaya-Castro, A.; van Grondelle, R., Lessons from nature about solar light harvesting. Nat Chem 2011, 3 (10), 763-774. 16. Mirkovic, T.; Ostroumov, E. E.; Anna, J. M.; van Grondelle, R.; Govindjee; Scholes, G. D., Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms. Chem Rev 2017, 117 (2), 249-293.



17. Chenu, A.; Scholes, G. D., Coherence in Energy Transfer and Photosynthesis. Annu Rev Phys Chem 2015, 66, 69-96. 18. Scholes, G. D.; Fleming, G. R.; Chen, L. X.; Aspuru-Guzik, A.; Buchleitner, A.; Coker, D. F.; Engel, G. S.; van Grondelle, R.; Ishizaki, A.; Jonas, D. M.; Lundeen, J. S.; McCusker, J. K.; Mukamel, S.; Ogilvie, J. P.; Olaya-Castro, A.; Ratner, M. A.; Spano, F. C.; Whaley, K. B.; Zhu, X. Y., Using coherence to enhance function in chemical and biophysical systems. Nature 2017, 543 (7647), 647-656. 19. Oostergetel, G. T.; van Amerongen, H.; Boekema, E. J., The chlorosome: a prototype for efficient light harvesting in photosynthesis. Photosynth Res 2010, 104 (2-3), 245-55. 20. Orf, G. S.; Blankenship, R. E., Chlorosome antenna complexes from green photosynthetic bacteria. Photosynth Res 2013, 116 (2-3), 315-331. 21. Cogdell, R. J.; Gall, A.; Kohler, J., The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q Rev Biophys 2006, 39 (3), 227-324. 22. Sturgis, J. N.; Niederman, R. A., Atomic force microscopy reveals multiple patterns of antenna organization in purple bacteria: implications for energy transduction mechanisms and membrane modeling. Photosynth Res 2008, 95 (2-3), 269-278. 23. Cheng, Y. C.; Fleming, G. R., Dynamics of Light Harvesting in Photosynthesis. Annual Review of Physical Chemistry 2009, 60, 241-262. 24. Lu, L.; Jones, R. M.; McBranch, D.; Whitten, D., Surface-Enhanced Superquenching of Cyanine Dyes as J-Aggregates on Laponite Clay Nanoparticles. Langmuir 2002, 18 (20), 7706-7713. 25. Wurthner, F.; Kaiser, T. E.; Saha-Moller, C. R., J-aggregates: from serendipitous discovery to supramolecular engineering of functional dye materials. Angew Chem Int Ed Engl 2011, 50 (15), 3376410. 26. Sengupta, S.; Wurthner, F., Chlorophyll J-aggregates: from bioinspired dye stacks to nanotubes, liquid crystals, and biosupramolecular electronics. Acc Chem Res 2013, 46 (11), 2498-512. 27. Haedler, A. T.; Kreger, K.; Issac, A.; Wittmann, B.; Kivala, M.; Hammer, N.; Kohler, J.; Schmidt, H. W.; Hildner, R., Long-range energy transport in single supramolecular nanofibres at room temperature. Nature 2015, 523 (7559), 196-9. 28. Peng, H. Q.; Niu, L. Y.; Chen, Y. Z.; Wu, L. Z.; Tung, C. H.; Yang, Q. Z., Biological Applications of Supramolecular Assemblies Designed for Excitation Energy Transfer. Chem Rev 2015, 115 (15), 7502-42. 29. Zou, Q.; Liu, K.; Abbas, M.; Yan, X., Peptide-Modulated Self-Assembly of Chromophores toward Biomimetic Light-Harvesting Nanoarchitectonics. Adv Mater 2016, 28 (6), 1031-43. 30. Freyria, F. S.; Cordero, J. M.; Caram, J. R.; Doria, S.; Dodin, A.; Chen, Y.; Willard, A. P.; Bawendi, M. G., Near-Infrared Quantum Dot Emission Enhanced by Stabilized Self-Assembled J-Aggregate Antennas. Nano Lett 2017, 17 (12), 7665-7674. 31. Wang, C.; Weiss, E. A., Accelerating FRET between Near-Infrared Emitting Quantum Dots Using a Molecular J-Aggregate as an Exciton Bridge. Nano Lett 2017, 17 (9), 5666-5671. 32. Brixner, T.; Hildner, R.; Köhler, J.; Lambert, C.; Würthner, F., Exciton Transport in Molecular Aggregates - From Natural Antennas to Synthetic Chromophore Systems. Advanced Energy Materials 2017, 7 (16). 33. Bricks, J. L.; Slominskii, Y. L.; Panas, I. D.; Demchenko, A. P., Fluorescent J-aggregates of cyanine dyes: basic research and applications review. Methods Appl Fluoresc 2017, 6 (1), 012001. 34. Wang, M.; Silva, G. L.; Armitage, B. A., DNA-Templated Formation of a Helical Cyanine Dye JAggregate. Journal of the American Chemical Society 2000, 122 (41), 9977-9986. 35. Hannah, K. C.; Armitage, B. A., DNA-templated assembly of helical cyanine dye aggregates: a supramolecular chain polymerization. Acc Chem Res 2004, 37 (11), 845-53.


Page 24 of 26

Page 25 of 26 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


36. Iwaura, R.; Ohnishi-Kameyama, M.; Iizawa, T., Construction of helical J-aggregates selfassembled from a thymidylic acid appended anthracene dye and DNA as a template. Chemistry 2009, 15 (15), 3729-35. 37. Asanuma, H.; Fujii, T.; Kato, T.; Kashida, H., Coherent interactions of dyes assembled on DNA. J Photoch Photobio C 2012, 13 (2), 124-135. 38. Cannon, B. L.; Kellis, D. L.; Patten, L. K.; Davis, P. H.; Lee, J.; Graugnard, E.; Yurke, B.; Knowlton, W. B., Coherent Exciton Delocalization in a Two-State DNA-Templated Dye Aggregate System. J Phys Chem A 2017, 121 (37), 6905-6916. 39. Pinheiro, A. V.; Han, D.; Shih, W. M.; Yan, H., Challenges and opportunities for structural DNA nanotechnology. Nat Nanotechnol 2011, 6 (12), 763-72. 40. Zhang, F.; Nangreave, J.; Liu, Y.; Yan, H., Structural DNA nanotechnology: state of the art and future perspective. J Am Chem Soc 2014, 136 (32), 11198-211. 41. Hong, F.; Zhang, F.; Liu, Y.; Yan, H., DNA Origami: Scaffolds for Creating Higher Order Structures. Chem Rev 2017, 117 (20), 12584-12640. 42. Boulais, E.; Sawaya, N. P. D.; Veneziano, R.; Andreoni, A.; Banal, J. L.; Kondo, T.; Mandal, S.; Lin, S.; Schlau-Cohen, G. S.; Woodbury, N. W.; Yan, H.; Aspuru-Guzik, A.; Bathe, M., Programmed coherent coupling in a synthetic DNA-based excitonic circuit. Nat Mater 2018, 17 (2), 159-166. 43. Armitage, B. A., Cyanine Dye–DNA Interactions: Intercalation, Groove Binding, and Aggregation. In DNA Binders and Related Subjects: -/-, Waring, M. J.; Chaires, J. B., Eds. Springer Berlin Heidelberg: Berlin, Heidelberg, 2005; pp 55-76. 44. Banal, J. L.; Kondo, T.; Veneziano, R.; Bathe, M.; Schlau-Cohen, G. S., Photophysics of JAggregate-Mediated Energy Transfer on DNA. J Phys Chem Lett 2017, 8 (23), 5827-5833. 45. Lakowicz, J. R., Energy Transfer. In Principle of Fluorescence SPectroscopy, third ed.; Lakowicz, J. R., Ed. Springer: 2006; p 443. 46. Fu, J.; Yang, Y. R.; Dhakal, S.; Zhao, Z.; Liu, M.; Zhang, T.; Walter, N. G.; Yan, H., Assembly of multienzyme complexes on DNA nanostructures. Nat Protoc 2016, 11 (11), 2243-2273. 47. Dutta, P. K.; Levenberg, S.; Loskutov, A.; Jun, D.; Saer, R.; Beatty, J. T.; Lin, S.; Liu, Y.; Woodbury, N. W.; Yan, H., A DNA-directed light-harvesting/reaction center system. J Am Chem Soc 2014, 136 (47), 16618-25.



TOC


Page 26 of 26

Efficient Long-range, Directional Energy Transfer through DNA

Recommend Documents