Photophysics of J-Aggregate-Mediated Energy Transfer on DNA

Banal, James L.; Kondo, Toru; Veneziano, Rémi; Bathe, Mark; Schlau-Cohen, Gabriela S.

doi:10.1021/acs.jpclett.7b01898

Title: Photophysics of J-Aggregate-Mediated Energy Transfer on DNA

Journal Article · Thu Nov 16 00:00:00 EST 2017 · Journal of Physical Chemistry Letters

DOI:https://doi.org/10.1021/acs.jpclett.7b01898· OSTI ID:1821493

^[1]; Kondo, Toru ^[1];

^[1];

^[1]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Achieving nanoscale spatial and electronic control over the formation of dye aggregates is a major synthetic challenge due to their typically inhomogeneous self-assembly, which limits control over their higher-order organization. To address these challenges, synthetic DNA-templated pseudoisocyanine (PIC) J-aggregates were recently introduced. However, the dependence of the photophysics of the superradiant exciton on the underlying DNA template length and the impact of static disorder on energy transfer through these PIC J-aggregates remain unknown. We examine the delocalization length progression of superradiant PIC excitons by varying the length of poly-A DNA tracts that template PIC J-aggregates. We then investigate the energy-transfer efficiency from PIC J-aggregates with DNA duplex template length, which we found to be limited by static disorder. Furthermore, utilizing the self-assembled and selective formation of superradiant excitons on DNA provides a platform to determine the function of delocalized excitons in the context of nanoscale energy transport.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); US Army Research Office (ARO); National Science Foundation (NSF)

Grant/Contract Number:: SC0001088

OSTI ID:: 1821493

Journal Information:: Journal of Physical Chemistry Letters, Vol. 8, Issue 23; ISSN 1948-7185

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 50 works

Citation information provided by
Web of Science

References (53)

Extending DNA-Based Molecular Photonic Wires with Homogeneous Förster Resonance Energy Transfer Díaz, Sebastián A.; Buckhout-White, Susan; Ancona, Mario G. Advanced Optical Materials, Vol. 4, Issue 3 https://doi.org/10.1002/adom.201500554	journal	January 2016
Light-Harvesting Metal–Organic Frameworks (MOFs) Efficient Strut-to-Strut Energy Transfer in Bodipy and Porphyrin-Based MOFs Lee, Chang Yeon; Farha, Omar K.; Hong, Bong Jin Journal of the American Chemical Society, Vol. 133, Issue 40, p. 15858-15861 https://doi.org/10.1021/ja206029a	journal	October 2011
Annihilation of singlet excitons in J aggregates of pseudoisocyanine (PIC) studied by pico‐ and subpicosecond spectroscopy Sundström, V.; Gillbro, T.; Gadonas, R. A. The Journal of Chemical Physics, Vol. 89, Issue 5 https://doi.org/10.1063/1.455027	journal	September 1988
Adapting the Förster Theory of Energy Transfer for Modeling Dynamics in Aggregated Molecular Assemblies Scholes, Gregory D.; Jordanides, Xanthipe J.; Fleming, Graham R. The Journal of Physical Chemistry B, Vol. 105, Issue 8 https://doi.org/10.1021/jp003571m	journal	March 2001
Spontaneous Assembly of Helical Cyanine Dye Aggregates on DNA Nanotemplates Seifert, Jennifer L.; Connor, Rebecca E.; Kushon, Stuart A. Journal of the American Chemical Society, Vol. 121, Issue 13 https://doi.org/10.1021/ja984279j	journal	April 1999
Porphyrin Light-Harvesting Arrays Constructed in the Recombinant Tobacco Mosaic Virus Scaffold Endo, Masayuki; Fujitsuka, Mamoru; Majima, Tetsuro Chemistry - A European Journal, Vol. 13, Issue 31 https://doi.org/10.1002/chem.200700895	journal	October 2007
DNA-Directed Artificial Light-Harvesting Antenna Dutta, Palash K.; Varghese, Reji; Nangreave, Jeanette Journal of the American Chemical Society, Vol. 133, Issue 31 https://doi.org/10.1021/ja1115138	journal	August 2011
Programming Light-Harvesting Efficiency Using DNA Origami Hemmig, Elisa A.; Creatore, Celestino; Wünsch, Bettina Nano Letters, Vol. 16, Issue 4 https://doi.org/10.1021/acs.nanolett.5b05139	journal	March 2016
Helical Aggregation of Cyanine Dyes on DNA Templates: Effect of Dye Structure on Formation of Homo- and Heteroaggregates Garoff, Rachel A.; Litzinger, Elizabeth A.; Connor, Rebecca E. Langmuir, Vol. 18, Issue 16 https://doi.org/10.1021/la025742f	journal	August 2002
Self-Assembled Nanoscale DNA–Porphyrin Complex for Artificial Light Harvesting Woller, Jakob G.; Hannestad, Jonas K.; Albinsson, Bo Journal of the American Chemical Society, Vol. 135, Issue 7 https://doi.org/10.1021/ja311828v	journal	February 2013
L ONG -R ANGE R ESONANCE E NERGY T RANSFER IN M OLECULAR S YSTEMS Scholes, Gregory D. Annual Review of Physical Chemistry, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.physchem.54.011002.103746	journal	October 2003
Structure of J-Aggregates of Pseudoisocyanine Dye in Aqueous Solution von Berlepsch, H.; Böttcher, C.; Dähne, L. The Journal of Physical Chemistry B, Vol. 104, Issue 37 https://doi.org/10.1021/jp000085q	journal	September 2000
Features of exciton dynamics in molecular nanoclusters ( J -aggregates): Exciton self-trapping (Review Article) Malyukin, Yu. V.; Sorokin, A. V.; Semynozhenko, V. P. Low Temperature Physics, Vol. 42, Issue 6 https://doi.org/10.1063/1.4955493	journal	June 2016
Designing light-harvesting antenna systems based on superradiant molecular aggregates Scholes, Gregory D. Chemical Physics, Vol. 275, Issue 1-3 https://doi.org/10.1016/S0301-0104(01)00533-X	journal	January 2002
Uniform exciton fluorescence from individual molecular nanotubes immobilized on solid substrates Eisele, Dörthe M.; Knoester, Jasper; Kirstein, Stefan Nature Nanotechnology, Vol. 4, Issue 10 https://doi.org/10.1038/nnano.2009.227	journal	August 2009
Design and engineering of water-soluble light-harvesting protein maquettes Kodali, Goutham; Mancini, Joshua A.; Solomon, Lee A. Chemical Science, Vol. 8, Issue 1 https://doi.org/10.1039/C6SC02417C	journal	January 2017
Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms Mirkovic, Tihana; Ostroumov, Evgeny E.; Anna, Jessica M. Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.6b00002	journal	March 2016
Temperature-dependent superradiant decay of excitons in small aggregates Spano, Francis C.; Kuklinski, Jan R.; Mukamel, Shaul Physical Review Letters, Vol. 65, Issue 2 https://doi.org/10.1103/PhysRevLett.65.211	journal	July 1990
Coherence in Energy Transfer and Photosynthesis Chenu, Aurélia; Scholes, Gregory D. Annual Review of Physical Chemistry, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-physchem-040214-121713	journal	April 2015
Cooperative radiative dynamics in molecular aggregates Spano, Francis C.; Kuklinski, Jan R.; Mukamel, Shaul The Journal of Chemical Physics, Vol. 94, Issue 11 https://doi.org/10.1063/1.460185	journal	June 1991
Energy Transfer Mechanisms and the Molecular Exciton Model for Molecular Aggregates Kasha, Michael Radiation Research, Vol. 20, Issue 1 https://doi.org/10.2307/3571331	journal	September 1963
Assembling programmable FRET-based photonic networks using designer DNA scaffolds Buckhout-White, Susan; Spillmann, Christopher M.; Algar, W. Russ Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6615	journal	December 2014
Superradiant emission and optical dephasing in J-aggregates Fidder, Henk; Knoester, Jasper; Wiersma, Douwe A. Chemical Physics Letters, Vol. 171, Issue 5-6 https://doi.org/10.1016/0009-2614(90)85258-E	journal	August 1990
Programmed coherent coupling in a synthetic DNA-based excitonic circuit Boulais, Étienne; Sawaya, Nicolas P. D.; Veneziano, Rémi Nature Materials, Vol. 17, Issue 2 https://doi.org/10.1038/nmat5033	journal	November 2017
DNA-Templated Formation of a Helical Cyanine Dye J-Aggregate Wang, Miaomiao; Silva, Gloria L.; Armitage, Bruce A. Journal of the American Chemical Society, Vol. 122, Issue 41 https://doi.org/10.1021/ja002184n	journal	October 2000
The exciton model in molecular spectroscopy Kasha, M.; Rawls, H. R.; Ashraf El-Bayoumi, M. Pure and Applied Chemistry, Vol. 11, Issue 3-4 https://doi.org/10.1351/pac196511030371	journal	January 1965
Virus-Templated Assembly of Porphyrins into Light-Harvesting Nanoantennae Nam, Yoon Sung; Shin, Taeho; Park, Heechul Journal of the American Chemical Society, Vol. 132, Issue 5 https://doi.org/10.1021/ja908812b	journal	February 2010
Enhanced energy transport in genetically engineered excitonic networks Park, Heechul; Heldman, Nimrod; Rebentrost, Patrick Nature Materials, Vol. 15, Issue 2 https://doi.org/10.1038/nmat4448	journal	October 2015
Self-Assembled Quantum Dot-Sensitized Multivalent DNA Photonic Wires Boeneman, Kelly; Prasuhn, Duane E.; Blanco-Canosa, Juan B. Journal of the American Chemical Society, Vol. 132, Issue 51 https://doi.org/10.1021/ja106465x	journal	December 2010
Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales Noy, Dror; Moser, Christopher C.; Dutton, P. Leslie Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 2 https://doi.org/10.1016/j.bbabio.2005.11.010	journal	February 2006
Evidence of Exciton Self-Trapping in Pseudoisocyanine J-Aggregates Formed in Layered Polymer Films Sorokin, Alexander V.; Pereverzev, Nikita V.; Grankina, Irina I. The Journal of Physical Chemistry C, Vol. 119, Issue 49 https://doi.org/10.1021/acs.jpcc.5b09940	journal	November 2015
Self-Assembled DNA-Based Fluorescence Waveguide with Selectable Output Hannestad, Jonas K.; Gerrard, Simon R.; Brown, Tom Small, Vol. 7, Issue 22 https://doi.org/10.1002/smll.201101144	journal	September 2011
Utilizing redox-chemistry to elucidate the nature of exciton transitions in supramolecular dye nanotubes Eisele, D. M.; Cone, C. W.; Bloemsma, E. A. Nature Chemistry, Vol. 4, Issue 8 https://doi.org/10.1038/nchem.1380	journal	July 2012
Size dependence of excited-state dynamics for J-aggregates at silver bromide interfaces Muenter, A. A.; Brumbaugh, D. V.; Apolito, J. The Journal of Physical Chemistry, Vol. 96, Issue 7 https://doi.org/10.1021/j100186a002	journal	April 1992
Symmetry-enhanced supertransfer of delocalized quantum states Lloyd, Seth; Mohseni, Masoud New Journal of Physics, Vol. 12, Issue 7 https://doi.org/10.1088/1367-2630/12/7/075020	journal	July 2010
Designer nanoscale DNA assemblies programmed from the top down Veneziano, R.; Ratanalert, S.; Zhang, K. Science, Vol. 352, Issue 6293 https://doi.org/10.1126/science.aaf4388	journal	May 2016
Linear absorption as a tool to measure the exciton delocalization length in molecular assemblies Bakalis, Lisette D.; Knoester, Jasper Journal of Luminescence, Vol. 87-89 https://doi.org/10.1016/S0022-2313(99)00231-8	journal	May 2000
Exciton superradiance in aggregates: The effect of disorder, higher order exciton-phonon coupling and dimensionality Potma, Eric O.; Wiersma, Douwe A. The Journal of Chemical Physics, Vol. 108, Issue 12 https://doi.org/10.1063/1.475898	journal	March 1998
Multi-step excitation energy transfer engineered in genetic fusions of natural and synthetic light-harvesting proteins Mancini, Joshua A.; Kodali, Goutham; Jiang, Jianbing Journal of The Royal Society Interface, Vol. 14, Issue 127 https://doi.org/10.1098/rsif.2016.0896	journal	February 2017
Quantum design of photosynthesis for bio-inspired solar-energy conversion Romero, Elisabet; Novoderezhkin, Vladimir I.; van Grondelle, Rienk Nature, Vol. 543, Issue 7645 https://doi.org/10.1038/nature22012	journal	March 2017
DNA-Templated Assembly of Helical Cyanine Dye Aggregates: A Supramolecular Chain Polymerization Hannah, Kristen C.; Armitage, Bruce A. Accounts of Chemical Research, Vol. 37, Issue 11 https://doi.org/10.1021/ar030257c	journal	November 2004
Förster Energy Transport in Metal–Organic Frameworks Is Beyond Step-by-Step Hopping Zhang, Qiongqiong; Zhang, Cankun; Cao, Lingyun Journal of the American Chemical Society, Vol. 138, Issue 16 https://doi.org/10.1021/jacs.6b01345	journal	January 2016
Structure-based model for light-harvesting properties of nucleic acid nanostructures Pan, Keyao; Boulais, Etienne; Yang, Lun Nucleic Acids Research, Vol. 42, Issue 4 https://doi.org/10.1093/nar/gkt1269	journal	December 2013
Beyond Förster Resonance Energy Transfer in Biological and Nanoscale Systems Beljonne, David; Curutchet, Carles; Scholes, Gregory D. The Journal of Physical Chemistry B, Vol. 113, Issue 19 https://doi.org/10.1021/jp900708f	journal	May 2009
J-Aggregates: From Serendipitous Discovery to Supramolecular Engineering of Functional Dye Materials Würthner, Frank; Kaiser, Theo E.; Saha-Möller, Chantu R. Angewandte Chemie International Edition, Vol. 50, Issue 15 https://doi.org/10.1002/anie.201002307	journal	March 2011
Room-Temperature Micron-Scale Exciton Migration in a Stabilized Emissive Molecular Aggregate Caram, Justin R.; Doria, Sandra; Eisele, Dörthe M. Nano Letters, Vol. 16, Issue 11 https://doi.org/10.1021/acs.nanolett.6b02529	journal	October 2016
Cooperative energy transfer Strȩk, W. Physics Letters A, Vol. 62, Issue 5 https://doi.org/10.1016/0375-9601(77)90427-3	journal	September 1977
Lessons from nature about solar light harvesting Scholes, Gregory D.; Fleming, Graham R.; Olaya-Castro, Alexandra Nature Chemistry, Vol. 3, Issue 10 https://doi.org/10.1038/nchem.1145	journal	September 2011
Energy Migration in Organic Solar Concentrators with a Molecularly Insulated Perylene Diimide Banal, James L.; Soleimaninejad, Hamid; Jradi, Fadi M. The Journal of Physical Chemistry C, Vol. 120, Issue 24 https://doi.org/10.1021/acs.jpcc.6b04479	journal	June 2016
Self-Assembled DNA Photonic Wire for Long-Range Energy Transfer Hannestad, Jonas K.; Sandin, Peter; Albinsson, Bo Journal of the American Chemical Society, Vol. 130, Issue 47 https://doi.org/10.1021/ja803407t	journal	November 2008
Vibronic Coupling in J-Aggregates and Beyond: A Direct Means of Determining the Exciton Coherence Length from the Photoluminescence Spectrum Spano, Frank C.; Yamagata, Hajime The Journal of Physical Chemistry B, Vol. 115, Issue 18 https://doi.org/10.1021/jp104752k	journal	May 2011
Membrane-Anchored DNA Assembly for Energy and Electron Transfer Börjesson, Karl; Tumpane, John; Ljungdahl, Thomas Journal of the American Chemical Society, Vol. 131, Issue 8 https://doi.org/10.1021/ja8038294	journal	February 2009
Does Coherence Enhance Transport in Photosynthesis? Kassal, Ivan; Yuen-Zhou, Joel; Rahimi-Keshari, Saleh The Journal of Physical Chemistry Letters, Vol. 4, Issue 3 https://doi.org/10.1021/jz301872b	journal	January 2013

Cited By (4)

Excitonic channels from bio-inspired templated supramolecular assembly of J-aggregate nanowires Anantharaman, Surendra B.; Messmer, Daniel; Sadeghpour, Amin Nanoscale, Vol. 11, Issue 14 https://doi.org/10.1039/c8nr10357g	journal	January 2019
Utilizing the Organizational Power of DNA Scaffolds for New Nanophotonic Applications Bui, Hieu; Díaz, Sebastián A.; Fontana, Jake Advanced Optical Materials, Vol. 7, Issue 18 https://doi.org/10.1002/adom.201900562	journal	July 2019
Bioproduction of pure, kilobase-scale single-stranded DNA Shepherd, Tyson R.; Du, Rebecca R.; Huang, Hellen Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-42665-1	journal	April 2019
Molecular model of J-aggregated pseudoisocyanine fibers Bricker, William P.; Banal, James L.; Stone, Matthew B. The Journal of Chemical Physics, Vol. 149, Issue 2 https://doi.org/10.1063/1.5036656	journal	July 2018

Similar Records

Directed Energy Transfer through DNA-templated J-aggregates

Journal Article · Mon Apr 15 00:00:00 EDT 2019 · Bioconjugate Chemistry · OSTI ID:1821493

Mandal, Sarthak; Zhou, Xu; Lin, Su; +2 more

Biomimetic Light Harvesting Complexes Based on Self-Assembled Dye-DNA Nanostructures (Final Technical Report)

Technical Report · Fri Dec 15 00:00:00 EST 2023 · OSTI ID:1821493

Yan, Hao

Photophysics of cyanine dyes: Subnanosecond relaxation dynamics in monomers, dimers, and H- and J-aggregates in solution

Journal Article · Thu Apr 03 00:00:00 EST 1997 · Journal of Physical Chemistry B: Materials, Surfaces, Interfaces, amp Biophysical · OSTI ID:1821493

Khairutdinov, R F; Serpone, N

Related Subjects

71 CLASSICAL AND QUANTUM MECHANICS
GENERAL PHYSICS
59 BASIC BIOLOGICAL SCIENCES
36 MATERIALS SCIENCE
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Excitons
Energy transfer
Genetics
Monomers
Delocalization

Title: Photophysics of J-Aggregate-Mediated Energy Transfer on DNA

Citation Formats

References (53)

Cited By (4)

Similar Records

Related Subjects