Directional Photonic Wire Mediated by Homo-Förster Resonance Energy Transfer on a DNA Origami Platform.

Elaborating efficient strategies and deepening the understanding of light transport at the nanoscale is of great importance for future designs of artificial light-harvesting assemblies and dye-based photonic circuits. In this work, we focus on studying the phenomenon of Förster resonance energy transfer (FRET) among fluorophores of the same kind (homo-FRET) and its implications for energy cascades containing two or three different dye molecules. Utilizing the spatial programmability of DNA origami, we arranged a chain of cyanine 3 (Cy3) dyes flanked at one end with a dye of lower excitation energy, cyanine 5 (Cy5), with or without an additional dye of higher excitation energy, Alexa488, at the other end. We characterized the response of our fluorophore assemblies with bulk and single-molecule spectroscopy and support our measurements by Monte Carlo modeling of energy transfer within the system. We find that, depending on the arrangement of the fluorophores, homo-FRET between the Cy3 dyes can lead to an overall enhanced energy transfer to the acceptor fluorophore. Furthermore, we systematically analyzed the homo-FRET system by addressing the fluorescence lifetime and anisotropy. Finally, we built a homo-FRET-mediated photonic wire capable of transferring energy through the homo-FRET system from the blue donor dye (Alexa488) to the red acceptor fluorophore (Cy5) across a total distance of 16 nm.

[1]  Igor L. Medintz,et al.  FRET from Multiple Pathways in Fluorophore-Labeled DNA , 2016 .

[2]  M. Fischer,et al.  Metal-free organic dyes for dye-sensitized solar cells: from structure: property relationships to design rules. , 2009, Angewandte Chemie.

[3]  Tao Zhang,et al.  DNA-Based Self-Assembly of Fluorescent Nanodiamonds. , 2015, Journal of the American Chemical Society.

[4]  Yusuke Kuramochi,et al.  Energy transfer among light-harvesting macrorings incorporated into a bilayer membrane. , 2009, Journal of the American Chemical Society.

[5]  Graham R Fleming,et al.  Lessons from nature about solar light harvesting. , 2011, Nature chemistry.

[6]  Sheshanath V. Bhosale,et al.  Photoproduction of Proton Gradients with π-Stacked Fluorophore Scaffolds in Lipid Bilayers , 2006, Science.

[7]  Igor L. Medintz,et al.  Assembling programmable FRET-based photonic networks using designer DNA scaffolds , 2014, Nature Communications.

[8]  K Schulten,et al.  Architecture and mechanism of the light-harvesting apparatus of purple bacteria. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  B. Valeur,et al.  Fluorescence depolarization by electronic energy transfer in donor–acceptor pairs of like and unlike chromophores , 1991 .

[10]  Tao Zhang,et al.  Hierarchical assembly of metal nanoparticles, quantum dots and organic dyes using DNA origami scaffolds. , 2013, Nature nanotechnology.

[11]  T. G. Martin,et al.  Facile and Scalable Preparation of Pure and Dense DNA Origami Solutions , 2014, Angewandte Chemie.

[12]  Richard G. Crisp,et al.  Theory of Directed Electronic Energy Transfer , 2006, Journal of Fluorescence.

[13]  Igor L. Medintz,et al.  Extending DNA‐Based Molecular Photonic Wires with Homogeneous Förster Resonance Energy Transfer , 2016 .

[14]  G. Calzaferri,et al.  Photon harvesting by excimer-forming multichromophores. , 2012, Chemical communications.

[15]  T. G. Martin,et al.  Cryo-EM structure of a 3D DNA-origami object , 2012, Proceedings of the National Academy of Sciences.

[16]  B. Albinsson,et al.  Self-assembled DNA photonic wire for long-range energy transfer. , 2008, Journal of the American Chemical Society.

[17]  P. Rothemund.  Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[18]  G. Weber.  Dependence of the polarization of the fluorescence on the concentration , 1954 .

[19]  B. Albinsson,et al.  Functionalized DNA Nanostructures for Light Harvesting and Charge Separation , 2012 .

[20]  Graham R Fleming,et al.  Dynamics of light harvesting in photosynthesis. , 2009, Annual review of physical chemistry.

[21]  Philip Tinnefeld,et al.  Single-molecule four-color FRET visualizes energy-transfer paths on DNA origami. , 2011, Journal of the American Chemical Society.

[22]  Joachim O. Rädler,et al.  Shape and Interhelical Spacing of DNA Origami Nanostructures Studied by Small-Angle X-ray Scattering. , 2016, Nano letters.

[23]  A. van der Vaart,et al.  Cy3-DNA stacking interactions strongly depend on the identity of the terminal basepair. , 2011, Biophysical journal.

[24]  J. Post,et al.  Imaging molecular interactions in cells by dynamic and static fluorescence anisotropy (rFLIM and emFRET). , 2003, Biochemical Society transactions.

[25]  D. Lilley,et al.  Orientation dependence in fluorescent energy transfer between Cy3 and Cy5 terminally attached to double-stranded nucleic acids , 2008, Proceedings of the National Academy of Sciences.

[26]  M. Somoza,et al.  Sequence-Dependent Fluorescence of Cy3- and Cy5-Labeled Double-Stranded DNA , 2016, Bioconjugate chemistry.

[27]  Tim Liedl,et al.  Single-molecule FRET ruler based on rigid DNA origami blocks. , 2011, Chemphyschem : a European journal of chemical physics and physical chemistry.

[28]  L. Runnels,et al.  Theory and application of fluorescence homotransfer to melittin oligomerization. , 1995, Biophysical journal.

[29]  M. Nango,et al.  Construction and Photocurrent of Light-harvesting Polypeptides/Zinc Bacteriochlorophyll a Complex in Lipid Bilayers , 2003 .

[30]  Vassili Ivanov,et al.  Impact of emission anisotropy on fluorescence spectroscopy and FRET distance measurements. , 2009, Biophysical journal.

[31]  Hieu Bui,et al.  DNA-Controlled Excitonic Switches , 2012, Nano letters.

[32]  Elisa A. Hemmig,et al.  Proximity-Induced H-Aggregation of Cyanine Dyes on DNA-Duplexes. , 2016, The journal of physical chemistry. A.

[33]  Brittany L. Cannon,et al.  Excitonic AND Logic Gates on DNA Brick Nanobreadboards , 2015, ACS photonics.

[34]  Philip Mair,et al.  Programming Light-Harvesting Efficiency Using DNA Origami , 2016, Nano letters.

[35]  A. Meller,et al.  The Effect of dye-dye interactions on the spatial resolution of single-molecule FRET measurements in nucleic acids. , 2010, Biophysical journal.

[36]  R. Cogdell,et al.  Selective assembly of photosynthetic antenna proteins into a domain-structured lipid bilayer for the construction of artificial photosynthetic antenna systems: structural analysis of the assembly using surface plasmon resonance and atomic force microscopy. , 2011, Langmuir.

[37]  A. van der Vaart,et al.  Photophysical and dynamical properties of doubly linked Cy3-DNA constructs. , 2014, The journal of physical chemistry. B.

[38]  T. Brown,et al.  Self-assembled DNA-based fluorescence waveguide with selectable output. , 2011, Small.

[39]  Volodymyr Kudryavtsev,et al.  Combining MFD and PIE for accurate single-pair Förster resonance energy transfer measurements. , 2012, Chemphyschem : a European journal of chemical physics and physical chemistry.

[40]  Gregory D Scholes,et al.  Long-range resonance energy transfer in molecular systems. , 2003, Annual review of physical chemistry.

[41]  Shawn M. Douglas,et al.  DNA-nanotube-induced alignment of membrane proteins for NMR structure determination , 2007, Proceedings of the National Academy of Sciences.

[42]  Hao Yan,et al.  DNA-directed artificial light-harvesting antenna. , 2011, Journal of the American Chemical Society.

[43]  Igor L. Medintz,et al.  Resonance energy transfer in DNA duplexes labeled with localized dyes. , 2014, The journal of physical chemistry. B.

[44]  D. S. Bradshaw,et al.  Resonance energy transfer: The unified theory revisited , 2003 .

[45]  Monika A. Ciuba,et al.  Demystifying PIFE: The Photophysics Behind the Protein-Induced Fluorescence Enhancement Phenomenon in Cy3. , 2015, The journal of physical chemistry letters.

[46]  N. Seeman.  Nanomaterials based on DNA. , 2010, Annual review of biochemistry.

[47]  K. Nelson,et al.  Virus-templated assembly of porphyrins into light-harvesting nanoantennae. , 2010, Journal of the American Chemical Society.

[48]  Shawn M. Douglas,et al.  Self-assembly of DNA into nanoscale three-dimensional shapes , 2009, Nature.

[49]  Masoud Mohseni,et al.  Enhanced energy transport in genetically engineered excitonic networks. , 2016, Nature materials.

[50]  Mike Heilemann,et al.  Design of molecular photonic wires based on multistep electronic excitation transfer. , 2005, Chemphyschem : a European journal of chemical physics and physical chemistry.

[51]  M. Levitus,et al.  Nucleobase-Specific Enhancement of Cy3 Fluorescence , 2009, Journal of Fluorescence.

[52]  M. Sanborn,et al.  Fluorescence properties and photophysics of the sulfoindocyanine Cy3 linked covalently to DNA. , 2007, The journal of physical chemistry. B.