Self-Assembled Light-Harvesting System from Chromophores in Lipid Vesicles

Sahin, Tuba; Harris, Michelle A.; Vairaprakash, Pothiappan; Niedzwiedzki, Dariusz M.; Subramanian, Vijaya; Shreve, Andrew P.; Bocian, David F.; Holten, Dewey; Lindsey, Jonathan S.

doi:10.1021/acs.jpcb.5b04841

Self-Assembled Light-Harvesting System from Chromophores in Lipid Vesicles

Journal Article · Fri Jul 31 00:00:00 EDT 2015 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.5b04841· OSTI ID:1386028

Sahin, Tuba ^[1]; Harris, Michelle A. ^[2]; Vairaprakash, Pothiappan ^[1]; Niedzwiedzki, Dariusz M. ^[1]; Subramanian, Vijaya ^[3]; Shreve, Andrew P. ^[3]; Bocian, David F. ^[4]; Holten, Dewey ^[2]; Lindsey, Jonathan S. ^[1]

North Carolina State Univ., Raleigh, NC (United States)
Washington Univ., St. Louis, MO (United States)
Univ. of New Mexico, Albuquerque, NM (United States)
Univ. of California, Riverside, CA (United States)

Lipid vesicles are used as the organizational structure of self-assembled light-harvesting systems. Following analysis of 17 chromophores, six were selected for inclusion in vesicle-based antennas. The complementary absorption features of the chromophores span the near-ultraviolet, visible, and near-infrared region. Although the overall concentration of the pigments is low (~1 μM for quantitative spectroscopic studies) in a cuvette, the lipid-vesicle system affords high concentration (≥10 mM) in the bilayer for efficient energy flow from donor to acceptor. Energy transfer was characterized in 13 representative binary mixtures using static techniques (fluorescence–excitation versus absorptance spectra, quenching of donor fluorescence, modeling emission spectra of a mixture versus components) and time-resolved spectroscopy (fluorescence, ultrafast absorption). Binary donor–acceptor systems that employ a boron-dipyrrin donor (S₀ ↔ S₁ absorption/emission in the blue-green) and a chlorin or bacteriochlorin acceptor (S₀ ↔ S₁ absorption/emission in the red or near-infrared) have an average excitation-energy-transfer efficiency (Φ_EET) of ~50%. Binary systems with a chlorin donor and a chlorin or bacteriochlorin acceptor have Φ_EET ~ 85%. The differences in Φ_EET generally track the donor-fluorescence/acceptor-absorption spectral overlap within a dipole–dipole coupling (Förster) mechanism. Substantial deviation from single-exponential decay of the excited donor (due to the dispersion of donor–acceptor distances) is expected and observed. The time profiles and resulting Φ_EET are modeled on the basis of (Förster) energy transfer between chromophores relatively densely packed in a two-dimensional compartment. Initial studies of two ternary and one quaternary combination of chromophores show the enhanced spectral coverage and energy-transfer efficacy expected on the basis of the binary systems. Collectively, this approach may provide one of the simplest designs for self-assembled light-harvesting systems that afford broad solar collection and efficient energy transfer.

View Accepted Manuscript (DOE)

Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC); Washington Univ., St. Louis, MO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0001035

OSTI ID:: 1386028

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Journal Name: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry Journal Issue: 32 Vol. 119; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Palladium-Catalyzed Coupling Reactions for the Functionalization of BODIPY Dyes with Fluorescence Spanning the Visible Spectrum Rohand, Taoufik; Qin, Wenwu; Boens, Noël European Journal of Organic Chemistry, Vol. 2006, Issue 20 https://doi.org/10.1002/ejoc.200600531	journal	October 2006
Light-Harvesting Antennas in Photosynthesis Green, Beverley R.; Parson, William W. Advances in Photosynthesis and Respiration https://doi.org/10.1007/978-94-017-2087-8	book	January 2003
Chlorins Programmed for Self-Assembly Balaban, Teodor Silviu; Tamiaki, Hitoshi; Holzwarth, Alfred R. Supermolecular Dye Chemistry https://doi.org/10.1007/b137480	book	January 2005
Nile red as a polarity-sensitive fluorescent probe of hydrophobic protein surfaces Sackett, Dan L.; Wolff, J. Analytical Biochemistry, Vol. 167, Issue 2 https://doi.org/10.1016/0003-2697(87)90157-6	journal	December 1987
Fluorescence quantum yield of oxazine and carbazine laser dyes Sens, Rüdiger; Drexhage, Karl H. Journal of Luminescence, Vol. 24-25 https://doi.org/10.1016/0022-2313(81)90075-2	journal	November 1981
Fluorescence quantum yields of some rhodamine dyes Kubin, R. F.; Fletcher, A. N. Journal of Luminescence, Vol. 27, Issue 4 https://doi.org/10.1016/0022-2313(82)90045-X	journal	December 1982
Porphyrins Seybold, Paul G.; Gouterman, Martin Journal of Molecular Spectroscopy, Vol. 31, Issue 1-13 https://doi.org/10.1016/0022-2852(69)90335-X	journal	January 1969
Photophysical properties of porphyrins in biological membranes Ricchelli, Fernanda Journal of Photochemistry and Photobiology B: Biology, Vol. 29, Issue 2-3 https://doi.org/10.1016/1011-1344(95)07155-U	journal	August 1995
Recent Advances in Free and Metalated Multiporphyrin Assemblies and Arrays; A Photophysical Behavior and Energy Transfer Perspective Harvey, Pierre D. The Porphyrin Handbook https://doi.org/10.1016/B978-0-08-092392-5.50008-0	book	January 2003
The Depth of Porphyrin in a Membrane and the Membrane’s Physical Properties Affect the Photosensitizing Efficiency Lavi, Adina; Weitman, Hana; Holmes, Robert T. Biophysical Journal, Vol. 82, Issue 4 https://doi.org/10.1016/S0006-3495(02)75557-4	journal	April 2002
An analytic solution to the Förster energy transfer problem in two dimensions Wolber, P. K.; Hudson, B. S. Biophysical Journal, Vol. 28, Issue 2 https://doi.org/10.1016/S0006-3495(79)85171-1	journal	November 1979
Characteristics of self-quenching of the fluorescence of lipid-conjugated rhodamine in membranes. MacDonald, R. I. Journal of Biological Chemistry, Vol. 265, Issue 23 https://doi.org/10.1016/S0021-9258(18)77380-8	journal	August 1990
Structure of lipid bilayers Nagle, John F.; Tristram-Nagle, Stephanie Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 1469, Issue 3 https://doi.org/10.1016/S0304-4157(00)00016-2	journal	November 2000
Photoinduced Charge Separation in Lipid Bilayers Mauzerall, D.; Sun, K. Membrane Science and Technology https://doi.org/10.1016/S0927-5193(03)80058-X	book	January 2003
Sparsely substituted chlorins as core constructs in chlorophyll analogue chemistry. Part 1: Synthesis Ptaszek, Marcin; McDowell, Brian E.; Taniguchi, Masahiko Tetrahedron, Vol. 63, Issue 18 https://doi.org/10.1016/j.tet.2007.02.038	journal	April 2007
Sparsely substituted chlorins as core constructs in chlorophyll analogue chemistry. Part 3: Spectral and structural properties Taniguchi, Masahiko; Ptaszek, Marcin; McDowell, Brian E. Tetrahedron, Vol. 63, Issue 18 https://doi.org/10.1016/j.tet.2007.02.040	journal	April 2007
Titrimetric and Equilibrium Studies Using Indicators Related to Nile Blue A. Davis, M. M.; Helzer, H. B. Analytical Chemistry, Vol. 38, Issue 3 https://doi.org/10.1021/ac60235a020	journal	March 1966
Tailoring Porphyrins and Chlorins for Self-Assembly in Biomimetic Artificial Antenna Systems Balaban, Teodor Silviu Accounts of Chemical Research, Vol. 38, Issue 8 https://doi.org/10.1021/ar040211z	journal	August 2005
Discrete Cyclic Porphyrin Arrays as Artificial Light-Harvesting Antenna Aratani, Naoki; Kim, Dongho; Osuka, Atsuhiro Accounts of Chemical Research, Vol. 42, Issue 12 https://doi.org/10.1021/ar9001697	journal	December 2009
Probing Electronic Communication in Covalently Linked Multiporphyrin Arrays. A Guide to the Rational Design of Molecular Photonic Devices Holten, Dewey; Bocian, David F.; Lindsey, Jonathan S. Accounts of Chemical Research, Vol. 35, Issue 1 https://doi.org/10.1021/ar970264z	journal	January 2002
Low-Density Lipoprotein Reconstituted by Pyropheophorbide Cholesteryl Oleate as Target-Specific Photosensitizer Zheng, Gang; Li, Hui; Zhang, Min Bioconjugate Chemistry, Vol. 13, Issue 3 https://doi.org/10.1021/bc025516h	journal	May 2002
Fluorescence method for measuring the kinetics of fusion between biological membranes Hoekstra, Dick; De Boer, Tiny; Klappe, Karin Biochemistry, Vol. 23, Issue 24 https://doi.org/10.1021/bi00319a002	journal	November 1984
BODIPY Dyes and Their Derivatives: Syntheses and Spectroscopic Properties Loudet, Aurore; Burgess, Kevin Chemical Reviews, Vol. 107, Issue 11 https://doi.org/10.1021/cr078381n	journal	November 2007
3,5-Diformylboron Dipyrromethenes as Fluorescent pH Sensors Madhu, Sheri; Rao, Malakalapalli Rajeswara; Shaikh, Mushtaque S. Inorganic Chemistry, Vol. 50, Issue 10 https://doi.org/10.1021/ic102499h	journal	May 2011
Absolute luminescence yield of cresyl violet. A standard for the red Magde, Douglas.; Brannon, James H.; Cremers, Teresa L. The Journal of Physical Chemistry, Vol. 83, Issue 6 https://doi.org/10.1021/j100469a012	journal	March 1979
Fluorescence and absorption studies on chlorophyll a in vitro at 77.deg.K Singhal, G. S.; Williams, W. P.; Rabinowitch, Eugene The Journal of Physical Chemistry, Vol. 72, Issue 12 https://doi.org/10.1021/j100858a002	journal	November 1968
Structural Control of the Excited-State Dynamics of Bis(dipyrrinato)zinc Complexes: Self-Assembling Chromophores for Light-Harvesting Architectures Sazanovich, Igor V.; Kirmaier, Christine; Hindin, Eve Journal of the American Chemical Society, Vol. 126, Issue 9 https://doi.org/10.1021/ja038763k	journal	March 2004
Biohybrid Photosynthetic Antenna Complexes for Enhanced Light-Harvesting Springer, Joseph W.; Parkes-Loach, Pamela S.; Reddy, Kanumuri Ramesh Journal of the American Chemical Society, Vol. 134, Issue 10 https://doi.org/10.1021/ja207390y	journal	February 2012
Synthesis of covalently linked dimeric derivatives of chlorophyll a, pyrochlorophyll a, chlorophyll b, and bacteriochlorophyll a Wasielewski, Michael R.; Svec, Walter A. The Journal of Organic Chemistry, Vol. 45, Issue 10 https://doi.org/10.1021/jo01298a043	journal	May 1980
Synthetic Chlorins Bearing Auxochromes at the 3- and 13-Positions Laha, Joydev K.; Muthiah, Chinnasamy; Taniguchi, Masahiko The Journal of Organic Chemistry, Vol. 71, Issue 11 https://doi.org/10.1021/jo060208o	journal	May 2006
Rational Synthesis of Meso-Substituted Porphyrins Bearing One Nitrogen Heterocyclic Group Gryko, Dorota; Lindsey, Jonathan S. The Journal of Organic Chemistry, Vol. 65, Issue 7 https://doi.org/10.1021/jo9918100	journal	April 2000
Refractive Index Dependence of the Förster Resonance Excitation Transfer Rate Knox, Robert S.; van Amerongen, Herbert The Journal of Physical Chemistry B, Vol. 106, Issue 20 https://doi.org/10.1021/jp013927+	journal	April 2002
Giant Multiporphyrin Arrays as Artificial Light-Harvesting Antennas Imahori, Hiroshi The Journal of Physical Chemistry B, Vol. 108, Issue 20 https://doi.org/10.1021/jp038036b	journal	May 2004
Excited-State Energy Flow in Covalently Linked Multiporphyrin Arrays: The Essential Contribution of Energy Transfer between Nonadjacent Chromophores Hindin, Eve; Forties, Robert A.; Loewe, Robert S. The Journal of Physical Chemistry B, Vol. 108, Issue 34 https://doi.org/10.1021/jp047803j	journal	August 2004
Structural Control of the Photodynamics of Boron−Dipyrrin Complexes Kee, Hooi Ling; Kirmaier, Christine; Yu, Lianhe The Journal of Physical Chemistry B, Vol. 109, Issue 43 https://doi.org/10.1021/jp0525078	journal	November 2005
Photophysical Properties and Electronic Structure of Stable, Tunable Synthetic Bacteriochlorins: Extending the Features of Native Photosynthetic Pigments Yang, Eunkyung; Kirmaier, Christine; Krayer, Michael The Journal of Physical Chemistry B, Vol. 115, Issue 37 https://doi.org/10.1021/jp205258s	journal	September 2011
Self-Assembling Properties of Porphyrinic Photosensitizers and Their Effect on Membrane Interactions Probed by NMR Spectroscopy Vermathen, Martina; Marzorati, Mattia; Bigler, Peter The Journal of Physical Chemistry B, Vol. 117, Issue 23 https://doi.org/10.1021/jp403331n	journal	May 2013
First Steps in Photophysics. I. Fluorescence Yield and Radiative Rate Coefficient of 9,10-Bis(phenylethynyl)anthracene in Paraffins Demeter, Attila The Journal of Physical Chemistry A, Vol. 118, Issue 43 https://doi.org/10.1021/jp507626h	journal	October 2014
Extending the Short and Long Wavelength Limits of Bacteriochlorin Near-Infrared Absorption via Dioxo- and Bisimide-Functionalization Vairaprakash, Pothiappan; Yang, Eunkyung; Sahin, Tuba The Journal of Physical Chemistry B, Vol. 119, Issue 12 https://doi.org/10.1021/jp512818g	journal	March 2015
Diblock Copolymer Micelles and Supported Films with Noncovalently Incorporated Chromophores: A Modular Platform for Efficient Energy Transfer Adams, Peter G.; Collins, Aaron M.; Sahin, Tuba Nano Letters, Vol. 15, Issue 4 https://doi.org/10.1021/nl504814x	journal	March 2015
Conjugated porphyrin arrays: synthesis, properties and applications for functional materials Tanaka, Takayuki; Osuka, Atsuhiro Chemical Society Reviews, Vol. 44, Issue 4 https://doi.org/10.1039/C3CS60443H	journal	January 2015
The localization and photosensitization of modified chlorin photosensitizers in artificial membranes Dror, Shimshon Ben; Bronshtein, Irena; Garini, Yuval Photochemical & Photobiological Sciences, Vol. 8, Issue 3 https://doi.org/10.1039/b814970d	journal	January 2009
De novo synthesis and properties of analogues of the self-assembling chlorosomal bacteriochlorophylls Mass, Olga; Pandithavidana, Dinesh R.; Ptaszek, Marcin New Journal of Chemistry, Vol. 35, Issue 11 https://doi.org/10.1039/c1nj20611g	journal	January 2011
Self-organization of tetrapyrrole constituents to give a photoactive protocell Soares, Ana R. M.; Taniguchi, Masahiko; Chandrashaker, Vanampally Chemical Science, Vol. 3, Issue 6 https://doi.org/10.1039/c2sc01120d	journal	January 2012
Amphiphilic chlorins and bacteriochlorins in micellar environments. Molecular design, de novo synthesis, and photophysical properties Aravindu, Kunche; Mass, Olga; Vairaprakash, Pothiappan Chemical Science, Vol. 4, Issue 9 https://doi.org/10.1039/c3sc51335a	journal	January 2013
Nonlinear partial differential equations and applications: Invisible liposomes: Refractive index matching with sucrose enables flow dichroism assessment of peptide orientation in lipid vesicle membrane Ardhammar, M.; Lincoln, P.; Norden, B. Proceedings of the National Academy of Sciences, Vol. 99, Issue 24 https://doi.org/10.1073/pnas.192583499	journal	November 2002
Energy transfer: a spectroscopic ruler. Stryer, L.; Haugland, R. P. Proceedings of the National Academy of Sciences, Vol. 58, Issue 2 https://doi.org/10.1073/pnas.58.2.719	journal	August 1967
Metal-mediated Discrete Supramolecular Assemblies of Porphyrins Alessio, Enzo; Iengo, Elisabetta; Marzilli, Luigi G. Supramolecular Chemistry, Vol. 14, Issue 2-3 https://doi.org/10.1080/10610270290026004	journal	March 2002
Energetics of Photophysical Processes in Chlorophyll-Like Molecules Gradyushko, A. T.; Sevchenko, A. N.; Solovyov, K. N. Photochemistry and Photobiology, Vol. 11, Issue 6 https://doi.org/10.1111/j.1751-1097.1970.tb06011.x	journal	June 1970
PhotochemCAD 2: A Refined Program with Accompanying Spectral Databases for Photochemical Calculations¶ Dixon, James M.; Taniguchi, Masahiko; Lindsey, Jonathan S. Photochemistry and Photobiology, Vol. 81, Issue 1 https://doi.org/10.1111/j.1751-1097.2005.tb01544.x	journal	January 2005
Enhanced Light-Harvesting Capacity by Micellar Assembly of Free Accessory Chromophores and LH1-like Antennas Harris, Michelle A.; Sahin, Tuba; Jiang, Jianbing Photochemistry and Photobiology, Vol. 90, Issue 6 https://doi.org/10.1111/php.12319	journal	September 2014
Förster’s resonance excitation transfer theory: not just a formula Knox, Robert S. Journal of Biomedical Optics, Vol. 17, Issue 1 https://doi.org/10.1117/1.JBO.17.1.011003	journal	January 2012
Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement Blankenship, R. E.; Tiede, D. M.; Barber, J. Science, Vol. 332, Issue 6031, p. 805-809 https://doi.org/10.1126/science.1200165	journal	May 2011
Boron-dipyrromethene dyes for incorporation in synthetic multi-pigment light-harvesting arrays Wagner, R. W.; Lindsey, J. S. Pure and Applied Chemistry, Vol. 68, Issue 7 https://doi.org/10.1351/pac199668071373	journal	January 1996
Experimentelle und theoretische Untersuchung des zwischenmolekularen Übergangs von Elektronenanregungsenergie Förster, Theodor Zeitschrift für Naturforschung A, Vol. 4, Issue 5 https://doi.org/10.1515/zna-1949-0501	journal	May 1949
Ein einfaches Verfahren zur Messung kleinster Jodkonzentrationen, Jod- und Natriumthiosulfatmengen in Lösungen Ehmert, Alfred Zeitschrift für Naturforschung B, Vol. 4, Issue 6 https://doi.org/10.1515/znb-1949-0603	journal	December 1949
Photodynamic activity of pyropheophorbide methyl ester and pyropheophorbide a in dimethylformamide solution Al-Omari, S.; Ali, A. General Physiology and Biophysics, Vol. 28, Issue 1 https://doi.org/10.4149/gpb_2009_01_70	journal	January 2009

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Self-Assembled Light-Harvesting System from Chromophores in Lipid Vesicles

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