Enhanced Light‐Harvesting Capacity by Micellar Assembly of Free Accessory Chromophores and LH1‐like Antennas

Harris, Michelle A.; Sahin, Tuba; Jiang, Jianbing; Vairaprakash, Pothiappan; Parkes‐Loach, Pamela S.; Niedzwiedzki, Dariusz M.; Kirmaier, Christine; Loach, Paul A.; Bocian, David F.; Holten, Dewey; Lindsey, Jonathan S.

doi:10.1111/php.12319

Title: Enhanced Light‐Harvesting Capacity by Micellar Assembly of Free Accessory Chromophores and LH1‐like Antennas

Journal Article · Fri Sep 05 00:00:00 EDT 2014 · Photochemistry and Photobiology

DOI:https://doi.org/10.1111/php.12319· OSTI ID:1144846

Harris, Michelle A. ^[1]; Sahin, Tuba ^[2]; Jiang, Jianbing ^[2]; Vairaprakash, Pothiappan ^[2]; Parkes‐Loach, Pamela S. ^[3]; Niedzwiedzki, Dariusz M. ^[1]; Kirmaier, Christine ^[1]; Loach, Paul A. ^[3]; Bocian, David F. ^[4]; Holten, Dewey ^[1]; Lindsey, Jonathan S. ^[2]

Department of Chemistry Washington University St. Louis MO
Department of Chemistry North Carolina State University Raleigh NC
Department of Molecular Biosciences Northwestern University Evanston IL
Department of Chemistry University of California Riverside CA

AbstractBiohybrid light-harvesting antennas are an emerging platform technology with versatile tailorability for solar-energy conversion. These systems combine the proven peptide scaffold unit utilized for light harvesting by purple photosynthetic bacteria with attached synthetic chromophores to extend solar coverage beyond that of the natural systems. Herein, synthetic unattached chromophores are employed that partition into the organized milieu (e.g. detergent micelles) that house the LH1-like biohybrid architectures. The synthetic chromophores include a hydrophobic boron-dipyrrin dye (A1) and an amphiphilic bacteriochlorin (A2), which transfer energy with reasonable efficiency to the bacteriochlorophyll acceptor array (B875) of the LH1-like cyclic oligomers. The energy-transfer efficiencies are markedly increased upon covalent attachment of a bacteriochlorin (B1 or B2) to the peptide scaffold, where the latter likely acts as an energy-transfer relay site for the (potentially diffusing) free chromophores. The efficiencies are consistent with a Förster (through-space) mechanism for energy transfer. The overall energy-transfer efficiency from the free chromophores via the relay to the target site can approach those obtained previously by relay-assisted energy transfer from chromophores attached at distant sites on the peptides. Thus, the use of free accessory chromophores affords a simple design to enhance the overall light-harvesting capacity of biohybrid LH-like architectures.

Cite

Export

Save

Research Organization:: Washington Univ., St. Louis, MO (United States)

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

DOE Contract Number:: SC0001035

OSTI ID:: 1144846

Report Number(s):: DE-SC0001035-120

Journal Information:: Photochemistry and Photobiology, Vol. 90, Issue 6; ISSN 0031-8655

Publisher:: The American Society of Photobiology

Country of Publication:: United States

Language:: English

References (61)

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
Palette of lipophilic bioconjugatable bacteriochlorins for construction of biohybrid light-harvesting architectures Reddy, Kanumuri Ramesh; Jiang, Jianbing; Krayer, Michael Chemical Science, Vol. 4, Issue 5 https://doi.org/10.1039/c3sc22317e	journal	January 2013
The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum Koepke, Juergen; Hu, Xiche; Muenke, Cornelia Structure, Vol. 4, Issue 5 https://doi.org/10.1016/S0969-2126(96)00063-9	journal	May 1996
Model for the Light-Harvesting Complex I (B875) of Rhodobacter sphaeroides Hu, Xiche; Schulten, Klaus Biophysical Journal, Vol. 75, Issue 2 https://doi.org/10.1016/S0006-3495(98)77558-7	journal	August 1998
Three-Dimensional Structure of the Rhodobacter sphaeroides RC-LH1-PufX Complex: Dimerization and Quinone Channels Promoted by PufX Qian, Pu; Papiz, Miroslav Z.; Jackson, Philip J. Biochemistry, Vol. 52, Issue 43 https://doi.org/10.1021/bi4011946	journal	October 2013
Integration of multiple chromophores with native photosynthetic antennas to enhance solar energy capture and delivery Harris, Michelle A.; Parkes-Loach, Pamela S.; Springer, Joseph W. Chemical Science, Vol. 4, Issue 10 https://doi.org/10.1039/c3sc51518d	journal	January 2013
Versatile design of biohybrid light-harvesting architectures to tune location, density, and spectral coverage of attached synthetic chromophores for enhanced energy capture Harris, Michelle A.; Jiang, Jianbing; Niedzwiedzki, Dariusz M. Photosynthesis Research, Vol. 121, Issue 1 https://doi.org/10.1007/s11120-014-9993-8	journal	March 2014
Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria McDermott, G.; Prince, S. M.; Freer, A. A. Nature, Vol. 374, Issue 6522 https://doi.org/10.1038/374517a0	journal	April 1995
The Structure and Thermal Motion of the B800–850 LH2 Complex from Rps.acidophila at 2.0Å Resolution and 100K: New Structural Features and Functionally Relevant Motions Papiz, Miroslav Z.; Prince, Steve M.; Howard, Tina Journal of Molecular Biology, Vol. 326, Issue 5 https://doi.org/10.1016/S0022-2836(03)00024-X	journal	March 2003
The 8.5 A projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. Karrasch, S.; Bullough, P. A.; Ghosh, R. The EMBO Journal, Vol. 14, Issue 4 https://doi.org/10.1002/j.1460-2075.1995.tb07041.x	journal	February 1995
Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 A resolution Jamieson, S. J. The EMBO Journal, Vol. 21, Issue 15 https://doi.org/10.1093/emboj/cdf410	journal	August 2002
Crystal Structure of the RC-LH1 Core Complex from Rhodopseudomonas palustris Roszak, A. W. Science, Vol. 302, Issue 5652 https://doi.org/10.1126/science.1088892	journal	December 2003
The 8.5Å Projection Structure of the Core RC–LH1–PufX Dimer of Rhodobacter sphaeroides Qian, Pu; Neil Hunter, C.; Bullough, Per A. Journal of Molecular Biology, Vol. 349, Issue 5 https://doi.org/10.1016/j.jmb.2005.04.032	journal	June 2005
Spectroscopic characterization of the light-harvesting complex of Rhodospirillum rubrum and its structural subunit Chang, Mary C.; Callahan, Patricia M.; Parkes-Loach, Pamela S. Biochemistry, Vol. 29, Issue 2 https://doi.org/10.1021/bi00454a017	journal	January 1990
Exciton interactions in the light-harvesting antenna of photosynthetic bacteria studied with triplet-singlet spectroscopy and singlet-triplet annihilation on the B820 subunit form of Rhodospirillum rubrum van Mourik, Frank; van der Oord, Cornelis J. R.; Visscher, Kees J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1059, Issue 1 https://doi.org/10.1016/S0005-2728(05)80193-8	journal	August 1991
Fluorescence polarization and low-temperature absorption spectroscopy of a subunit form of light-harvesting complex I from purple photosynthetic bacteria Visschers, R. W.; Chang, M. C.; Van Mourik, F. Biochemistry, Vol. 30, Issue 23 https://doi.org/10.1021/bi00237a015	journal	June 1991
Selective Detection and Assignment of the Solution NMR Signals of Bacteriochlorophyll a in a Reconstituted Subunit of a Light-Harvesting Complex Wang, Zheng-Yu; Muraoka, Yoshiyuki; Shimonaga, Masahiro Journal of the American Chemical Society, Vol. 124, Issue 6 https://doi.org/10.1021/ja0112994	journal	February 2002
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
Amphiphilic, hydrophilic, or hydrophobic synthetic bacteriochlorins in biohybrid light-harvesting architectures: consideration of molecular designs Jiang, Jianbing; Reddy, Kanumuri Ramesh; Pavan, M. Phani Photosynthesis Research, Vol. 122, Issue 2 https://doi.org/10.1007/s11120-014-0021-9	journal	July 2014
Difluorboryl-Komplexe von Di- und Tripyrrylmethenen Treibs, Alfred; Kreuzer, Franz-Heinrich Justus Liebigs Annalen der Chemie, Vol. 718, Issue 1 https://doi.org/10.1002/jlac.19687180119	journal	December 1968
Synthesis and spectroscopic properties of a new 4-bora-3a,4a-diaza-s-indacene (BODIPY®) dye Kim, Heejin; Burghart, Armin; Welch, Mike B. Chemical Communications, Issue 18 https://doi.org/10.1039/a905739k	journal	January 1999
3,5-Diaryl-4,4-difluoro-4-bora-3a,4a-diaza-s-indacene (BODIPY) Dyes: Synthesis, Spectroscopic, Electrochemical, and Structural Properties Burghart, Armin; Kim, Heejin; Welch, Mike B. The Journal of Organic Chemistry, Vol. 64, Issue 21 https://doi.org/10.1021/jo990796o	journal	October 1999
4,4-Difluoro-4-bora-3a,4a-diaza- s -indacene (BODIPY) Dyes Modified for Extended Conjugation and Restricted Bond Rotations Chen, Jiong; Burghart, Armin; Derecskei-Kovacs, Agnes The Journal of Organic Chemistry, Vol. 65, Issue 10 https://doi.org/10.1021/jo991927o	journal	May 2000
Energy transfer cassettes based on BODIPY® dyes Burghart, Armin; Thoresen, Lars H.; Chen, Jiong Chemical Communications, Issue 22 https://doi.org/10.1039/b006769p	journal	January 2000
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
The Chemistry of Fluorescent Bodipy Dyes: Versatility Unsurpassed Ulrich, Gilles; Ziessel, Raymond; Harriman, Anthony Angewandte Chemie International Edition, Vol. 47, Issue 7 https://doi.org/10.1002/anie.200702070	journal	February 2008
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
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
Enzymic and chemical cleavage of the core light-harvesting polypeptides of photosynthetic bacteria: Determination of the minimal polypeptide size and structure required for subunit and light-harvesting complex formation Meadows, Kelley A.; Iida, Kouji; Tsuda, Kazuichi Biochemistry, Vol. 34, Issue 5 https://doi.org/10.1021/bi00005a012	journal	February 1995
Temperature dependence of the vesicle-micelle transition of egg phosphatidylcholine and octyl glucoside Miguel, Maria da Graca; Eidelman, Ofer; Ollivon, Michel Biochemistry, Vol. 28, Issue 22 https://doi.org/10.1021/bi00448a035	journal	October 1989
De Novo Synthesis of Stable Tetrahydroporphyrinic Macrocycles: Bacteriochlorins and a Tetradehydrocorrin Kim, Han-Je; Lindsey, Jonathan S. The Journal of Organic Chemistry, Vol. 70, Issue 14 https://doi.org/10.1021/jo050467y	journal	July 2005
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
PhotochemCAD: A Computer-Aided Design and Research Tool in Photochemistry Du, Hai; Fuh, Ru-Chun Amy; Li, Junzhong Photochemistry and Photobiology, Vol. 68, Issue 2 https://doi.org/10.1111/j.1751-1097.1998.tb02480.x	journal	August 1998
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
Aqueous–membrane partitioning of β-substituted porphyrins encompassing diverse polarity Soares, Ana R. M.; Thanaiah, Yugaananthy; Taniguchi, Masahiko New Journal of Chemistry, Vol. 37, Issue 4 https://doi.org/10.1039/c3nj41042k	journal	January 2013
One-electron oxidation of photosynthetic pigments in micelles. Bacteriochlorophyll A, chlorophyll A, chlorophyll B, and pheophytin a Chauvet, Jean Paul; Viovy, Roger; Santus, Rene The Journal of Physical Chemistry, Vol. 85, Issue 23 https://doi.org/10.1021/j150623a020	journal	November 1981
Oligomers of bacteriochlorophyll and bacteriopheophytin with spectroscopic properties resembling those found in photosynthetic bacteria Scherz, Avigdor; Parson, William W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 766, Issue 3 https://doi.org/10.1016/0005-2728(84)90127-0	journal	September 1984
Self Assembly of Bacterio Chlorophyll a and Bacteriopheophytin a in Micellar and Non-Micellar Aqueous Solutions; Application to the Pigment-Protein Organization in Light-Harvesting Complexes and Reaction Centers Scherz, A.; Rosenbach-Belkin, V.; Fisher, J. R. E. Perspectives in Photosynthesis https://doi.org/10.1007/978-94-009-0489-7_29	book	January 1990
Permanent hole burning with a diode laser: excited-state dynamics of bacteriochlorophyll in glasses and micelles van der Laan, H.; Smorenburg, H. E.; Schmidt, Th. Journal of the Optical Society of America B, Vol. 9, Issue 6 https://doi.org/10.1364/JOSAB.9.000931	journal	January 1992
Bacteriochlorophyll aggregates in positively charged micelles Gottstein, J.; Scherz, A.; Scheer, H. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1183, Issue 2 https://doi.org/10.1016/0005-2728(93)90247-D	journal	December 1993
The Microenvironment Effect on the Generation of Reactive Oxygen Species by Pd−Bacteriopheophorbide Vakrat-Haglili, Yahel; Weiner, Lev; Brumfeld, Vlad Journal of the American Chemical Society, Vol. 127, Issue 17 https://doi.org/10.1021/ja046210j	journal	May 2005
Supramolecular energy transfer from photoexcited chlorosomal zinc porphyrin self-aggregates to a chlorin or bacteriochlorin monomer as models of main light-harvesting antenna systems in green photosynthetic bacteria Kataoka, Yumiko; Shibata, Yutaka; Tamiaki, Hitoshi Bioorganic & Medicinal Chemistry Letters, Vol. 22, Issue 16 https://doi.org/10.1016/j.bmcl.2012.06.066	journal	August 2012
Stable Synthetic Bacteriochlorins for Photodynamic Therapy: Role of Dicyano Peripheral Groups, Central Metal Substitution (2H, Zn, Pd), and Cremophor EL Delivery Huang, Ying-Ying; Balasubramanian, Thiagarajan; Yang, Eunkyung ChemMedChem, Vol. 7, Issue 12 https://doi.org/10.1002/cmdc.201200351	journal	October 2012
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
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
Self-aggregates of natural chlorophylls and their synthetic analogues in aqueous media for making light-harvesting systems Miyatake, Tomohiro; Tamiaki, Hitoshi Coordination Chemistry Reviews, Vol. 254, Issue 21-22 https://doi.org/10.1016/j.ccr.2009.12.027	journal	November 2010
Fluorescence and Absorption Spectroscopic Properties of Dipyrrometheneboron Difluoride (BODIPY) Derivatives in Liquids, Lipid Membranes, and Proteins Karolin, Jan; Johansson, Lennart B. -A.; Strandberg, Leif Journal of the American Chemical Society, Vol. 116, Issue 17 https://doi.org/10.1021/ja00096a042	journal	August 1994
New BODIPY lipid probes for fluorescence studies of membranes Boldyrev, Ivan A.; Zhai, Xiuhong; Momsen, Maureen M. Journal of Lipid Research, Vol. 48, Issue 7 https://doi.org/10.1194/jlr.M600459-JLR200	journal	April 2007
Light-Harvesting and Photocurrent Generation by Gold Electrodes Modified with Mixed Self-Assembled Monolayers of Boron−Dipyrrin and Ferrocene−Porphyrin−Fullerene Triad Imahori, Hiroshi; Norieda, Hiroyuki; Yamada, Hiroko Journal of the American Chemical Society, Vol. 123, Issue 1 https://doi.org/10.1021/ja002154k	journal	January 2001
Preparation and characterization of multi-cationic BODIPYs and their synthetically versatile precursors Bartelmess, Juergen; Weare, Walter W. Dyes and Pigments, Vol. 97, Issue 1 https://doi.org/10.1016/j.dyepig.2012.11.017	journal	April 2013
Synthesis and properties of amphiphilic BODIPY derivatives bearing hydroxyl groups Vincent, Matthew; Beabout, Eva; Bennett, Richard Tetrahedron Letters, Vol. 54, Issue 16 https://doi.org/10.1016/j.tetlet.2013.01.128	journal	April 2013
Preparation of BODIPY probes for multicolor fluorescence imaging studies of membrane dynamics Yamada, Koji; Toyota, Taro; Takakura, Katsuto New Journal of Chemistry, Vol. 25, Issue 5 https://doi.org/10.1039/b100757m	journal	January 2001
Architecture and mechanism of the light-harvesting apparatus of purple bacteria Hu, X.; Damjanovic, A.; Ritz, T. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.5935	journal	May 1998
Direct Visualization of Exciton Reequilibration in the LH1 and LH2 Complexes of Rhodobacter sphaeroides by Multipulse Spectroscopy Cohen Stuart, Thomas A.; Vengris, Mikas; Novoderezhkin, Vladimir I. Biophysical Journal, Vol. 100, Issue 9 https://doi.org/10.1016/j.bpj.2011.02.048	journal	May 2011
Interaction of membrane proteins and lipids with solubilizing detergents le Maire, Marc; Champeil, Philippe; Møller, Jesper V. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1508, Issue 1-2 https://doi.org/10.1016/S0304-4157(00)00010-1	journal	November 2000
Insight into the Structure of Light-Harvesting Complex II and Its Stabilization in Detergent Solution Cardoso, Mateus B.; Smolensky, Dmitriy; Heller, William T. The Journal of Physical Chemistry B, Vol. 113, Issue 51 https://doi.org/10.1021/jp905050b	journal	December 2009
Detergent Structure in Crystals of the Integral Membrane Light-harvesting Complex LH2 from Rhodopseudomonas acidophila Strain 10050 Prince, S. M.; Howard, T. D.; Myles, D. A. A. Journal of Molecular Biology, Vol. 326, Issue 1 https://doi.org/10.1016/S0022-2836(02)01361-X	journal	February 2003
Detergent structure in crystals of a bacterial photosynthetic reaction centre Roth, M.; Lewit-Bentley, A.; Michel, H. Nature, Vol. 340, Issue 6235 https://doi.org/10.1038/340659a0	journal	August 1989
Detergent structure in tetragonal crystals of OmpF porin Pebay-Peyroula, E.; Garavito, Rm; Rosenbusch, Jp Structure, Vol. 3, Issue 10 https://doi.org/10.1016/S0969-2126(01)00241-6	journal	October 1995
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
Synthesis and Physicochemical Properties of Metallobacteriochlorins Chen, Chih-Yuan; Sun, Erjun; Fan, Dazhong Inorganic Chemistry, Vol. 51, Issue 17 https://doi.org/10.1021/ic301262k	journal	August 2012

Similar Records

Expanding Covalent Attachment Sites of Nonnative Chromophores to Encompass the C-Terminal Hydrophilic Domain in Biohybrid Light-Harvesting Architectures

Journal Article · Sun Dec 31 00:00:00 EST 2017 · ChemPhotoChem · OSTI ID:1144846

Hood, Don; Sahin, Tuba; Parkes-Loach, Pamela S.; +9 more

Integration of multiple chromophores with native photosynthetic antennas to enhance solar energy capture and delivery

Journal Article · Tue Jan 01 00:00:00 EST 2013 · Chemical Science · OSTI ID:1144846

Harris, Michelle A.; Parkes-Loach, Pamela S.; Springer, Joseph W.; +12 more

Contact heterogeneities in feral swine: implications for disease management and future research

Journal Article · Thu Mar 17 00:00:00 EDT 2016 · Ecosphere · OSTI ID:1144846

Pepin, Kim M.; Davis, Amy J.; Beasley, James; +10 more

Related Subjects

14 SOLAR ENERGY

Title: Enhanced Light‐Harvesting Capacity by Micellar Assembly of Free Accessory Chromophores and LH1‐like Antennas

Citation Formats

References (61)

Similar Records

Related Subjects