Robust light harvesting by a noisy antenna

Malý, Pavel; Gardiner, Alastair T.; Cogdell, Richard J.; van Grondelle, Rienk; Mančal, Tomáš

doi:10.1039/C7CP06139K

Robust light harvesting by a noisy antenna

Journal Article · Sun Dec 31 23:00:00 EST 2017 · Physical Chemistry Chemical Physics. PCCP

DOI:https://doi.org/10.1039/C7CP06139K· OSTI ID:1418068

^[1]; ^[2]; ^[2]; van Grondelle, Rienk ^[1]; ^[3]

Department of Biophysics, Faculty of Sciences, Vrije Universiteit Amsterdam, 1081HV Amsterdam, The Netherlands
Institute of Molecular, Cellular and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow
Faculty of Mathematics and Physics, Charles University, 121 16 Prague, Czech Republic

Ultrafast bulk and single-molecule spectroscopy experiments described by a single theoretical model show how protein fluctuations influence photosynthetic light harvesting.

View Journal Article

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

Grant/Contract Number:: SC0001035

OSTI ID:: 1418068

Journal Information:: Physical Chemistry Chemical Physics. PCCP, Journal Name: Physical Chemistry Chemical Physics. PCCP Journal Issue: 6 Vol. 20; ISSN 1463-9076; ISSN PPCPFQ

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (62)

Charge and Energy Transfer Dynamics in Molecular Systems May, Volkhard; Kühn, Oliver Wiley-VCH Verlag GmbH & Co. KGaA https://doi.org/10.1002/9783527633791	book	February 2011
Molecular Excitation Dynamics and Relaxation Valkunas, Leonas; Abramavicius, Darius; Mančal, Tomáš Wiley‐VCH Verlag GmbH & Co. https://doi.org/10.1002/9783527653652	book	January 2013
Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems Berera, Rudi; van Grondelle, Rienk; Kennis, John T. M. Photosynthesis Research, Vol. 101, Issue 2-3 https://doi.org/10.1007/s11120-009-9454-y	journal	July 2009
Light-harvesting in photosystem I Croce, Roberta; van Amerongen, Herbert Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9838-x	journal	May 2013
Size and structure of antenna complexes of photosynthetic bacteria as studied by singlet-singlet quenching of the bacteriochlorophyll fluorescence yield Van Grondelle, Rienk; Hunter, C. Neil; Bakker, Jacques G. C. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 723, Issue 1 https://doi.org/10.1016/0005-2728(83)90005-1	journal	April 1983
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Excitation energy transfer, trapping and annihilation in photosynthetic systems van Grondelle, R. Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 811, Issue 2 https://doi.org/10.1016/0304-4173(85)90017-5	journal	June 1985
Preparation, Purification, and Crystallization of Purple Bacteria Antenna Complexes Cogdell, Richard J.; Hawthornthwaite, Anna M. Photosynthetic Reaction Center https://doi.org/10.1016/B978-0-12-208661-8.50008-5	book	January 1993
Spectroscopy of Individual Light-Harvesting 2 Complexes of Rhodopseudomonas acidophila: Diagonal Disorder, Intercomplex Heterogeneity, Spectral Diffusion, and Energy Transfer in the B800 Band van Oijen, A. M.; Ketelaars, M.; Köhler, J. Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76709-9	journal	March 2000
B800→B850 Energy Transfer Mechanism in Bacterial LH2 Complexes Investigated by B800 Pigment Exchange Herek, J. L.; Fraser, N. J.; Pullerits, T. Biophysical Journal, Vol. 78, Issue 5 https://doi.org/10.1016/S0006-3495(00)76803-2	journal	May 2000
Spectroscopy on the B850 Band of Individual Light-Harvesting 2 Complexes of Rhodopseudomonas acidophila I. Experiments and Monte Carlo Simulations Ketelaars, M.; van Oijen, A. M.; Matsushita, M. Biophysical Journal, Vol. 80, Issue 3 https://doi.org/10.1016/S0006-3495(01)76132-2	journal	March 2001
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 structure and function of the LH2 (B800–850) complex from the purple photosynthetic bacterium Rhodopseudomonas acidophila strain 10050 Cogdell, Richard J.; Isaacs, Neil W.; Freer, Andy A. Progress in Biophysics and Molecular Biology, Vol. 68, Issue 1 https://doi.org/10.1016/S0079-6107(97)00010-2	journal	January 1997
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
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
Controlled Disorder in Plant Light-Harvesting Complex II Explains Its Photoprotective Role Krüger, Tjaart P. J.; Ilioaia, Cristian; Johnson, Matthew P. Biophysical Journal, Vol. 102, Issue 11 https://doi.org/10.1016/j.bpj.2012.04.044	journal	June 2012
Origin of non-Gaussian site energy disorder in molecular aggregates Rancova, Olga; Jakučionis, Mantas; Valkunas, Leonas Chemical Physics Letters, Vol. 674 https://doi.org/10.1016/j.cplett.2017.02.056	journal	April 2017
Room to Move: Crystallizing Membrane Proteins in Swollen Lipidic Mesophases Cherezov, Vadim; Clogston, Jeffrey; Papiz, Miroslav Z. Journal of Molecular Biology, Vol. 357, Issue 5 https://doi.org/10.1016/j.jmb.2006.01.049	journal	April 2006
The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes Cogdell, Richard J.; Gall, Andrew; Köhler, Jürgen Quarterly Reviews of Biophysics, Vol. 39, Issue 3 https://doi.org/10.1017/S0033583506004434	journal	August 2006
Single-Molecule Fluorescence Spectroscopy of Photosynthetic Systems Kondo, Toru; Chen, Wei Jia; Schlau-Cohen, Gabriela S. Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.6b00195	journal	March 2016
Conformational Memory of a Protein Revealed by Single-Molecule Spectroscopy Schörner, Mario; Beyer, Sebastian Reinhardt; Southall, June The Journal of Physical Chemistry B, Vol. 119, Issue 44 https://doi.org/10.1021/acs.jpcb.5b07494	journal	October 2015
Protein Configuration Landscape Fluctuations Revealed by Exciton Transition Polarizations in Single Light Harvesting Complexes Tubasum, Sumera; Torbjörnsson, Magne; Yadav, Dheerendra The Journal of Physical Chemistry B, Vol. 120, Issue 4 https://doi.org/10.1021/acs.jpcb.5b12466	journal	January 2016
Fluorescence Spectral Fluctuations of Single LH2 Complexes from Rhodopseudomonas acidophila Strain 10050 ^† Rutkauskas, Danielis; Novoderezkhin, Vladimir; Cogdell, Richard J. Biochemistry, Vol. 43, Issue 15 https://doi.org/10.1021/bi0497648	journal	April 2004
Inter- and Intraband Energy Transfer in LH2-Antenna Complexes of Purple Bacteria. A Fluorescence Line-Narrowing and Hole-Burning Study De Caro, C.; Visschers, R. W.; van Grondelle, R. The Journal of Physical Chemistry, Vol. 98, Issue 41 https://doi.org/10.1021/j100092a032	journal	October 1994
Conformational and environmental effects on bacteriochlorophyll optical spectra: correlations of calculated spectra with structural results Gudowska-Nowak, E.; Newton, M. D.; Fajer, J. The Journal of Physical Chemistry, Vol. 94, Issue 15 https://doi.org/10.1021/j100378a036	journal	July 1990
Nature of Disorder and Inter-Complex Energy Transfer in LH2 at Room Temperature: A Three Pulse Photon Echo Peak Shift Study ^† Agarwal, Ritesh; Rizvi, Abbas H.; Prall, Bradley S. The Journal of Physical Chemistry A, Vol. 106, Issue 33 https://doi.org/10.1021/jp014054m	journal	August 2002
Intra- and Interband Transfers in the B800−B850 Antenna of Rhodospirillum m olischianum : Redfield Theory Modeling of Polarized Pump−Probe Kinetics Novoderezhkin, Vladimir; Wendling, Markus; van Grondelle, Rienk The Journal of Physical Chemistry B, Vol. 107, Issue 41 https://doi.org/10.1021/jp035432l	journal	October 2003
Multichromophoric Förster Resonance Energy Transfer from B800 to B850 in the Light Harvesting Complex 2: Evidence for Subtle Energetic Optimization by Purple Bacteria ^† Jang, Seogjoo; Newton, Marshall D.; Silbey, Robert J. The Journal of Physical Chemistry B, Vol. 111, Issue 24 https://doi.org/10.1021/jp070111l	journal	June 2007
Dynamics of Exciton Relaxation in LH2 Antenna Probed by Multipulse Nonlinear Spectroscopy Novoderezhkin, Vladimir I.; Cohen Stuart, Thomas A.; van Grondelle, Rienk The Journal of Physical Chemistry A, Vol. 115, Issue 16 https://doi.org/10.1021/jp108187m	journal	April 2011
Spectra and Dynamics in the B800 Antenna: Comparing Hierarchical Equations, Redfield and Förster Theories Novoderezhkin, Vladimir; van Grondelle, Rienk The Journal of Physical Chemistry B, Vol. 117, Issue 38 https://doi.org/10.1021/jp400957t	journal	April 2013
Static and Dynamic Disorder in Bacterial Light-Harvesting Complex LH2: A 2DES Simulation Study Rancova, Olga; Abramavicius, Darius The Journal of Physical Chemistry B, Vol. 118, Issue 27 https://doi.org/10.1021/jp5043156	journal	June 2014
Low-Temperature Protein Dynamics of the B800 Molecules in the LH2 Light-Harvesting Complex: Spectral Hole Burning Study and Comparison with Single Photosynthetic Complex Spectroscopy Grozdanov, Daniel; Herascu, Nicoleta; Reinot, Tõnu The Journal of Physical Chemistry B, Vol. 114, Issue 10 https://doi.org/10.1021/jp9089358	journal	March 2010
Electronic Excitation Transfer in the LH2 Complex of Rhodobacter sphaeroides Jimenez, Ralph; Dikshit, Srivatsan N.; Bradforth, Stephen E. The Journal of Physical Chemistry, Vol. 100, Issue 16 https://doi.org/10.1021/jp953074j	journal	January 1996
Energy Transfer and Exciton Annihilation in the B800−850 Antenna Complex of the Photosynthetic Purple Bacterium Rhodopseudomonas acidophila (Strain 10050). A Femtosecond Transient Absorption Study Ma, Ying-Zhong; Cogdell, Richard J.; Gillbro, Tomas The Journal of Physical Chemistry B, Vol. 101, Issue 6 https://doi.org/10.1021/jp962470e	journal	February 1997
Pigment Binding-Site and Electronic Properties in Light-Harvesting Proteins of Purple Bacteria Sturgis, James N.; Robert, B. The Journal of Physical Chemistry B, Vol. 101, Issue 37 https://doi.org/10.1021/jp963363n	journal	September 1997
Superradiance and Exciton Delocalization in Bacterial Photosynthetic Light-Harvesting Systems Monshouwer, René; Abrahamsson, Malin; van Mourik, Frank The Journal of Physical Chemistry B, Vol. 101, Issue 37 https://doi.org/10.1021/jp963377t	journal	September 1997
Calculations of Spectroscopic Properties of the LH2 Bacteriochlorophyll−Protein Antenna Complex from Rhodopseudomonas acidophila ^† Alden, R. G.; Johnson, E.; Nagarajan, V. The Journal of Physical Chemistry B, Vol. 101, Issue 23 https://doi.org/10.1021/jp970005r	journal	June 1997
Theory on Rates of Excitation-Energy Transfer between Molecular Aggregates through Distributed Transition Dipoles with Application to the Antenna System in Bacterial Photosynthesis Sumi, Hitoshi The Journal of Physical Chemistry B, Vol. 103, Issue 1 https://doi.org/10.1021/jp983477u	journal	January 1999
Photosynthetic Light-Harvesting: Reconciling Dynamics and Structure of Purple Bacterial LH2 Reveals Function of Photosynthetic Unit Sundström, Villy; Pullerits, Tõnu; van Grondelle, Rienk The Journal of Physical Chemistry B, Vol. 103, Issue 13 https://doi.org/10.1021/jp983722+	journal	March 1999
Disordered Exciton Analysis of Linear and Nonlinear Absorption Spectra of Antenna Bacteriochlorophyll Aggregates: LH2−Only Mutant Chromatophores of Rhodobacter sphaeroides at 8 K under Spectrally Selective Excitation Freiberg, Arvi; Timpmann, Kõu; Ruus, Rein The Journal of Physical Chemistry B, Vol. 103, Issue 45 https://doi.org/10.1021/jp991676n	journal	November 1999
How Photosynthetic Proteins Switch Valkunas, Leonas; Chmeliov, Jevgenij; Krüger, Tjaart P. J. The Journal of Physical Chemistry Letters, Vol. 3, Issue 19 https://doi.org/10.1021/jz300983r	journal	September 2012
Single Molecule Spectroscopy of Monomeric LHCII: Experiment and Theory Malý, Pavel; Gruber, J. Michael; van Grondelle, Rienk Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep26230	journal	May 2016
Understanding photosynthetic light-harvesting: a bottom up theoretical approach Renger, Thomas; Müh, Frank Phys. Chem. Chem. Phys., Vol. 15, Issue 10 https://doi.org/10.1039/C3CP43439G	journal	January 2013
Ultrafast dynamics of single molecules Brinks, Daan; Hildner, Richard; van Dijk, Erik M. H. P. Chem. Soc. Rev., Vol. 43, Issue 8 https://doi.org/10.1039/C3CS60269A	journal	January 2014
The nature of coherences in the B820 bacteriochlorophyll dimer revealed by two-dimensional electronic spectroscopy Ferretti, Marco; Novoderezhkin, Vladimir I.; Romero, Elisabet Physical Chemistry Chemical Physics, Vol. 16, Issue 21 https://doi.org/10.1039/c3cp54634a	journal	January 2014
Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes Zhang, Wei Min; Meier, Torsten; Chernyak, Vladimir The Journal of Chemical Physics, Vol. 108, Issue 18 https://doi.org/10.1063/1.476212	journal	May 1998
Two-dimensional electronic spectroscopy of the B800-B820 light-harvesting complex Zigmantas, D.; Read, E. L.; Mancal, T. Proceedings of the National Academy of Sciences, Vol. 103, Issue 34 https://doi.org/10.1073/pnas.0602961103	journal	August 2006
Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes Kruger, T. P. J.; Wientjes, E.; Croce, R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 33 https://doi.org/10.1073/pnas.1105411108	journal	August 2011
Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states Schlau-Cohen, G. S.; Wang, Q.; Southall, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1310222110	journal	June 2013
Ultrafast energy relaxation in single light-harvesting complexes Malý, Pavel; Gruber, J. Michael; Cogdell, Richard J. Proceedings of the National Academy of Sciences, Vol. 113, Issue 11 https://doi.org/10.1073/pnas.1522265113	journal	February 2016
Direct observation of tiers in the energy landscape of a chromoprotein: A single-molecule study Hofmann, C.; Aartsma, T. J.; Michel, H. Proceedings of the National Academy of Sciences, Vol. 100, Issue 26 https://doi.org/10.1073/pnas.2533896100	journal	December 2003
The dynamics of structural deformations of immobilized single light-harvesting complexes Bopp, M. A.; Sytnik, A.; Howard, T. D. Proceedings of the National Academy of Sciences, Vol. 96, Issue 20 https://doi.org/10.1073/pnas.96.20.11271	journal	September 1999
Multichromophoric Förster Resonance Energy Transfer Jang, Seogjoo; Newton, Marshall D.; Silbey, Robert J. Physical Review Letters, Vol. 92, Issue 21 https://doi.org/10.1103/PhysRevLett.92.218301	journal	May 2004
Single-Molecule Pump-Probe Detection Resolves Ultrafast Pathways in Individual and Coupled Quantum Systems van Dijk, Erik M. H. P.; Hernando, Jordi; García-López, Juan-José Physical Review Letters, Vol. 94, Issue 7 https://doi.org/10.1103/PhysRevLett.94.078302	journal	February 2005
Coherence in the B800 Ring of Purple Bacteria LH2 Cheng, Y. C.; Silbey, R. J. Physical Review Letters, Vol. 96, Issue 2 https://doi.org/10.1103/PhysRevLett.96.028103	journal	January 2006
Quantum Coherent Energy Transfer over Varying Pathways in Single Light-Harvesting Complexes Hildner, R.; Brinks, D.; Nieder, J. B. Science, Vol. 340, Issue 6139 https://doi.org/10.1126/science.1235820	journal	June 2013
Photosynthetic Excitons van Amerongen, Herbert; van Grondelle, Rienk; Valkunas, Leonas World Scientific https://doi.org/10.1142/3609	book	January 2000
Biomolecular Simulation: A Computational Microscope for Molecular Biology Dror, Ron O.; Dirks, Robert M.; Grossman, J. P. Annual Review of Biophysics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev-biophys-042910-155245	journal	June 2012
Femtobiology Sundström, Villy Annual Review of Physical Chemistry, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.physchem.59.032607.093615	journal	May 2008
RETRACTED: Fluorescence Spectroscopy of Conformational Changes of Single LH2 Complexes Rutkauskas, Danielis; Novoderezhkin, Vladimir; Cogdell, Richard J. Biophysical Journal, Vol. 88, Issue 1 https://doi.org/10.1529/biophysj.104.048629	journal	January 2005
Single-Molecule Spectroscopic Characterization of Light-Harvesting 2 Complexes Reconstituted into Model Membranes Richter, Martin F.; Baier, Jürgen; Cogdell, Richard J. Biophysical Journal, Vol. 93, Issue 1 https://doi.org/10.1529/biophysj.106.103606	journal	July 2007
Chlorophyll Ring Deformation Modulates Qy Electronic Energy in Chlorophyll-Protein Complexes and Generates Spectral Forms Zucchelli, Giuseppe; Brogioli, Doriano; Casazza, Anna Paola Biophysical Journal, Vol. 93, Issue 6 https://doi.org/10.1529/biophysj.107.104554	journal	September 2007

Similar Records

Quieting a noisy antenna reproduces photosynthetic light-harvesting spectra

Journal Article · Thu Jun 25 00:00:00 EDT 2020 · Science · OSTI ID:1801413

Quieting a noisy antenna reproduces photosynthetic light-harvesting spectra

Journal Article · Thu Jun 25 00:00:00 EDT 2020 · Science · OSTI ID:1635075

Robust light harvesting by a noisy antenna

Citation Formats

References (62)

Similar Records

Related Subjects