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Title: Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells

Abstract

Photosynthesis transfers energy efficiently through a series of antenna complexes to the reaction center where charge separation occurs. Energy transfer in vivo is primarily monitored by measuring fluorescence signals from the small fraction of excitations that fail to result in charge separation. Here, we use two-dimensional electronic spectroscopy to follow the entire energy transfer process in a thriving culture of the purple bacteria, Rhodobacter sphaeroides. By removing contributions from scattered light, we extract the dynamics of energy transfer through the dense network of antenna complexes and into the reaction center. Simulations demonstrate that these dynamics constrain the membrane organization into small pools of core antenna complexes that rapidly trap energy absorbed by surrounding peripheral antenna complexes. The rapid trapping and limited back transfer of these excitations lead to transfer efficiencies of 83% and a small functional light-harvesting unit.

Authors:
 [1];  [1]; ORCiD logo [1];  [1];  [2]; ORCiD logo [2]; ORCiD logo [1]
  1. The Univ. of Chicago, Chicago, IL (United States)
  2. Univ. of Sheffield, Sheffield (United Kingdom)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC), Washington, D.C. (United States). Photosynthetic Antenna Research Center (PARC); Washington Univ., St. Louis, MO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1469984
Alternate Identifier(s):
OSTI ID: 1545601
Grant/Contract Number:  
SC0001035
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Related Information: PARC partners with Washington University in St. Louis (lead); University of California, Riverside; University of Glasgow, UK; Los Alamos National Laboratory; University of New Mexico; New Mexico Corsortium; North Carolina State University; Northwestern University; Oak Ridge National Laboratory; University of Pennsylvania; Sandia National Laboratories; University of Sheffield, UK; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
14 SOLAR ENERGY; solar (fuels); photosynthesis (natural and artificial); biofuels (including algae and biomass); bio-inspired; charge transport; membrane; synthesis (novel materials); synthesis (self-assembly)

Citation Formats

Dahlberg, Peter D., Ting, Po -Chieh, Massey, Sara C., Allodi, Marco A., Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells. United States: N. p., 2017. Web. doi:10.1038/s41467-017-01124-z.
Dahlberg, Peter D., Ting, Po -Chieh, Massey, Sara C., Allodi, Marco A., Martin, Elizabeth C., Hunter, C. Neil, & Engel, Gregory S. Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells. United States. doi:10.1038/s41467-017-01124-z.
Dahlberg, Peter D., Ting, Po -Chieh, Massey, Sara C., Allodi, Marco A., Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Tue . "Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells". United States. doi:10.1038/s41467-017-01124-z. https://www.osti.gov/servlets/purl/1469984.
@article{osti_1469984,
title = {Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells},
author = {Dahlberg, Peter D. and Ting, Po -Chieh and Massey, Sara C. and Allodi, Marco A. and Martin, Elizabeth C. and Hunter, C. Neil and Engel, Gregory S.},
abstractNote = {Photosynthesis transfers energy efficiently through a series of antenna complexes to the reaction center where charge separation occurs. Energy transfer in vivo is primarily monitored by measuring fluorescence signals from the small fraction of excitations that fail to result in charge separation. Here, we use two-dimensional electronic spectroscopy to follow the entire energy transfer process in a thriving culture of the purple bacteria, Rhodobacter sphaeroides. By removing contributions from scattered light, we extract the dynamics of energy transfer through the dense network of antenna complexes and into the reaction center. Simulations demonstrate that these dynamics constrain the membrane organization into small pools of core antenna complexes that rapidly trap energy absorbed by surrounding peripheral antenna complexes. The rapid trapping and limited back transfer of these excitations lead to transfer efficiencies of 83% and a small functional light-harvesting unit.},
doi = {10.1038/s41467-017-01124-z},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
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Cited by: 5 works
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Figures / Tables:

Fig. 1 Fig. 1: Annihilation reveals a highly connected network of light-harvesting complexes in vivo. a, Crystal structures of LH2 and RC-LH1-PufX (PDB 1KZU and PDB 4JC9, respectively) with the carotenoids and Bchl a phytyl tails removed for clarity. LH2 contains two bands of Bchl a, the B800 (blue) and the B850more » (green). LH1 contains a single band of Bchl a, B875 (red) that transfers energy to the special pair of the RC (orange). b, Absorption spectra in a 200 μm path length of cells containing only LH2, cells containing only LH1, and wild-type (WT) cells. The large offset from zero optical density is due to optical scattering. The 2DES excitation spectrum is shown in gray and is produced by super continuum generation in argon gas. The spectrum is broad enough to interrogate the entire energy transfer process from LH2→LH1→RC. c, Absorptive 2DES spectrum of LH2-only cells taken with 17.6 μJ cm−2 at T = 1 ps. d, Waiting time traces acquired at different powers from the maximum of the GSB/SE feature. The traces are the average of three scans and the shaded background is the mean ± the standard deviation. The change in dynamics with power is indicative of exciton-exciton annihilation. The dashed traces are the population of excited LH2 from a random walk simulation with a lifetime for energy transfer between LH2s of 2.7 ps, a domain size of 64 LH2, and a fluorescence lifetime of 250 ps« less

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Works referenced in this record:

Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria
journal, April 1995

  • McDermott, G.; Prince, S. M.; Freer, A. A.
  • Nature, Vol. 374, Issue 6522
  • DOI: 10.1038/374517a0

Two-dimensional spectroscopy of electronic couplings in photosynthesis
journal, March 2005

  • Brixner, Tobias; Stenger, Jens; Vaswani, Harsha M.
  • Nature, Vol. 434, Issue 7033
  • DOI: 10.1038/nature03429

Superradiance and Exciton Delocalization in Bacterial Photosynthetic Light-Harvesting Systems
journal, September 1997

  • Monshouwer, René; Abrahamsson, Malin; van Mourik, Frank
  • The Journal of Physical Chemistry B, Vol. 101, Issue 37
  • DOI: 10.1021/jp963377t

Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides
journal, February 1999


Direct Imaging of Protein Organization in an Intact Bacterial Organelle Using High-Resolution Atomic Force Microscopy
journal, November 2016


Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides
journal, October 2014

  • Cartron, Michaël L.; Olsen, John D.; Sener, Melih
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 10
  • DOI: 10.1016/j.bbabio.2014.02.003

Biodiversity of NPQ
journal, January 2015


Pigment content and molar extinction coefficients of photochemical reaction centers from Rhodopseudomonas spheroides
journal, June 1973

  • Straley, Susan C.; Parson, William W.; Mauzerall, David C.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 305, Issue 3
  • DOI: 10.1016/0005-2728(73)90079-0

Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties
journal, May 2012

  • Slouf, V.; Chabera, P.; Olsen, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 22
  • DOI: 10.1073/pnas.1201413109

Kinetics of Excitation Migration and Trapping in the Photosynthetic Unit of Purple Bacteria
journal, August 2001

  • Ritz, Thorsten; Park, Sanghyun; Schulten, Klaus
  • The Journal of Physical Chemistry B, Vol. 105, Issue 34
  • DOI: 10.1021/jp011032r

Non-Photochemical Quenching. A Response to Excess Light Energy
journal, April 2001

  • Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K.
  • Plant Physiology, Vol. 125, Issue 4
  • DOI: 10.1104/pp.125.4.1558

Energy transfer properties of Rhodobacter sphaeroides chromatophores during adaptation to low light intensity
journal, January 2014

  • Driscoll, B.; Lunceford, C.; Lin, S.
  • Phys. Chem. Chem. Phys., Vol. 16, Issue 32
  • DOI: 10.1039/C4CP01981D

Excitation Energy Transfer between the B850 and B875 Antenna Complexes of Rhodobacter sphaeroides
journal, February 1997


Real-time mapping of electronic structure with single-shot two-dimensional electronic spectroscopy
journal, September 2010

  • Harel, E.; Fidler, A. F.; Engel, G. S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 38
  • DOI: 10.1073/pnas.1007579107

Dynamics of energy transfer and trapping in the light-harvesting antenna of Rhodopseudomonas viridis
journal, March 1992


Energy transfer and trapping in photosynthesis
journal, August 1994

  • van Grondelle, Rienk; Dekker, Jan P.; Gillbro, Tomas
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1187, Issue 1
  • DOI: 10.1016/0005-2728(94)90166-X

Overall energy conversion efficiency of a photosynthetic vesicle
journal, August 2016


The native architecture of a photosynthetic membrane
journal, August 2004

  • Bahatyrova, Svetlana; Frese, Raoul N.; Siebert, C. Alistair
  • Nature, Vol. 430, Issue 7003
  • DOI: 10.1038/nature02823

Förster Energy Transfer Theory as Reflected in the Structures of Photosynthetic Light‐Harvesting Systems
journal, February 2011


The photoprotective molecular switch in the photosystem II antenna
journal, January 2012

  • Ruban, Alexander V.; Johnson, Matthew P.; Duffy, Christopher D. P.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.04.007

Three-Dimensional Structure of the Rhodobacter sphaeroides RC-LH1-PufX Complex: Dimerization and Quinone Channels Promoted by PufX
journal, October 2013

  • Qian, Pu; Papiz, Miroslav Z.; Jackson, Philip J.
  • Biochemistry, Vol. 52, Issue 43
  • DOI: 10.1021/bi4011946

The organization of the photosynthetic apparatus of Rhodobacter sphaeroides: Studies of antenna mutants using singlet-singlet quenching
journal, March 1988

  • Vos, Marcel; van Dorssen, Rob J.; Amesz, Jan
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 933, Issue 1
  • DOI: 10.1016/0005-2728(88)90063-1

PucC and LhaA direct efficient assembly of the light-harvesting complexes in Rhodobacter sphaeroides : Photosystem assembly in
journal, November 2015

  • Mothersole, David J.; Jackson, Philip J.; Vasilev, Cvetelin
  • Molecular Microbiology, Vol. 99, Issue 2
  • DOI: 10.1111/mmi.13235

Singlet–Singlet Annihilation Kinetics in Aggregates and Trimers of LHCII
journal, May 2001


Temporally and spectrally resolved subpicosecond energy transfer within the peripheral antenna complex (LH2) and from LH2 to the core antenna complex in photosynthetic purple bacteria.
journal, December 1995

  • Hess, S.; Chachisvilis, M.; Timpmann, K.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 26
  • DOI: 10.1073/pnas.92.26.12333

Energy-transfer dynamics in three light-harvesting mutants of Rhodobacter sphaeroides: a picosecond spectroscopy study
journal, April 1990

  • Hunter, C. Neil; Bergstroem, Hans; Van Grondelle, Rienk
  • Biochemistry, Vol. 29, Issue 13
  • DOI: 10.1021/bi00465a008

The Organization of LH2 Complexes in Membranes from Rhodobacter sphaeroides
journal, August 2008

  • Olsen, John D.; Tucker, Jaimey D.; Timney, John A.
  • Journal of Biological Chemistry, Vol. 283, Issue 45
  • DOI: 10.1074/jbc.M804824200

Aberrant Assembly Complexes of the Reaction Center Light-harvesting 1 PufX (RC-LH1-PufX) Core Complex of Rhodobacter sphaeroides Imaged by Atomic Force Microscopy
journal, September 2014

  • Olsen, John D.; Adams, Peter G.; Jackson, Philip J.
  • Journal of Biological Chemistry, Vol. 289, Issue 43
  • DOI: 10.1074/jbc.M114.596585

Flexibility and Size Heterogeneity of the LH1 Light Harvesting Complex Revealed by Atomic Force Microscopy: FUNCTIONAL SIGNIFICANCE FOR BACTERIAL PHOTOSYNTHESIS
journal, March 2004

  • Bahatyrova, Svetlana; Frese, Raoul N.; van der Werf, Kees O.
  • Journal of Biological Chemistry, Vol. 279, Issue 20
  • DOI: 10.1074/jbc.M313039200

Photosynthetic Vesicle Architecture and Constraints on Efficient Energy Harvesting
journal, July 2010


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