skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo

Abstract

In photosynthetic organisms, the pigment-protein complexes that comprise the light-harvesting antenna exhibit complex electronic structures and ultrafast dynamics due to the coupling among the chromophores. In this work, we present absorptive two-dimensional (2D) electronic spectra from living cultures of the purple bacterium, Rhodobacter sphaeroides, acquired using gradient assisted photon echo spectroscopy. Diagonal slices through the 2D lineshape of the LH1 stimulated emission/ground state bleach feature reveal a resolvable higher energy population within the B875 manifold. The waiting time evolution of diagonal, horizontal, and vertical slices through the 2D lineshape shows a sub-100 fs intra-complex relaxation as this higher energy population red shifts. The absorption (855 nm) of this higher lying sub-population of B875 before it has red shifted optimizes spectral overlap between the LH1 B875 band and the B850 band of LH2. Access to an energetically broad distribution of excitonic states within B875 offers a mechanism for efficient energy transfer from LH2 to LH1 during photosynthesis while limiting back transfer. Two-dimensional lineshapes reveal a rapid decay in the ground-state bleach/stimulated emission of B875. This signal, identified as a decrease in the dipole strength of a strong transition in LH1 on the red side of the B875 band, is assigned tomore » the rapid localization of an initially delocalized exciton state, a dephasing process that frustrates back transfer from LH1 to LH2.« less

Authors:
 [1];  [2]; ORCiD logo [1]; ORCiD logo [1];  [1];  [3];  [3]; ORCiD logo [1]
  1. Univ. of Chicago, IL (United States). Dept. of Chemistry, Inst. for Biophysical Dynamics, and The James Franck Inst.
  2. Univ. of Chicago, IL (United States). Graduate Program in the Biophysical Sciences, Inst. for Biophysical Dynamics, and The James Franck Inst.
  3. Univ. of Sheffield (United Kingdom). Dept. of Molecular Biology and Biotechnology
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1469878
Alternate Identifier(s):
OSTI ID: 1396635
Grant/Contract Number:  
SC0001035; SC 0001035
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Chemical Physics
Additional Journal Information:
Journal Volume: 147; Journal Issue: 13; 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 0021-9606
Publisher:
American Institute of Physics (AIP)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 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

Sohail, Sara H., Dahlberg, Peter D., Allodi, Marco A., Massey, Sara C., Ting, Po-Chieh, Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo. United States: N. p., 2017. Web. doi:10.1063/1.4999057.
Sohail, Sara H., Dahlberg, Peter D., Allodi, Marco A., Massey, Sara C., Ting, Po-Chieh, Martin, Elizabeth C., Hunter, C. Neil, & Engel, Gregory S. Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo. United States. doi:10.1063/1.4999057.
Sohail, Sara H., Dahlberg, Peter D., Allodi, Marco A., Massey, Sara C., Ting, Po-Chieh, Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Wed . "Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo". United States. doi:10.1063/1.4999057. https://www.osti.gov/servlets/purl/1469878.
@article{osti_1469878,
title = {Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo},
author = {Sohail, Sara H. and Dahlberg, Peter D. and Allodi, Marco A. and Massey, Sara C. and Ting, Po-Chieh and Martin, Elizabeth C. and Hunter, C. Neil and Engel, Gregory S.},
abstractNote = {In photosynthetic organisms, the pigment-protein complexes that comprise the light-harvesting antenna exhibit complex electronic structures and ultrafast dynamics due to the coupling among the chromophores. In this work, we present absorptive two-dimensional (2D) electronic spectra from living cultures of the purple bacterium, Rhodobacter sphaeroides, acquired using gradient assisted photon echo spectroscopy. Diagonal slices through the 2D lineshape of the LH1 stimulated emission/ground state bleach feature reveal a resolvable higher energy population within the B875 manifold. The waiting time evolution of diagonal, horizontal, and vertical slices through the 2D lineshape shows a sub-100 fs intra-complex relaxation as this higher energy population red shifts. The absorption (855 nm) of this higher lying sub-population of B875 before it has red shifted optimizes spectral overlap between the LH1 B875 band and the B850 band of LH2. Access to an energetically broad distribution of excitonic states within B875 offers a mechanism for efficient energy transfer from LH2 to LH1 during photosynthesis while limiting back transfer. Two-dimensional lineshapes reveal a rapid decay in the ground-state bleach/stimulated emission of B875. This signal, identified as a decrease in the dipole strength of a strong transition in LH1 on the red side of the B875 band, is assigned to the rapid localization of an initially delocalized exciton state, a dephasing process that frustrates back transfer from LH1 to LH2.},
doi = {10.1063/1.4999057},
journal = {Journal of Chemical Physics},
number = 13,
volume = 147,
place = {United States},
year = {2017},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Exciton Delocalization and Initial Dephasing Dynamics of Purple Bacterial LH2
journal, August 2000

  • Book, L. D.; Ostafin, A. E.; Ponomarenko, N.
  • The Journal of Physical Chemistry B, Vol. 104, Issue 34
  • DOI: 10.1021/jp000485d

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

Structural model and excitonic properties of the dimeric RC–LH1–PufX complex from Rhodobacter sphaeroides
journal, February 2009


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

Energy Transfer Observed in Live Cells Using Two-Dimensional Electronic Spectroscopy
journal, October 2013

  • Dahlberg, Peter D.; Fidler, Andrew F.; Caram, Justin R.
  • The Journal of Physical Chemistry Letters, Vol. 4, Issue 21
  • DOI: 10.1021/jz401944q

Coherent Two-Dimensional Optical Spectroscopy
journal, April 2008


Vibronic coherence in oxygenic photosynthesis
journal, July 2014

  • Fuller, Franklin D.; Pan, Jie; Gelzinis, Andrius
  • Nature Chemistry, Vol. 6, Issue 8
  • DOI: 10.1038/nchem.2005

Hydrogen bonds in liquid water are broken only fleetingly
journal, August 2005

  • Eaves, J. D.; Loparo, J. J.; Fecko, C. J.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 37
  • DOI: 10.1073/pnas.0505125102

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

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


Two-dimensional spectroscopy using diffractive optics based phased-locked photon echoes
journal, March 2004


T WO -D IMENSIONAL F EMTOSECOND S PECTROSCOPY
journal, October 2003


Two-dimensional Fourier transform electronic spectroscopy
journal, October 2001

  • Hybl, John D.; Albrecht Ferro, Allison; Jonas, David M.
  • The Journal of Chemical Physics, Vol. 115, Issue 14, p. 6606-6622
  • DOI: 10.1063/1.1398579

In situ mapping of the energy flow through the entire photosynthetic apparatus
journal, May 2016

  • Dostál, Jakub; Pšenčík, Jakub; Zigmantas, Donatas
  • Nature Chemistry, Vol. 8, Issue 7
  • DOI: 10.1038/nchem.2525

Two-Dimensional Line Shapes Derived from Coherent Third-Order Nonlinear Spectroscopy
journal, May 2000

  • Tokmakoff, Andrei
  • The Journal of Physical Chemistry A, Vol. 104, Issue 18
  • DOI: 10.1021/jp993207r

Experimental Implementations of Two-Dimensional Fourier Transform Electronic Spectroscopy
journal, April 2015


Two-dimensional electronic spectroscopy and photosynthesis: Fundamentals and applications to photosynthetic light-harvesting
journal, July 2011


Communication: Coherences observed in vivo in photosynthetic bacteria using two-dimensional electronic spectroscopy
journal, September 2015

  • Dahlberg, Peter D.; Norris, Graham J.; Wang, Cheng
  • The Journal of Chemical Physics, Vol. 143, Issue 10
  • DOI: 10.1063/1.4930539

Intra- and Interband Transfers in the B800−B850 Antenna of Rhodospirillum m olischianum :  Redfield Theory Modeling of Polarized Pump−Probe Kinetics
journal, October 2003

  • Novoderezhkin, Vladimir; Wendling, Markus; van Grondelle, Rienk
  • The Journal of Physical Chemistry B, Vol. 107, Issue 41
  • DOI: 10.1021/jp035432l

Three-Pulse Photon Echo Measurements on LH1 and LH2 Complexes of Rhodobacter sphaeroides :  A Nonlinear Spectroscopic Probe of Energy Transfer
journal, September 1997

  • Jimenez, Ralph; van Mourik, Frank; Yu, Jae Young
  • The Journal of Physical Chemistry B, Vol. 101, Issue 37
  • DOI: 10.1021/jp970299g

Independent phasing of rephasing and non-rephasing 2D electronic spectra
journal, August 2013

  • Singh, V. P.; Fidler, A. F.; Rolczynski, B. S.
  • The Journal of Chemical Physics, Vol. 139, Issue 8
  • DOI: 10.1063/1.4818808

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


Single-Shot Gradient-Assisted Photon Echo Electronic Spectroscopy
journal, April 2011

  • Harel, Elad; Fidler, Andrew F.; Engel, Gregory S.
  • The Journal of Physical Chemistry A, Vol. 115, Issue 16
  • DOI: 10.1021/jp107022f

Energy transfer in photosynthesis: experimental insights and quantitative models
journal, January 2006

  • van Grondelle, Rienk; Novoderezhkin, Vladimir I.
  • Phys. Chem. Chem. Phys., Vol. 8, Issue 7
  • DOI: 10.1039/b514032c

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

Characterization of spectral diffusion from two-dimensional line shapes
journal, August 2006

  • Roberts, Sean T.; Loparo, Joseph J.; Tokmakoff, Andrei
  • The Journal of Chemical Physics, Vol. 125, Issue 8
  • DOI: 10.1063/1.2232271

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

Electronic Structure and Dynamics of Higher-Lying Excited States in Light Harvesting Complex 1 from Rhodobacter sphaeroides
journal, June 2016

  • Dahlberg, Peter D.; Ting, Po-Chieh; Massey, Sara C.
  • The Journal of Physical Chemistry A, Vol. 120, Issue 24
  • DOI: 10.1021/acs.jpca.6b04146

Time-Resolved Absorption Difference Spectroscopy of the LH-1 Antenna of Rhodopseudomonas viridis
journal, June 1998

  • Monshouwer, René; Baltuška, Andrius; van Mourik, Frank
  • The Journal of Physical Chemistry A, Vol. 102, Issue 23
  • DOI: 10.1021/jp980412i

Two-Dimensional Electronic Spectroscopy Reveals Ultrafast Energy Diffusion in Chlorosomes
journal, July 2012

  • Dostál, Jakub; Mančal, Tomáš; Augulis, Ramu-nas
  • Journal of the American Chemical Society, Vol. 134, Issue 28
  • DOI: 10.1021/ja3025627