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Title: Dark States in the Light-Harvesting complex 2 Revealed by Two-dimensional Electronic Spectroscopy

Abstract

Energy transfer and trapping in the light harvesting antennae of purple photosynthetic bacteria is an ultrafast process, which occurs with a quantum efficiency close to unity. However the mechanisms behind this process have not yet been fully understood. Recently it was proposed that low-lying energy dark states, such as charge transfer states and polaron pairs, play an important role in the dynamics and directionality of energy transfer. However, it is difficult to directly detect those states because of their small transition dipole moment and overlap with the B850/B870 exciton bands. Here we present a new experimental approach, which combines the selectivity of two-dimensional electronic spectroscopy with the availability of genetically modified light harvesting complexes, to reveal the presence of those dark states in both the genetically modified and the wild-type light harvesting 2 complexes of Rhodopseudomonas palustris. In conclusion, we suggest that Nature has used the unavoidable charge transfer processes that occur when LH pigments are concentrated to enhance and direct the flow of energy.

Authors:
 [1];  [1];  [1];  [2];  [2];  [3];  [4];  [1]
  1. Vrije Univ., Amsterdam (Netherlands). Department of Physics and Astronomy
  2. Univ. of Glasgow, Scotland (United Kingdom). Division of Biochemistry and Molecular Biology
  3. Moscow State Univ., Moscow (Russia). A. N. Belozersky Institute of Physico-Chemical Biology
  4. Princeton Univ., NJ (United States). Dept. of Chemistry
Publication Date:
Research Org.:
Vrije Univ., Amsterdam (Netherlands); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1242364
Grant/Contract Number:  
SC0001035
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Ferretti, Marco, Hendrikx, Ruud, Romero, Elisabet, Southall, June, Cogdell, Richard J., Novoderezhkin, Vladimir I., Scholes, Gregory D., and van Grondelle, Rienk. Dark States in the Light-Harvesting complex 2 Revealed by Two-dimensional Electronic Spectroscopy. United States: N. p., 2016. Web. doi:10.1038/srep20834.
Ferretti, Marco, Hendrikx, Ruud, Romero, Elisabet, Southall, June, Cogdell, Richard J., Novoderezhkin, Vladimir I., Scholes, Gregory D., & van Grondelle, Rienk. Dark States in the Light-Harvesting complex 2 Revealed by Two-dimensional Electronic Spectroscopy. United States. doi:10.1038/srep20834.
Ferretti, Marco, Hendrikx, Ruud, Romero, Elisabet, Southall, June, Cogdell, Richard J., Novoderezhkin, Vladimir I., Scholes, Gregory D., and van Grondelle, Rienk. Tue . "Dark States in the Light-Harvesting complex 2 Revealed by Two-dimensional Electronic Spectroscopy". United States. doi:10.1038/srep20834. https://www.osti.gov/servlets/purl/1242364.
@article{osti_1242364,
title = {Dark States in the Light-Harvesting complex 2 Revealed by Two-dimensional Electronic Spectroscopy},
author = {Ferretti, Marco and Hendrikx, Ruud and Romero, Elisabet and Southall, June and Cogdell, Richard J. and Novoderezhkin, Vladimir I. and Scholes, Gregory D. and van Grondelle, Rienk},
abstractNote = {Energy transfer and trapping in the light harvesting antennae of purple photosynthetic bacteria is an ultrafast process, which occurs with a quantum efficiency close to unity. However the mechanisms behind this process have not yet been fully understood. Recently it was proposed that low-lying energy dark states, such as charge transfer states and polaron pairs, play an important role in the dynamics and directionality of energy transfer. However, it is difficult to directly detect those states because of their small transition dipole moment and overlap with the B850/B870 exciton bands. Here we present a new experimental approach, which combines the selectivity of two-dimensional electronic spectroscopy with the availability of genetically modified light harvesting complexes, to reveal the presence of those dark states in both the genetically modified and the wild-type light harvesting 2 complexes of Rhodopseudomonas palustris. In conclusion, we suggest that Nature has used the unavoidable charge transfer processes that occur when LH pigments are concentrated to enhance and direct the flow of energy.},
doi = {10.1038/srep20834},
journal = {Scientific Reports},
issn = {2045-2322},
number = ,
volume = 6,
place = {United States},
year = {2016},
month = {2}
}

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Works referenced in this record:

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

Lessons from nature about solar light harvesting
journal, September 2011

  • Scholes, Gregory D.; Fleming, Graham R.; Olaya-Castro, Alexandra
  • Nature Chemistry, Vol. 3, Issue 10
  • DOI: 10.1038/nchem.1145

Exciton (De)Localization in the LH2 Antenna of Rhodobacter sphaeroides As Revealed by Relative Difference Absorption Measurements of the LH2 Antenna and the B820 Subunit
journal, November 1999

  • Novoderezhkin, Vladimir; Monshouwer, René; van Grondelle, Rienk
  • The Journal of Physical Chemistry B, Vol. 103, Issue 47
  • DOI: 10.1021/jp9844415

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

Disordered Exciton Model for the Core Light-Harvesting Antenna of Rhodopseudomonas viridis
journal, August 1999


Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment–protein complexes
journal, January 2015


Excitation energy transfer, trapping and annihilation in photosynthetic systems
journal, June 1985


The Primary Steps of Photosynthesis
journal, February 1994

  • Fleming, Graham R.; Grondelle, Rienk van
  • Physics Today, Vol. 47, Issue 2
  • DOI: 10.1063/1.881413

B800→B850 Energy Transfer Mechanism in Bacterial LH2 Complexes Investigated by B800 Pigment Exchange
journal, May 2000


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

Quantum coherence in photosynthesis for efficient solar-energy conversion
journal, July 2014

  • Romero, Elisabet; Augulis, Ramunas; Novoderezhkin, Vladimir I.
  • Nature Physics, Vol. 10, Issue 9
  • DOI: 10.1038/nphys3017

How exciton-vibrational coherences control charge separation in the photosystem II reaction center
journal, January 2015

  • Novoderezhkin, Vladimir I.; Romero, Elisabet; van Grondelle, Rienk
  • Physical Chemistry Chemical Physics, Vol. 17, Issue 46
  • DOI: 10.1039/C5CP00582E

Characterization of the Light-Harvesting Antennas of Photosynthetic Purple Bacteria by Stark Spectroscopy. 1. LH1 Antenna Complex and the B820 Subunit from Rhodospirillum rubrum
journal, September 1997

  • Beekman, Lucas M. P.; Steffen, Martin; van Stokkum, Ivo H. M.
  • The Journal of Physical Chemistry B, Vol. 101, Issue 37
  • DOI: 10.1021/jp963445b

Broadband 2D Electronic Spectroscopy Reveals a Carotenoid Dark State in Purple Bacteria
journal, April 2013

  • Ostroumov, Evgeny E.; Mulvaney, Rachel M.; Cogdell, Richard J.
  • Science, Vol. 340, Issue 6128
  • DOI: 10.1126/science.1230106

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

Time Scales of Coherent Dynamics in the Light-Harvesting Complex 2 (LH2) of Rhodobacter sphaeroides
journal, April 2013

  • Fidler, Andrew F.; Singh, Ved P.; Long, Phillip D.
  • The Journal of Physical Chemistry Letters, Vol. 4, Issue 9
  • DOI: 10.1021/jz400438m

Static and Dynamic Disorder in Bacterial Light-Harvesting Complex LH2: A 2DES Simulation Study
journal, June 2014

  • Rancova, Olga; Abramavicius, Darius
  • The Journal of Physical Chemistry B, Vol. 118, Issue 27
  • DOI: 10.1021/jp5043156

Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems
journal, April 2007

  • Engel, Gregory S.; Calhoun, Tessa R.; Read, Elizabeth L.
  • Nature, Vol. 446, Issue 7137
  • DOI: 10.1038/nature05678

The nature of coherences in the B820 bacteriochlorophyll dimer revealed by two-dimensional electronic spectroscopy
journal, January 2014

  • Ferretti, Marco; Novoderezhkin, Vladimir I.; Romero, Elisabet
  • Physical Chemistry Chemical Physics, Vol. 16, Issue 21
  • DOI: 10.1039/c3cp54634a

Probing Photosynthetic Energy and Charge Transfer with Two-Dimensional Electronic Spectroscopy
journal, January 2012

  • Lewis, Kristin L. M.; Ogilvie, Jennifer P.
  • The Journal of Physical Chemistry Letters, Vol. 3, Issue 4
  • DOI: 10.1021/jz201592v

Coherence Quantum Beats in Two-Dimensional Electronic Spectroscopy
journal, May 2008

  • Cheng, Yuan-Chung; Fleming, Graham R.
  • The Journal of Physical Chemistry A, Vol. 112, Issue 18
  • DOI: 10.1021/jp7107889

Origin of Long-Lived Coherences in Light-Harvesting Complexes
journal, June 2012

  • Christensson, Niklas; Kauffmann, Harald F.; Pullerits, Tõnu
  • The Journal of Physical Chemistry B, Vol. 116, Issue 25
  • DOI: 10.1021/jp304649c

The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae
journal, November 2012

  • Kolli, Avinash; O’Reilly, Edward J.; Scholes, Gregory D.
  • The Journal of Chemical Physics, Vol. 137, Issue 17
  • DOI: 10.1063/1.4764100

The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment–protein complexes
journal, January 2013

  • Chin, A. W.; Prior, J.; Rosenbach, R.
  • Nature Physics, Vol. 9, Issue 2
  • DOI: 10.1038/nphys2515

Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework
journal, December 2012

  • Tiwari, Vivek; Peters, William K.; Jonas, David M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 4
  • DOI: 10.1073/pnas.1211157110

Coherent Energy Transfer under Incoherent Light Conditions
journal, October 2012

  • Fassioli, Francesca; Olaya-Castro, Alexandra; Scholes, Gregory D.
  • The Journal of Physical Chemistry Letters, Vol. 3, Issue 21
  • DOI: 10.1021/jz3010317

Electronic Excitation Transfer in the LH2 Complex of Rhodobacter sphaeroides
journal, January 1996

  • Jimenez, Ralph; Dikshit, Srivatsan N.; Bradforth, Stephen E.
  • The Journal of Physical Chemistry, Vol. 100, Issue 16
  • DOI: 10.1021/jp953074j

Two Different Charge Separation Pathways in Photosystem II
journal, May 2010

  • Romero, Elisabet; van Stokkum, Ivo H. M.; Novoderezhkin, Vladimir I.
  • Biochemistry, Vol. 49, Issue 20
  • DOI: 10.1021/bi1003926

Excitonic Interactions and Stark Spectroscopy of Light Harvesting Systems
journal, October 1998

  • Somsen, Oscar J. G.; Chernyak, Vladimir; Frese, Raoul N.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 44
  • DOI: 10.1021/jp981114o

Charge Photogeneration in Neat Conjugated Polymers
journal, September 2013

  • Reid, Obadiah G.; Pensack, Ryan D.; Song, Yin
  • Chemistry of Materials, Vol. 26, Issue 1
  • DOI: 10.1021/cm4027144

Exciton Relaxation and Polaron Formation in LH2 at Low Temperature
journal, February 2000

  • Polívka, Tomáš; Pullerits, Tõnu; Herek, Jennifer L.
  • The Journal of Physical Chemistry B, Vol. 104, Issue 5
  • DOI: 10.1021/jp9915984

Two-dimensional electronic spectroscopy of the B800-B820 light-harvesting complex
journal, August 2006

  • Zigmantas, D.; Read, E. L.; Mancal, T.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 34
  • DOI: 10.1073/pnas.0602961103

Low Light Adaptation: Energy Transfer Processes in Different Types of Light Harvesting Complexes from Rhodopseudomonas palustris
journal, December 2009

  • Moulisová, Vladimíra; Luer, Larry; Hoseinkhani, Sajjad
  • Biophysical Journal, Vol. 97, Issue 11
  • DOI: 10.1016/j.bpj.2009.09.023

Dynamics of Exciton Relaxation in LH2 Antenna Probed by Multipulse Nonlinear Spectroscopy
journal, April 2011

  • Novoderezhkin, Vladimir I.; Cohen Stuart, Thomas A.; van Grondelle, Rienk
  • The Journal of Physical Chemistry A, Vol. 115, Issue 16
  • DOI: 10.1021/jp108187m

Mixing of Exciton and Charge-Transfer States in Photosystem II Reaction Centers: Modeling of Stark Spectra with Modified Redfield Theory
journal, August 2007

  • Novoderezhkin, Vladimir I.; Dekker, Jan P.; van Grondelle, Rienk
  • Biophysical Journal, Vol. 93, Issue 4
  • DOI: 10.1529/biophysj.106.096867

Concentration quenching in chlorophyll
journal, March 1976


Phase-stabilized two-dimensional electronic spectroscopy
journal, September 2004

  • Brixner, Tobias; Mančal, Tomáš; Stiopkin, Igor V.
  • The Journal of Chemical Physics, Vol. 121, Issue 9
  • DOI: 10.1063/1.1776112

    Works referencing / citing this record:

    Introduction to State-of-the-Art Multidimensional Time-Resolved Spectroscopy Methods
    journal, June 2018


    Before Förster. Initial excitation in photosynthetic light harvesting
    journal, January 2019

    • Karki, Khadga J.; Chen, Junsheng; Sakurai, Atsunori
    • Chemical Science, Vol. 10, Issue 34
    • DOI: 10.1039/c9sc01888c

    Introduction to State-of-the-Art Multidimensional Time-Resolved Spectroscopy Methods
    journal, June 2018


    Before Förster. Initial excitation in photosynthetic light harvesting
    journal, January 2019

    • Karki, Khadga J.; Chen, Junsheng; Sakurai, Atsunori
    • Chemical Science, Vol. 10, Issue 34
    • DOI: 10.1039/c9sc01888c

    The role of charge-transfer states in the spectral tuning of antenna complexes of purple bacteria
    journal, March 2018

    • Nottoli, Michele; Jurinovich, Sandro; Cupellini, Lorenzo
    • Photosynthesis Research, Vol. 137, Issue 2
    • DOI: 10.1007/s11120-018-0492-1

    Studying light-harvesting models with superconducting circuits
    journal, March 2018

    • Potočnik, Anton; Bargerbos, Arno; Schröder, Florian A. Y. N.
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-03312-x

    Spatially-resolved fluorescence-detected two-dimensional electronic spectroscopy probes varying excitonic structure in photosynthetic bacteria
    journal, October 2018

    • Tiwari, Vivek; Matutes, Yassel Acosta; Gardiner, Alastair T.
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-06619-x

    Multiscale modelling of photoinduced processes in composite systems
    journal, April 2019


    Revealing and Characterizing Dark Excitons through Coherent Multidimensional Spectroscopy
    journal, August 2016


    Delocalized excitons in natural light-harvesting complexes
    journal, August 2018