Efficiency of light harvesting in a photosynthetic bacterium adapted to different levels of light
Abstract
In this study, we use the photosynthetic purple bacterium Rhodobacter sphaeroides to find out how the acclimation of photosynthetic apparatus to growth conditions influences the rates of energy migration toward the reaction center traps and the efficiency of charge separation at the reaction centers. To answer these questions we measured the spectral and picosecond kinetic fluorescence responses as a function of excitation intensity in membranes prepared from cells grown under different illumination conditions. A kinetic model analysis yielded the microscopic rate constants that characterize the energy transfer and trapping inside the photosynthetic unit as well as the dependence of exciton trapping efficiency on the ratio of the peripheral LH2 and core LH1 antenna complexes, and on the wavelength of the excitation light. A high quantum efficiency of trapping over 80% was observed in most cases, which decreased toward shorter excitation wavelengths within the near infrared absorption band. At a fixed excitation wavelength the efficiency declines with the LH2/LH1 ratio. From the perspective of the ecological habitat of the bacteria the higher population of peripheral antenna facilitates growth under dim light even though the energy trapping is slower in low light adapted membranes. The similar values for the trapping efficiencies inmore »
- Authors:
- Publication Date:
- Research Org.:
- Washington Univ., St. Louis, MO (United States); 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:
- 1227544
- Alternate Identifier(s):
- OSTI ID: 1136126; OSTI ID: 1167765
- Report Number(s):
- DE-SC0001035-115
Journal ID: ISSN 0005-2728; S0005272814005222; PII: S0005272814005222
- Grant/Contract Number:
- SC0001035
- Resource Type:
- Published Article
- Journal Name:
- Biochimica et Biophysica Acta - Bioenergetics
- Additional Journal Information:
- Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1837 Journal Issue: 10; Journal ID: ISSN 0005-2728
- Publisher:
- Elsevier
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 14 SOLAR ENERGY; 59 BASIC BIOLOGICAL SCIENCES; photosynthesis; photosynthetic unit; optical spectroscopy; light harvesting; picosecond excitation energy transfer; exciton
Citation Formats
Timpmann, Kõu, Chenchiliyan, Manoop, Jalviste, Erko, Timney, John A., Hunter, C. Neil, and Freiberg, Arvi. Efficiency of light harvesting in a photosynthetic bacterium adapted to different levels of light. Netherlands: N. p., 2014.
Web. doi:10.1016/j.bbabio.2014.06.007.
Timpmann, Kõu, Chenchiliyan, Manoop, Jalviste, Erko, Timney, John A., Hunter, C. Neil, & Freiberg, Arvi. Efficiency of light harvesting in a photosynthetic bacterium adapted to different levels of light. Netherlands. https://doi.org/10.1016/j.bbabio.2014.06.007
Timpmann, Kõu, Chenchiliyan, Manoop, Jalviste, Erko, Timney, John A., Hunter, C. Neil, and Freiberg, Arvi. Wed .
"Efficiency of light harvesting in a photosynthetic bacterium adapted to different levels of light". Netherlands. https://doi.org/10.1016/j.bbabio.2014.06.007.
@article{osti_1227544,
title = {Efficiency of light harvesting in a photosynthetic bacterium adapted to different levels of light},
author = {Timpmann, Kõu and Chenchiliyan, Manoop and Jalviste, Erko and Timney, John A. and Hunter, C. Neil and Freiberg, Arvi},
abstractNote = {In this study, we use the photosynthetic purple bacterium Rhodobacter sphaeroides to find out how the acclimation of photosynthetic apparatus to growth conditions influences the rates of energy migration toward the reaction center traps and the efficiency of charge separation at the reaction centers. To answer these questions we measured the spectral and picosecond kinetic fluorescence responses as a function of excitation intensity in membranes prepared from cells grown under different illumination conditions. A kinetic model analysis yielded the microscopic rate constants that characterize the energy transfer and trapping inside the photosynthetic unit as well as the dependence of exciton trapping efficiency on the ratio of the peripheral LH2 and core LH1 antenna complexes, and on the wavelength of the excitation light. A high quantum efficiency of trapping over 80% was observed in most cases, which decreased toward shorter excitation wavelengths within the near infrared absorption band. At a fixed excitation wavelength the efficiency declines with the LH2/LH1 ratio. From the perspective of the ecological habitat of the bacteria the higher population of peripheral antenna facilitates growth under dim light even though the energy trapping is slower in low light adapted membranes. The similar values for the trapping efficiencies in all samples imply a robust photosynthetic apparatus that functions effectively at a variety of light intensities.},
doi = {10.1016/j.bbabio.2014.06.007},
journal = {Biochimica et Biophysica Acta - Bioenergetics},
number = 10,
volume = 1837,
place = {Netherlands},
year = {Wed Oct 01 00:00:00 EDT 2014},
month = {Wed Oct 01 00:00:00 EDT 2014}
}
https://doi.org/10.1016/j.bbabio.2014.06.007
Web of Science
Works referenced in this record:
A master equation theory of fluorescence induction, photochemical yield, and singlet-triplet exciton quenching in photosynthetic systems
journal, October 1983
- Paillotin, G.; Geacintov, N. E.; Breton, J.
- Biophysical Journal, Vol. 44, Issue 1
A Role for a Light-Harvesting Antenna Complex of Photosystem II in Photoprotection
journal, August 2002
- Govindjee,
- The Plant Cell, Vol. 14, Issue 8
Isolation and characterisation of the different B800–850 light-harvesting complexes from low- and high-light grown cells of Rhodopseudomonas palustris, strain 2.1.6
journal, March 1990
- Evans, Mark B.; Hawthornthwaite, Anna M.; Cogdell, Richard J.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1016, Issue 1
The architecture of Rhodobacter sphaeroides chromatophores
journal, August 2014
- Scheuring, Simon; Nevo, Reinat; Liu, Lu-Ning
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 8
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
Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light-harvesting 1 antenna of Rhodobacter sphaeroides.
journal, July 1994
- Olsen, J. D.; Sockalingum, G. D.; Robert, B.
- Proceedings of the National Academy of Sciences, Vol. 91, Issue 15
The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes
journal, August 2006
- Cogdell, Richard J.; Gall, Andrew; Köhler, Jürgen
- Quarterly Reviews of Biophysics, Vol. 39, Issue 3
Control of Photosystem Formation inRhodobacter sphaeroides
journal, June 1998
- Zeilstra-Ryalls, Jill; Gomelsky, Mark; Eraso, Jesus M.
- Journal of Bacteriology, Vol. 180, Issue 11
Energy trapping and detrapping in the photosynthetic bacterium Rhodopseudomonas viridis: transfer-to-trap-limited dynamics
journal, May 1995
- Timpmann, Kõu; Freiberg, Arvi; Sundström, Villy
- Chemical Physics, Vol. 194, Issue 2-3
Adaptation of intracytoplasmic membranes to altered light intensity in Rhodobacter sphaeroides
journal, September 2012
- Adams, Peter G.; Hunter, C. Neil
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 9
Structure and functional organization of light-harvesting complexes and photochemical reaction centers in membranes of phototrophic bacteria
journal, March 1985
- Drews, G.
- Microbiological Reviews, p. 59-70
Picosecond dynamics of directed excitation transfer in spectrally heterogeneous light-harvesting antenna of purple bacteria
journal, January 1989
- Freiberg, A.; Godik, V. I.; Pullerits, T.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 973, Issue 1
Role of the PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 2. PufX is required for efficient ubiquinone/ubiquinol exchange between the reaction center QB site and the cytochrome bc1 complex.
journal, November 1995
- Barz, Wolfgang P.; Vermeglio, Andre; Francia, Francesco
- Biochemistry, Vol. 34, Issue 46
Kinetics of picosecond bacteriochlorophyll luminescence in vivo as a function of the reaction center state
journal, May 1985
- Borisov, A. Yu; Freiberg, A. M.; Godik, V. I.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 807, Issue 3
Monomeric RC–LH1 core complexes retard LH2 assembly and intracytoplasmic membrane formation in PufX-minus mutants of Rhodobacter sphaeroides
journal, September 2011
- Adams, Peter G.; Mothersole, David J.; Ng, Irene W.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 9
Excitation Energy Transfer and Trapping in Higher Plant Photosystem II Complexes with Different Antenna Sizes
journal, May 2011
- Caffarri, Stefano; Broess, Koen; Croce, Roberta
- Biophysical Journal, Vol. 100, Issue 9
Zur Theorie der Assimilation
journal, February 1936
- Gaffron, H.; Wohl, K.
- Die Naturwissenschaften, Vol. 24, Issue 7
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
Three-dimensional Reconstruction of a Membrane-bending Complex
journal, March 2008
- Qian, Pu; Bullough, Per A.; Hunter, C. Neil
- Journal of Biological Chemistry, Vol. 283, Issue 20
Photochemical Electron Transport in Photosynthetic Reaction Centers
journal, October 1972
- Clayton, Roderick K.; Straley, Susan C.
- Biophysical Journal, Vol. 12, Issue 10
Membrane invagination in Rhodobacter sphaeroides is initiated at curved regions of the cytoplasmic membrane, then forms both budded and fully detached spherical vesicles: Membrane biogenesis in Rba. sphaeroides
journal, April 2010
- Tucker, Jaimey D.; Siebert, C. Alistair; Escalante, Maryana
- Molecular Microbiology, Vol. 76, Issue 4
Energy Transfer in Light-Adapted Photosynthetic Membranes: From Active to Saturated Photosynthesis
journal, November 2009
- Fassioli, Francesca; Olaya-Castro, Alexandra; Scheuring, Simon
- Biophysical Journal, Vol. 97, Issue 9
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
Transfer of Energy from Bacteriochlorophyll to a Reaction Centre During Bacterial Photosynthesis
journal, January 1963
- Vredenberg, W. J.; Duysens, L. N. M.
- Nature, Vol. 197, Issue 4865
Fluorescence Micro-Spectroscopy Study of Individual Photosynthetic Membrane Vesicles and Light-Harvesting Complexes
journal, August 2013
- Leiger, Kristjan; Reisberg, Liis; Freiberg, Arvi
- The Journal of Physical Chemistry B, Vol. 117, Issue 32
Energy trapping and detrapping by wild type and mutant reaction centers of purple non-sulfur bacteria
journal, May 1996
- Freiberg, Arvi; Allen, James P.; Williams, JoAnn C.
- Photosynthesis Research, Vol. 48, Issue 1-2
Membrane potential effect on nanosecond recombination luminescence in Rhodospirillum rubrum
journal, September 1980
- Borisov, A. Yu.; Godik, V. I.; Kotova, E. A.
- FEBS Letters, Vol. 119, Issue 1
Excitons in Intact Cells of Photosynthetic Bacteria
journal, February 2013
- Freiberg, Arvi; Pajusalu, Mihkel; Rätsep, Margus
- The Journal of Physical Chemistry B, Vol. 117, Issue 38
Picosecond fluorescence spectroscope of light-harvesting antenna complexes from Rhodospirillum rubrum in the 300-4 K temperature range. Comparison with the data on chromatophores
journal, August 1992
- Freiberg, Arvi; Timpmann, Kõu
- Journal of Photochemistry and Photobiology B: Biology, Vol. 15, Issue 1-2
Photosynthetic Vesicle Architecture and Constraints on Efficient Energy Harvesting
journal, July 2010
- Şener, Melih; Strümpfer, Johan; Timney, John A.
- Biophysical Journal, Vol. 99, Issue 1
Fluorescence Yield Properties of a Fraction Enriched in Newly Synthesized Bacteriochlorophyll U-Protein Complexes from Rhodopseudomonas Sphaeroides
journal, August 1979
- Hunter, C. Neil; Grondelle, Renk van; Holes, Nigel G.
- Photochemistry and Photobiology, Vol. 30, Issue 2
Detrapping of excitation energy from the reaction centre in the photosynthetic purple bacterium Rhodospirillum rubrum
journal, November 1993
- Timpmann, Kõu; Zhang, Fu Geng; Freiberg, Arvi
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1183, Issue 1
Electronic Couplings and Energy Transfer Dynamics in the Oxidized Primary Electron Donor of the Bacterial Reaction Center
journal, February 2004
- Jordanides, Xanthipe J.; Scholes, Gregory D.; Shapley, Warwick A.
- The Journal of Physical Chemistry B, Vol. 108, Issue 5
Towards an understanding of photosynthetic acclimation
journal, November 2004
- Walters, R. G.
- Journal of Experimental Botany, Vol. 56, Issue 411
Pico- and nanosecond fluorescence kinetics of Photosystem II reaction centre and its complex with CP47 antenna
journal, February 1994
- Freiberg, Arvi; Timpmann, Kõu; Moskalenko, Andrei A.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1184, Issue 1
Solar light harvesting by energy transfer: from ecology to coherence
journal, January 2012
- Scholes, Gregory D.; Mirkovic, Tihana; Turner, Daniel B.
- Energy & Environmental Science, Vol. 5, Issue 11
Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides.
journal, January 1988
- Kiley, P. J.; Kaplan, S.
- Microbiological Reviews, Vol. 52, Issue 1
Picosecond spectrochronography
journal, April 1983
- Freiberg, A.; Saari, P.
- IEEE Journal of Quantum Electronics, Vol. 19, Issue 4
Chromatic Adaptation of Photosynthetic Membranes
journal, July 2005
- Scheuring, S.
- Science, Vol. 309, Issue 5733
Spectral fine-tuning in excitonically coupled cyclic photosynthetic antennas
journal, November 2010
- Freiberg, Arvi; Timpmann, Kõu; Trinkunas, Gediminas
- Chemical Physics Letters, Vol. 500, Issue 1-3
Tracking energy transfer between light harvesting complex 2 and 1 in photosynthetic membranes grown under high and low illumination
journal, January 2012
- Luer, L.; Moulisova, V.; Henry, S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
Trapping, loss and annihilation of excitations in a photosynthetic system
journal, December 1983
- Bakker, J. G. C.; Van Grondelle, R.; Den Hollander, W. T. F.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 725, Issue 3
‘Uphill’ Energy Transfer in a Photosynthetic Bacterium
journal, January 1969
- Zankel, Kenneth L.; Clayton, Roderick K.
- Photochemistry and Photobiology, Vol. 9, Issue 1
Membranes of Rhodopseudomonas sphaeroides. VI. Isolation of a fraction enriched in newly synthesized bacteriochlorophyll a-protein complexes
journal, August 1979
- Niederman, Robert A.; Mallon, David E.; Parks, Lawrence C.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 555, Issue 2
Mutants of Rhodobacter sphaeroides lacking one or more pigment-protein complexes and complementation with reaction-centre, LH1, and LH2 genes
journal, May 1992
- Jones, M. R.; Fowler, G. J. S.; Gibson, L. C. D.
- Molecular Microbiology, Vol. 6, Issue 9
The Mechanism of Energy Transfer in the Bacterial Photosynthetic Reaction Center
journal, March 2001
- Jordanides, Xanthipe J.; Scholes, Gregory D.; Fleming, Graham R.
- The Journal of Physical Chemistry B, Vol. 105, Issue 8
Excitation trapping by different states of photosynthetic reaction centres
journal, October 1977
- Godik, V. I.; Borisov, A. Yu.
- FEBS Letters, Vol. 82, Issue 2
Excitation energy transfer, trapping and annihilation in photosynthetic systems
journal, June 1985
- van Grondelle, R.
- Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 811, Issue 2
Excitation transfer connectivity in different purple bacteria: A theoretical and experimental study
journal, November 2010
- de Rivoyre, Matthieu; Ginet, Nicolas; Bouyer, Pierre
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 11
Photosynthetic apparatus of purple bacteria
journal, February 2002
- Hu, Xiche; Ritz, Thorsten; Damjanović, Ana
- Quarterly Reviews of Biophysics, Vol. 35, Issue 1
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
The Crystallographic Structure of the B800-820 LH3 Light-Harvesting Complex from the Purple Bacteria Rhodopseudomonas Acidophila Strain 7050 †
journal, July 2001
- McLuskey, K.; Prince, S. M.; Cogdell, R. J.
- Biochemistry, Vol. 40, Issue 30
Directed picosecond excitation transport in purple photosynthetic bacteria
journal, December 1988
- Freiberg, A.; Godik, V. I.; Pullerits, T.
- Chemical Physics, Vol. 128, Issue 1
Antenna size dependent exciton dynamics in the chlorosomal antenna of the green bacteriumChloroflexus aurantiacus
journal, April 1996
- Fetisova, Zoya; Freiberg, Arvi; Novoderezhkin, Vladimir
- FEBS Letters, Vol. 383, Issue 3
The 7.5-Å Electron Density and Spectroscopic Properties of a NovelLow-Light B800 LH2 from Rhodopseudomonas palustris
journal, February 2002
- Hartigan, Nichola; Tharia, Hazel A.; Sweeney, Frank
- Biophysical Journal, Vol. 82, Issue 2
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
Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates.
journal, March 1987
- Owens, T. G.; Webb, S. P.; Mets, L.
- Proceedings of the National Academy of Sciences, Vol. 84, Issue 6
Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX
journal, February 2004
- Siebert, C. Alistair; Qian, Pu; Fotiadis, Dimitrios
- The EMBO Journal, Vol. 23, Issue 4
The purple bacterial photosynthetic unit
journal, May 1996
- Cogdell, Richard J.; Fyfe, Paul K.; Barrett, Stuart J.
- Photosynthesis Research, Vol. 48, Issue 1-2