Efficiency of light harvesting in a photosynthetic bacterium adapted to different levels of light

Timpmann, Kõu; Chenchiliyan, Manoop; Jalviste, Erko; Timney, John A.; Hunter, C. Neil; Freiberg, Arvi

doi:10.1016/j.bbabio.2014.06.007

Title: 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 »« less

Authors:: Timpmann, Kõu; Chenchiliyan, Manoop; Jalviste, Erko; Timney, John A.; Hunter, C. Neil; Freiberg, Arvi

Publication Date:: Wed Oct 01 00:00:00 EDT 2014

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.

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                    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

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                    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.

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@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}

}

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Title: Efficiency of light harvesting in a photosynthetic bacterium adapted to different levels of light

Abstract

Citation Formats

A master equation theory of fluorescence induction, photochemical yield, and singlet-triplet exciton quenching in photosynthetic systems journal, October 1983

A Role for a Light-Harvesting Antenna Complex of Photosystem II in Photoprotection journal, August 2002

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

The architecture of Rhodobacter sphaeroides chromatophores journal, August 2014

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

Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light-harvesting 1 antenna of Rhodobacter sphaeroides. journal, July 1994

The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes journal, August 2006

Control of Photosystem Formation inRhodobacter sphaeroides journal, June 1998

Energy trapping and detrapping in the photosynthetic bacterium Rhodopseudomonas viridis: transfer-to-trap-limited dynamics journal, May 1995

Adaptation of intracytoplasmic membranes to altered light intensity in Rhodobacter sphaeroides journal, September 2012

Structure and functional organization of light-harvesting complexes and photochemical reaction centers in membranes of phototrophic bacteria journal, March 1985

Picosecond dynamics of directed excitation transfer in spectrally heterogeneous light-harvesting antenna of purple bacteria journal, January 1989

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

Kinetics of picosecond bacteriochlorophyll luminescence in vivo as a function of the reaction center state journal, May 1985

Monomeric RC–LH1 core complexes retard LH2 assembly and intracytoplasmic membrane formation in PufX-minus mutants of Rhodobacter sphaeroides journal, September 2011

Excitation Energy Transfer and Trapping in Higher Plant Photosystem II Complexes with Different Antenna Sizes journal, May 2011

Zur Theorie der Assimilation journal, February 1936

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

Three-dimensional Reconstruction of a Membrane-bending Complex journal, March 2008

Photochemical Electron Transport in Photosynthetic Reaction Centers journal, October 1972

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

Energy Transfer in Light-Adapted Photosynthetic Membranes: From Active to Saturated Photosynthesis journal, November 2009

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

Transfer of Energy from Bacteriochlorophyll to a Reaction Centre During Bacterial Photosynthesis journal, January 1963

Fluorescence Micro-Spectroscopy Study of Individual Photosynthetic Membrane Vesicles and Light-Harvesting Complexes journal, August 2013

Energy trapping and detrapping by wild type and mutant reaction centers of purple non-sulfur bacteria journal, May 1996

Membrane potential effect on nanosecond recombination luminescence in Rhodospirillum rubrum journal, September 1980

Excitons in Intact Cells of Photosynthetic Bacteria journal, February 2013

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

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

Fluorescence Yield Properties of a Fraction Enriched in Newly Synthesized Bacteriochlorophyll U-Protein Complexes from Rhodopseudomonas Sphaeroides journal, August 1979

Detrapping of excitation energy from the reaction centre in the photosynthetic purple bacterium Rhodospirillum rubrum journal, November 1993

Electronic Couplings and Energy Transfer Dynamics in the Oxidized Primary Electron Donor of the Bacterial Reaction Center journal, February 2004

Towards an understanding of photosynthetic acclimation journal, November 2004

Pico- and nanosecond fluorescence kinetics of Photosystem II reaction centre and its complex with CP47 antenna journal, February 1994

Solar light harvesting by energy transfer: from ecology to coherence journal, January 2012

Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. journal, January 1988

Picosecond spectrochronography journal, April 1983

Chromatic Adaptation of Photosynthetic Membranes journal, July 2005

Spectral fine-tuning in excitonically coupled cyclic photosynthetic antennas journal, November 2010

Tracking energy transfer between light harvesting complex 2 and 1 in photosynthetic membranes grown under high and low illumination journal, January 2012

Trapping, loss and annihilation of excitations in a photosynthetic system journal, December 1983

‘Uphill’ Energy Transfer in a Photosynthetic Bacterium journal, January 1969

Membranes of Rhodopseudomonas sphaeroides. VI. Isolation of a fraction enriched in newly synthesized bacteriochlorophyll a-protein complexes journal, August 1979

Mutants of Rhodobacter sphaeroides lacking one or more pigment-protein complexes and complementation with reaction-centre, LH1, and LH2 genes journal, May 1992

The Mechanism of Energy Transfer in the Bacterial Photosynthetic Reaction Center journal, March 2001

Excitation trapping by different states of photosynthetic reaction centres journal, October 1977

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

Excitation transfer connectivity in different purple bacteria: A theoretical and experimental study journal, November 2010

Photosynthetic apparatus of purple bacteria journal, February 2002

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

The Crystallographic Structure of the B800-820 LH3 Light-Harvesting Complex from the Purple Bacteria Rhodopseudomonas Acidophila Strain 7050 † journal, July 2001

Directed picosecond excitation transport in purple photosynthetic bacteria journal, December 1988

Antenna size dependent exciton dynamics in the chlorosomal antenna of the green bacteriumChloroflexus aurantiacus journal, April 1996

The 7.5-Å Electron Density and Spectroscopic Properties of a NovelLow-Light B800 LH2 from Rhodopseudomonas palustris journal, February 2002

Lessons from nature about solar light harvesting journal, September 2011

Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates. journal, March 1987

Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX journal, February 2004

The purple bacterial photosynthetic unit journal, May 1996

A master equation theory of fluorescence induction, photochemical yield, and singlet-triplet exciton quenching in photosynthetic systems
journal, October 1983

A Role for a Light-Harvesting Antenna Complex of Photosystem II in Photoprotection
journal, August 2002

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

The architecture of Rhodobacter sphaeroides chromatophores
journal, August 2014

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

Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light-harvesting 1 antenna of Rhodobacter sphaeroides.
journal, July 1994

The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes
journal, August 2006

Control of Photosystem Formation inRhodobacter sphaeroides
journal, June 1998

Energy trapping and detrapping in the photosynthetic bacterium Rhodopseudomonas viridis: transfer-to-trap-limited dynamics
journal, May 1995

Adaptation of intracytoplasmic membranes to altered light intensity in Rhodobacter sphaeroides
journal, September 2012

Structure and functional organization of light-harvesting complexes and photochemical reaction centers in membranes of phototrophic bacteria
journal, March 1985

Picosecond dynamics of directed excitation transfer in spectrally heterogeneous light-harvesting antenna of purple bacteria
journal, January 1989

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

Kinetics of picosecond bacteriochlorophyll luminescence in vivo as a function of the reaction center state
journal, May 1985

Monomeric RC–LH1 core complexes retard LH2 assembly and intracytoplasmic membrane formation in PufX-minus mutants of Rhodobacter sphaeroides
journal, September 2011

Excitation Energy Transfer and Trapping in Higher Plant Photosystem II Complexes with Different Antenna Sizes
journal, May 2011

Zur Theorie der Assimilation
journal, February 1936

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

Three-dimensional Reconstruction of a Membrane-bending Complex
journal, March 2008

Photochemical Electron Transport in Photosynthetic Reaction Centers
journal, October 1972

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

Energy Transfer in Light-Adapted Photosynthetic Membranes: From Active to Saturated Photosynthesis
journal, November 2009

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

Transfer of Energy from Bacteriochlorophyll to a Reaction Centre During Bacterial Photosynthesis
journal, January 1963

Fluorescence Micro-Spectroscopy Study of Individual Photosynthetic Membrane Vesicles and Light-Harvesting Complexes
journal, August 2013

Energy trapping and detrapping by wild type and mutant reaction centers of purple non-sulfur bacteria
journal, May 1996

Membrane potential effect on nanosecond recombination luminescence in Rhodospirillum rubrum
journal, September 1980

Excitons in Intact Cells of Photosynthetic Bacteria
journal, February 2013

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

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

Fluorescence Yield Properties of a Fraction Enriched in Newly Synthesized Bacteriochlorophyll U-Protein Complexes from Rhodopseudomonas Sphaeroides
journal, August 1979

Detrapping of excitation energy from the reaction centre in the photosynthetic purple bacterium Rhodospirillum rubrum
journal, November 1993

Electronic Couplings and Energy Transfer Dynamics in the Oxidized Primary Electron Donor of the Bacterial Reaction Center
journal, February 2004

Towards an understanding of photosynthetic acclimation
journal, November 2004

Pico- and nanosecond fluorescence kinetics of Photosystem II reaction centre and its complex with CP47 antenna
journal, February 1994

Solar light harvesting by energy transfer: from ecology to coherence
journal, January 2012

Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides.
journal, January 1988

Picosecond spectrochronography
journal, April 1983

Chromatic Adaptation of Photosynthetic Membranes
journal, July 2005

Spectral fine-tuning in excitonically coupled cyclic photosynthetic antennas
journal, November 2010

Tracking energy transfer between light harvesting complex 2 and 1 in photosynthetic membranes grown under high and low illumination
journal, January 2012

Trapping, loss and annihilation of excitations in a photosynthetic system
journal, December 1983

‘Uphill’ Energy Transfer in a Photosynthetic Bacterium
journal, January 1969

Membranes of Rhodopseudomonas sphaeroides. VI. Isolation of a fraction enriched in newly synthesized bacteriochlorophyll a-protein complexes
journal, August 1979

Mutants of Rhodobacter sphaeroides lacking one or more pigment-protein complexes and complementation with reaction-centre, LH1, and LH2 genes
journal, May 1992

The Mechanism of Energy Transfer in the Bacterial Photosynthetic Reaction Center
journal, March 2001

Excitation trapping by different states of photosynthetic reaction centres
journal, October 1977

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

Excitation transfer connectivity in different purple bacteria: A theoretical and experimental study
journal, November 2010

Photosynthetic apparatus of purple bacteria
journal, February 2002

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

The Crystallographic Structure of the B800-820 LH3 Light-Harvesting Complex from the Purple Bacteria Rhodopseudomonas Acidophila Strain 7050 ^†
journal, July 2001

Directed picosecond excitation transport in purple photosynthetic bacteria
journal, December 1988

Antenna size dependent exciton dynamics in the chlorosomal antenna of the green bacteriumChloroflexus aurantiacus
journal, April 1996

The 7.5-Å Electron Density and Spectroscopic Properties of a NovelLow-Light B800 LH2 from Rhodopseudomonas palustris
journal, February 2002

Lessons from nature about solar light harvesting
journal, September 2011

Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates.
journal, March 1987

Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX
journal, February 2004

The purple bacterial photosynthetic unit
journal, May 1996