Cryo-EM structures of light-harvesting 2 complexes from Rhodopseudomonas palustris reveal the molecular origin of absorption tuning

Qian, Pu; Nguyen-Phan, Cam T.; Gardiner, Alastair T.; Croll, Tristan I.; Roszak, Aleksander W.; Southall, June; Jackson, Philip J.; Vasilev, Cvetelin; Castro-Hartmann, Pablo; Sader, Kasim; Hunter, C. Neil; Cogdell, Richard J.

doi:10.1073/pnas.2210109119

Title: Cryo-EM structures of light-harvesting 2 complexes from Rhodopseudomonas palustris reveal the molecular origin of absorption tuning

Abstract

The genomes of some purple photosynthetic bacteria contain a multigene puc family encoding a series of α- and β-polypeptides that together form a heterogeneous antenna of light-harvesting 2 (LH2) complexes. To unravel this complexity, we generated four sets of puc deletion mutants in Rhodopseudomonas palustris , each encoding a single type of pucBA gene pair and enabling the purification of complexes designated as PucA-LH2, PucB-LH2, PucD-LH2, and PucE-LH2. The structures of all four purified LH2 complexes were determined by cryogenic electron microscopy (cryo-EM) at resolutions ranging from 2.7 to 3.6 Å. Uniquely, each of these complexes contains a hitherto unknown polypeptide, γ, that forms an extended undulating ribbon that lies in the plane of the membrane and that encloses six of the nine LH2 αβ-subunits. The γ-subunit, which is located near to the cytoplasmic side of the complex, breaks the C9 symmetry of the LH2 complex and binds six extra bacteriochlorophylls (BChls) that enhance the 800-nm absorption of each complex. The structures show that all four complexes have two complete rings of BChls, conferring absorption bands centered at 800 and 850 nm on the PucA-LH2, PucB-LH2, and PucE-LH2 complexes, but, unusually, the PucD-LH2 antenna has only a single strong near-infaredmore »« less

Authors:

Qian, Pu ^[1]; Nguyen-Phan, Cam T. ^[2];

^[3];

^[4];

^[2]; Southall, June ^[2];

^[5]; Vasilev, Cvetelin ^[5];

^[1]; Sader, Kasim ^[1];

^[5];

^[2]

Materials and Structure Analysis, Thermofisher Scientific, Eindhoven, 5651 GG The Netherlands
School of Molecular Biosciences, Glasgow University, Glasgow G12 8QQ, United Kingdom
Laboratory of Anoxygenic Phototrophs, Institute of Microbiology, Czech Academy of Sciences, Třeboň, 37981 Czechia
Cambridge Institute for Medical Research, University of Cambridge, Cambridge CB2 0XY, United Kingdom
School of Biosciences, The University of Sheffield, Sheffield S10 2TN, United Kingdom

Publication Date:: Mon Oct 17 00:00:00 EDT 2022

Sponsoring Org.:: USDOE

OSTI Identifier:: 1893223

Grant/Contract Number:: SC0001035

Resource Type:: Published Article

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 119 Journal Issue: 43; Journal ID: ISSN 0027-8424

Publisher:: Proceedings of the National Academy of Sciences

Country of Publication:: United States

Language:: English

Citation Formats


                    Qian, Pu, Nguyen-Phan, Cam T., Gardiner, Alastair T., Croll, Tristan I., Roszak, Aleksander W., Southall, June, Jackson, Philip J., Vasilev, Cvetelin, Castro-Hartmann, Pablo, Sader, Kasim, Hunter, C. Neil, and Cogdell, Richard J. Cryo-EM structures of light-harvesting 2 complexes from Rhodopseudomonas palustris reveal the molecular origin of absorption tuning.  United States: N. p., 2022. 
Web.  doi:10.1073/pnas.2210109119.

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                    Qian, Pu, Nguyen-Phan, Cam T., Gardiner, Alastair T., Croll, Tristan I., Roszak, Aleksander W., Southall, June, Jackson, Philip J., Vasilev, Cvetelin, Castro-Hartmann, Pablo, Sader, Kasim, Hunter, C. Neil, & Cogdell, Richard J. Cryo-EM structures of light-harvesting 2 complexes from Rhodopseudomonas palustris reveal the molecular origin of absorption tuning.  United States.  https://doi.org/10.1073/pnas.2210109119

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                    Qian, Pu, Nguyen-Phan, Cam T., Gardiner, Alastair T., Croll, Tristan I., Roszak, Aleksander W., Southall, June, Jackson, Philip J., Vasilev, Cvetelin, Castro-Hartmann, Pablo, Sader, Kasim, Hunter, C. Neil, and Cogdell, Richard J. Mon .  
"Cryo-EM structures of light-harvesting 2 complexes from Rhodopseudomonas palustris reveal the molecular origin of absorption tuning".  United States.  https://doi.org/10.1073/pnas.2210109119.

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@article{osti_1893223,

  title        = {Cryo-EM structures of light-harvesting 2 complexes from Rhodopseudomonas palustris reveal the molecular origin of absorption tuning},

  author       = {Qian, Pu and Nguyen-Phan, Cam T. and Gardiner, Alastair T. and Croll, Tristan I. and Roszak, Aleksander W. and Southall, June and Jackson, Philip J. and Vasilev, Cvetelin and Castro-Hartmann, Pablo and Sader, Kasim and Hunter, C. Neil and Cogdell, Richard J.},

  abstractNote = {The genomes of some purple photosynthetic bacteria contain a multigene puc family encoding a series of α- and β-polypeptides that together form a heterogeneous antenna of light-harvesting 2 (LH2) complexes. To unravel this complexity, we generated four sets of puc deletion mutants in Rhodopseudomonas palustris , each encoding a single type of pucBA gene pair and enabling the purification of complexes designated as PucA-LH2, PucB-LH2, PucD-LH2, and PucE-LH2. The structures of all four purified LH2 complexes were determined by cryogenic electron microscopy (cryo-EM) at resolutions ranging from 2.7 to 3.6 Å. Uniquely, each of these complexes contains a hitherto unknown polypeptide, γ, that forms an extended undulating ribbon that lies in the plane of the membrane and that encloses six of the nine LH2 αβ-subunits. The γ-subunit, which is located near to the cytoplasmic side of the complex, breaks the C9 symmetry of the LH2 complex and binds six extra bacteriochlorophylls (BChls) that enhance the 800-nm absorption of each complex. The structures show that all four complexes have two complete rings of BChls, conferring absorption bands centered at 800 and 850 nm on the PucA-LH2, PucB-LH2, and PucE-LH2 complexes, but, unusually, the PucD-LH2 antenna has only a single strong near-infared (NIR) absorption peak at 803 nm. Comparison of the cryo-EM structures of these LH2 complexes reveals altered patterns of hydrogen bonds between LH2 αβ-side chains and the bacteriochlorin rings, further emphasizing the major role that H bonds play in spectral tuning of bacterial antenna complexes.},

  doi          = {10.1073/pnas.2210109119},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 43,

  volume       = 119,

  place        = {United States},

  year         = {Mon Oct 17 00:00:00 EDT 2022},

  month        = {Mon Oct 17 00:00:00 EDT 2022}

}

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Abstract

Citation Formats

The 2.4 Å cryo-EM structure of a heptameric light-harvesting 2 complex reveals two carotenoid energy transfer pathways journal, February 2021

Rhodobacter capsulatus puc operon: promoter location, transcript sizes and effects of deletions on photosynthetic growth journal, January 1993

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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

Developmental acclimation of the thylakoid proteome to light intensity in Arabidopsis journal, November 2020

A Second and Unusual pucBA Operon of Rhodobacter sphaeroides 2.4.1: Genetics and Function of the Encoded Polypeptides journal, October 2003

Controlling Photosynthetic Excitons by Selective Pigment Photooxidation journal, December 2018

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

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

The Synthesis and Assembly of Functional High and Low Light LH2 Antenna Complexes from Rhodopseudomonas palustris in Rhodobacter sphaeroides journal, June 1996

DNA-directed spatial assembly of photosynthetic light-harvesting proteins journal, January 2016

Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix journal, October 2019

cisTEM, user-friendly software for single-particle image processing journal, March 2018

Atomic Force Microscopy Studies of Native Photosynthetic Membranes † journal, May 2009

Cloning, DNA sequence, and expression of the Rhodobacter sphaeroides light-harvesting B800-850-alpha and B800-850-beta genes. journal, July 1987

Industrial cryo-EM facility setup and management journal, April 2020

Control of Synthesis of Reaction Center Bacteriochlorophyll in Photosynthetic Bacteria journal, February 1972

Adaptation of Rhodopseudomonas acidophila strain 7050 to growth at different light intensities: what are the benefits to changing the type of LH2? journal, January 2018

CTFFIND4: Fast and accurate defocus estimation from electron micrographs journal, November 2015

Conformational and environmental effects on bacteriochlorophyll optical spectra: correlations of calculated spectra with structural results journal, July 1990

Highly accurate protein structure prediction with AlphaFold journal, July 2021

Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands journal, February 1992

The origin of the unusual Qy red shift in LH1–RC complexes from purple bacteria Thermochromatium tepidum as revealed by Stark absorption spectroscopy journal, December 2015

New tools for automated high-resolution cryo-EM structure determination in RELION-3 journal, November 2018

Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells journal, October 2017

Cryo-EM Structure of the Rhodobacter sphaeroides Light-Harvesting 2 Complex at 2.1 Å journal, October 2021

Characterisation of a pucBA deletion mutant from Rhodopseudomonas palustris lacking all but the pucBAd genes journal, May 2017

Blue shifts in bacteriochlorophyll absorbance correlate with changed hydrogen bonding patterns in light-harvesting 2 mutants of Rhodobacter sphaeroides with alterations at α-Tyr-44 and α-Tyr-45 journal, May 1994

Evaluating the Nature of So-Called S*-State Feature in Transient Absorption of Carotenoids in Light-Harvesting Complex 2 (LH2) from Purple Photosynthetic Bacteria journal, October 2016

UCSF Chimera?A visualization system for exploratory research and analysis journal, January 2004

The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum journal, May 1996

The light intensity under which cells are grown controls the type of peripheral light-harvesting complexes that are assembled in a purple photosynthetic bacterium journal, October 2011

The effects of hydrogen bonding and coordination interaction in visible absorption and vibrational spectra of chlorophyll a journal, September 1989

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

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

Antenna organization of Rhodopseudomonas acidophila: a study of the excitation migration journal, September 1991

In situ formation of photoactive B-ring reduced chlorophyll isomer in photosynthetic protein LH2 journal, November 2020

Cryo-EM structure of the Blastochloris viridis LH1–RC complex at 2.9 Å journal, April 2018

Ab Initio Molecular Orbital Calculations of Electronic Couplings in the LH2 Bacterial Light-Harvesting Complex of Rps. Acidophila journal, April 1999

Coot model-building tools for molecular graphics journal, November 2004

Use of single-molecule spectroscopy to tackle fundamental problems in biochemistry: using studies on purple bacterial antenna complexes as an example journal, August 2009

The effect of growth conditions on the light-harvesting apparatus in Rhodopseudomonas acidophila journal, November 1993

Chromatic Adaptation of Photosynthetic Membranes journal, July 2005

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

Multiple copies of the coding regions for the light-harvesting B800-850 alpha- and beta-polypeptides are present in the Rhodopseudomonas palustris genome. journal, May 1989

Light-harvesting II (B800-B850 complex) structural genes from Rhodopseudomonas capsulata journal, January 1985

Top-Down Mass Spectrometry Analysis of Membrane-Bound Light-Harvesting Complex 2 from Rhodobacter sphaeroides journal, November 2015

Energy transfer in photosynthetic light-harvesting antennas journal, August 1990

Molecular Origins and Consequences of High-800 LH2 in Roseobacter denitrificans journal, August 2011

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

The native architecture of a photosynthetic membrane journal, August 2004

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

Cloning, nucleotide sequence and transfer of genes for the B800-850 light harvesting complex of Rhodobacter sphaeroides journal, March 1987

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

Light harvesting in phototrophic bacteria: structure and function journal, June 2017

Computational Modeling of Exciton-Bath Hamiltonians for Light Harvesting 2 and Light Harvesting 3 Complexes of Purple Photosynthetic Bacteria at Room Temperature journal, March 2018

Comparative Studies of Protein Properties and Bacteriochlorophyll Contents of Bacteriochlorophyll-Protein Complexes from Spectrally Different Types of Rhodopseudomonas palustris journal, October 1982

The 2.4 Å cryo-EM structure of a heptameric light-harvesting 2 complex reveals two carotenoid energy transfer pathways
journal, February 2021

Rhodobacter capsulatus puc operon: promoter location, transcript sizes and effects of deletions on photosynthetic growth
journal, January 1993

ISOLDE : a physically realistic environment for model building into low-resolution electron-density maps
journal, April 2018

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

Developmental acclimation of the thylakoid proteome to light intensity in Arabidopsis
journal, November 2020

A Second and Unusual pucBA Operon of Rhodobacter sphaeroides 2.4.1: Genetics and Function of the Encoded Polypeptides
journal, October 2003

Controlling Photosynthetic Excitons by Selective Pigment Photooxidation
journal, December 2018

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

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

The Synthesis and Assembly of Functional High and Low Light LH2 Antenna Complexes from Rhodopseudomonas palustris in Rhodobacter sphaeroides
journal, June 1996

DNA-directed spatial assembly of photosynthetic light-harvesting proteins
journal, January 2016

Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix
journal, October 2019

cisTEM, user-friendly software for single-particle image processing
journal, March 2018

Atomic Force Microscopy Studies of Native Photosynthetic Membranes ^†
journal, May 2009

Cloning, DNA sequence, and expression of the Rhodobacter sphaeroides light-harvesting B800-850-alpha and B800-850-beta genes.
journal, July 1987

Industrial cryo-EM facility setup and management
journal, April 2020

Control of Synthesis of Reaction Center Bacteriochlorophyll in Photosynthetic Bacteria
journal, February 1972

Adaptation of Rhodopseudomonas acidophila strain 7050 to growth at different light intensities: what are the benefits to changing the type of LH2?
journal, January 2018

CTFFIND4: Fast and accurate defocus estimation from electron micrographs
journal, November 2015

Conformational and environmental effects on bacteriochlorophyll optical spectra: correlations of calculated spectra with structural results
journal, July 1990

Highly accurate protein structure prediction with AlphaFold
journal, July 2021

Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands
journal, February 1992

The origin of the unusual Qy red shift in LH1–RC complexes from purple bacteria Thermochromatium tepidum as revealed by Stark absorption spectroscopy
journal, December 2015

New tools for automated high-resolution cryo-EM structure determination in RELION-3
journal, November 2018

Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells
journal, October 2017

Cryo-EM Structure of the Rhodobacter sphaeroides Light-Harvesting 2 Complex at 2.1 Å
journal, October 2021

Characterisation of a pucBA deletion mutant from Rhodopseudomonas palustris lacking all but the pucBAd genes
journal, May 2017

Blue shifts in bacteriochlorophyll absorbance correlate with changed hydrogen bonding patterns in light-harvesting 2 mutants of Rhodobacter sphaeroides with alterations at α-Tyr-44 and α-Tyr-45
journal, May 1994

Evaluating the Nature of So-Called S*-State Feature in Transient Absorption of Carotenoids in Light-Harvesting Complex 2 (LH2) from Purple Photosynthetic Bacteria
journal, October 2016

UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum
journal, May 1996

The light intensity under which cells are grown controls the type of peripheral light-harvesting complexes that are assembled in a purple photosynthetic bacterium
journal, October 2011

The effects of hydrogen bonding and coordination interaction in visible absorption and vibrational spectra of chlorophyll a
journal, September 1989

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

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

Antenna organization of Rhodopseudomonas acidophila: a study of the excitation migration
journal, September 1991

In situ formation of photoactive B-ring reduced chlorophyll isomer in photosynthetic protein LH2
journal, November 2020

Cryo-EM structure of the Blastochloris viridis LH1–RC complex at 2.9 Å
journal, April 2018

Ab Initio Molecular Orbital Calculations of Electronic Couplings in the LH2 Bacterial Light-Harvesting Complex of Rps. Acidophila
journal, April 1999

Coot model-building tools for molecular graphics
journal, November 2004

Use of single-molecule spectroscopy to tackle fundamental problems in biochemistry: using studies on purple bacterial antenna complexes as an example
journal, August 2009

The effect of growth conditions on the light-harvesting apparatus in Rhodopseudomonas acidophila
journal, November 1993

Chromatic Adaptation of Photosynthetic Membranes
journal, July 2005

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

Multiple copies of the coding regions for the light-harvesting B800-850 alpha- and beta-polypeptides are present in the Rhodopseudomonas palustris genome.
journal, May 1989

Light-harvesting II (B800-B850 complex) structural genes from Rhodopseudomonas capsulata
journal, January 1985

Top-Down Mass Spectrometry Analysis of Membrane-Bound Light-Harvesting Complex 2 from Rhodobacter sphaeroides
journal, November 2015

Energy transfer in photosynthetic light-harvesting antennas
journal, August 1990

Molecular Origins and Consequences of High-800 LH2 in Roseobacter denitrificans
journal, August 2011

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

The native architecture of a photosynthetic membrane
journal, August 2004

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

Cloning, nucleotide sequence and transfer of genes for the B800-850 light harvesting complex of Rhodobacter sphaeroides
journal, March 1987

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

Light harvesting in phototrophic bacteria: structure and function
journal, June 2017

Computational Modeling of Exciton-Bath Hamiltonians for Light Harvesting 2 and Light Harvesting 3 Complexes of Purple Photosynthetic Bacteria at Room Temperature
journal, March 2018

Comparative Studies of Protein Properties and Bacteriochlorophyll Contents of Bacteriochlorophyll-Protein Complexes from Spectrally Different Types of Rhodopseudomonas palustris
journal, October 1982