Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light

Gisriel, Christopher J.; Huang, Hao-Li; Reiss, Krystle M.; Flesher, David A.; Batista, Victor S.; Bryant, Donald A.; Brudvig, Gary W.; Wang, Jimin

doi:10.1016/j.bbadva.2021.100019

Title: Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light

Abstract

Chlorophyll cofactors are vital for the metabolism of photosynthetic organisms. Cryo-electron microscopy (cryo-EM) has been used to elucidate molecular structures of pigment-protein complexes, but the minor structural differences between multiple types of chlorophylls make them difficult to distinguish in cryo-EM maps. This is exemplified by inconsistencies in the assignments of chlorophyll f molecules in structures of photosystem I acclimated to far-red light (FRL-PSI). A quantitative assessment of chlorophyll substituents in cryo-EM maps was used to identify chlorophyll f-binding sites in structures of FRL-PSI from two cyanobacteria. The two cryo-EM maps provide direct evidence for chlorophyll f-binding at two and three binding sites, respectively, and three more sites in each structure exhibit strong indirect evidence for chlorophyll f binding. Common themes in chlorophyll f binding are described that clarify the current understanding of the molecular basis for FRL photoacclimation in photosystems.

Authors:: Gisriel, Christopher J.; Huang, Hao-Li; Reiss, Krystle M.; Flesher, David A.; Batista, Victor S.; Bryant, Donald A.; Brudvig, Gary W.; Wang, Jimin

Publication Date:: Fri Jan 01 00:00:00 EST 2021

Research Org.:: Yale Univ., New Haven, CT (United States)

Sponsoring Org.:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)

OSTI Identifier:: 1798902

Alternate Identifier(s):: OSTI ID: 1860613

Grant/Contract Number:: FG02-05ER15646; SC0001423; MCB-1613022

Resource Type:: Published Article

Journal Name:: BBA Advances

Additional Journal Information:: Journal Name: BBA Advances Journal Volume: 1 Journal Issue: C; Journal ID: ISSN 2667-1603

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Chlorophyll; Photosynthesis; Photosystem I; Cryo-EM; Far-red light

Citation Formats


                    Gisriel, Christopher J., Huang, Hao-Li, Reiss, Krystle M., Flesher, David A., Batista, Victor S., Bryant, Donald A., Brudvig, Gary W., and Wang, Jimin. Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light.  Netherlands: N. p., 2021. 
Web.  doi:10.1016/j.bbadva.2021.100019.

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                    Gisriel, Christopher J., Huang, Hao-Li, Reiss, Krystle M., Flesher, David A., Batista, Victor S., Bryant, Donald A., Brudvig, Gary W., & Wang, Jimin. Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light.  Netherlands.  https://doi.org/10.1016/j.bbadva.2021.100019

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                    Gisriel, Christopher J., Huang, Hao-Li, Reiss, Krystle M., Flesher, David A., Batista, Victor S., Bryant, Donald A., Brudvig, Gary W., and Wang, Jimin. Fri .  
"Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light".  Netherlands.  https://doi.org/10.1016/j.bbadva.2021.100019.

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@article{osti_1798902,

  title        = {Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light},

  author       = {Gisriel, Christopher J. and Huang, Hao-Li and Reiss, Krystle M. and Flesher, David A. and Batista, Victor S. and Bryant, Donald A. and Brudvig, Gary W. and Wang, Jimin},

  abstractNote = {Chlorophyll cofactors are vital for the metabolism of photosynthetic organisms. Cryo-electron microscopy (cryo-EM) has been used to elucidate molecular structures of pigment-protein complexes, but the minor structural differences between multiple types of chlorophylls make them difficult to distinguish in cryo-EM maps. This is exemplified by inconsistencies in the assignments of chlorophyll f molecules in structures of photosystem I acclimated to far-red light (FRL-PSI). A quantitative assessment of chlorophyll substituents in cryo-EM maps was used to identify chlorophyll f-binding sites in structures of FRL-PSI from two cyanobacteria. The two cryo-EM maps provide direct evidence for chlorophyll f-binding at two and three binding sites, respectively, and three more sites in each structure exhibit strong indirect evidence for chlorophyll f binding. Common themes in chlorophyll f binding are described that clarify the current understanding of the molecular basis for FRL photoacclimation in photosystems.},

  doi          = {10.1016/j.bbadva.2021.100019},

  journal      = {BBA Advances},

  number       = C,

  volume       = 1,

  place        = {Netherlands},

  year         = {Fri Jan 01 00:00:00 EST 2021},

  month        = {Fri Jan 01 00:00:00 EST 2021}

}

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Title: Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light

Abstract

Citation Formats

Density‐functional thermochemistry. III. The role of exact exchange journal, April 1993

Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002 journal, August 2020

Overview of the CCP 4 suite and current developments journal, March 2011

Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002 journal, January 2019

The influence of polarization functions on molecular orbital hydrogenation energies journal, January 1973

Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective journal, June 2009

Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts journal, May 2007

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An approach to computing electrostatic charges for molecules journal, April 1984

The Resolution Revolution journal, March 2014

Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light journal, August 2014

Chlorophyll Modifications and Their Spectral Extension in Oxygenic Photosynthesis journal, June 2014

The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis journal, February 2020

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Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light journal, July 2018

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Photochemistry beyond the red limit in chlorophyll f–containing photosystems journal, June 2018

VMD: Visual molecular dynamics journal, February 1996

The primary donor of far-red photosystem II: ChlD1 or PD2? journal, October 2020

Self—Consistent Molecular Orbital Methods. XII. Further Extensions of Gaussian—Type Basis Sets for Use in Molecular Orbital Studies of Organic Molecules journal, March 1972

Density‐functional thermochemistry. III. The role of exact exchange
journal, April 1993

Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002
journal, August 2020

Overview of the CCP 4 suite and current developments
journal, March 2011

Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002
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The influence of polarization functions on molecular orbital hydrogenation energies
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Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective
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Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts
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Femtosecond infrared spectroscopy of chlorophyll f-containing photosystem I
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Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light
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Atomic charges derived from semiempirical methods
journal, May 1990

Features and development of Coot
journal, March 2010

Far-red light acclimation in diverse oxygenic photosynthetic organisms
journal, June 2019

Femtosecond visible transient absorption spectroscopy of chlorophyll- f -containing photosystem II
journal, August 2020

Biosynthesis of the modified tetrapyrroles—the pigments of life
journal, April 2020

Self‐Consistent Molecular‐Orbital Methods. IX. An Extended Gaussian‐Type Basis for Molecular‐Orbital Studies of Organic Molecules
journal, January 1971

PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution
journal, June 2001

Characterization of isolated photosystem I from Halomicronema hongdechloris, a chlorophyll f-producing cyanobacterium
journal, January 2018

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

Extensive remodeling of the photosynthetic apparatus alters energy transfer among photosynthetic complexes when cyanobacteria acclimate to far-red light
journal, April 2020

Breaking the Red Limit: Efficient Trapping of Long-Wavelength Excitations in Chlorophyll-f-Containing Photosystem I
journal, January 2021

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

Opportunities and challenges for assigning cofactors in cryo-EM density maps of chlorophyll-containing proteins
journal, July 2020

MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy
journal, February 2017

Structural basis for the adaptation and function of chlorophyll f in photosystem I
journal, January 2020

Real-space refinement in PHENIX for cryo-EM and crystallography
journal, May 2018

Long‐term adaptation of Arabidopsis thaliana to far‐red light
journal, May 2021

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

Photochemistry beyond the red limit in chlorophyll f–containing photosystems
journal, June 2018

VMD: Visual molecular dynamics
journal, February 1996

The primary donor of far-red photosystem II: ChlD1 or PD2?
journal, October 2020

Self—Consistent Molecular Orbital Methods. XII. Further Extensions of Gaussian—Type Basis Sets for Use in Molecular Orbital Studies of Organic Molecules
journal, March 1972