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Title: Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation

Abstract

Far-red light photoacclimation (FaRLiP) exhibited by some cyanobacteria allows these organisms to use light of the far-red region of the solar spectrum (700 to 800 nm) for photosynthesis. Part of this process includes the replacement of six photosystem I (PSI) subunits with isoforms that confer the binding of chlorophyll (Chl) f molecules that are synthesized by chlorophyll f synthase and that absorb far-red light. However, the exact sites at which Chl f molecules are bound are still challenging to determine. To aid in the identification of Chl fbinding sites, we solved the cryo-EM structure of PSI from far-red light-acclimated cells (FRLPSI) of the cyanobacterium Synechococcus sp. PCC 7335. We identified six sites that bind Chl f with high specificity, and three additional sites that are likely to bind Chl f at lower specificity. All of these binding sites are in the core antenna regions of PSI, and Chl f was not observed among the electron transport cofactors. This structural analysis also reveals both conserved and non-conserved Chl f-binding sites, the latter of which exemplify the diversity in FRL-PSI among species. We found that the FRL-PSI structure also contains a bound soluble ferredoxin, PetF1, at low occupancy, which suggests that ferredoxinmore » binds less transiently than expected according to the canonical view of ferredoxin-binding to facilitate electron transfer. We suggest that this may result from structural changes in FRL-PSI that occur specifically during FaRLiP.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [2]
  1. Yale Univ., New Haven, CT (United States)
  2. Pennsylvania State Univ., University Park, PA (United States)
  3. National Taiwan Univ., Taipei (Taiwan)
Publication Date:
Research Org.:
Yale Univ., New Haven, CT (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1860617
Grant/Contract Number:  
FG02-05ER15646
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 298; Journal Issue: 1; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; photosystem I; far-red light photoacclimation; chlorophyll f; ferredoxin; PsaF; PsaJ; photosynthesis; cyanobacteria

Citation Formats

Gisriel, Christopher J., Flesher, David A., Shen, Gaozhong, Wang, Jimin, Ho, Ming-Yang, Brudvig, Gary W., and Bryant, Donald A. Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation. United States: N. p., 2021. Web. doi:10.1016/j.jbc.2021.101408.
Gisriel, Christopher J., Flesher, David A., Shen, Gaozhong, Wang, Jimin, Ho, Ming-Yang, Brudvig, Gary W., & Bryant, Donald A. Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation. United States. https://doi.org/10.1016/j.jbc.2021.101408
Gisriel, Christopher J., Flesher, David A., Shen, Gaozhong, Wang, Jimin, Ho, Ming-Yang, Brudvig, Gary W., and Bryant, Donald A. Mon . "Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation". United States. https://doi.org/10.1016/j.jbc.2021.101408. https://www.osti.gov/servlets/purl/1860617.
@article{osti_1860617,
title = {Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation},
author = {Gisriel, Christopher J. and Flesher, David A. and Shen, Gaozhong and Wang, Jimin and Ho, Ming-Yang and Brudvig, Gary W. and Bryant, Donald A.},
abstractNote = {Far-red light photoacclimation (FaRLiP) exhibited by some cyanobacteria allows these organisms to use light of the far-red region of the solar spectrum (700 to 800 nm) for photosynthesis. Part of this process includes the replacement of six photosystem I (PSI) subunits with isoforms that confer the binding of chlorophyll (Chl) f molecules that are synthesized by chlorophyll f synthase and that absorb far-red light. However, the exact sites at which Chl f molecules are bound are still challenging to determine. To aid in the identification of Chl fbinding sites, we solved the cryo-EM structure of PSI from far-red light-acclimated cells (FRLPSI) of the cyanobacterium Synechococcus sp. PCC 7335. We identified six sites that bind Chl f with high specificity, and three additional sites that are likely to bind Chl f at lower specificity. All of these binding sites are in the core antenna regions of PSI, and Chl f was not observed among the electron transport cofactors. This structural analysis also reveals both conserved and non-conserved Chl f-binding sites, the latter of which exemplify the diversity in FRL-PSI among species. We found that the FRL-PSI structure also contains a bound soluble ferredoxin, PetF1, at low occupancy, which suggests that ferredoxin binds less transiently than expected according to the canonical view of ferredoxin-binding to facilitate electron transfer. We suggest that this may result from structural changes in FRL-PSI that occur specifically during FaRLiP.},
doi = {10.1016/j.jbc.2021.101408},
journal = {Journal of Biological Chemistry},
number = 1,
volume = 298,
place = {United States},
year = {Mon Nov 15 00:00:00 EST 2021},
month = {Mon Nov 15 00:00:00 EST 2021}
}

Works referenced in this record:

Electron transfer in photosystem I
journal, October 2001


Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II
journal, June 2018


Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335: I. Regulation of FaRLiP gene expression
journal, September 2016


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

  • Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
  • DOI: 10.1107/S0907444910045749

Interaction of Ferredoxin:NADP + Oxidoreductase with Phycobilisomes and Phycobilisome Substructures of the Cyanobacterium Synechococcus sp. Strain PCC 7002
journal, December 2003

  • Gómez-Lojero, Carlos; Pérez-Gómez, Bertha; Shen, Gaozhong
  • Biochemistry, Vol. 42, Issue 47
  • DOI: 10.1021/bi0346998

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


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

  • Guex, Nicolas; Peitsch, Manuel C.; Schwede, Torsten
  • ELECTROPHORESIS, Vol. 30, Issue S1
  • DOI: 10.1002/elps.200900140

Structural and functional insights into the tetrameric photosystem I from heterocyst-forming cyanobacteria
journal, October 2019


Complementary chromatic and far-red photoacclimations in Synechococcus ATCC 29403 (PCC 7335). I: The phycobilisomes, a proteomic approach
journal, June 2018

  • Herrera-Salgado, Priscila; Leyva-Castillo, Lourdes E.; Ríos-Castro, Emmanuel
  • Photosynthesis Research, Vol. 138, Issue 1
  • DOI: 10.1007/s11120-018-0536-6

Prevention of overfitting in cryo-EM structure determination
journal, July 2012

  • Scheres, Sjors H. W.; Chen, Shaoxia
  • Nature Methods, Vol. 9, Issue 9
  • DOI: 10.1038/nmeth.2115

Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center
journal, February 2010

  • Muller, M. G.; Slavov, C.; Luthra, R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 9
  • DOI: 10.1073/pnas.0905407107

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


Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria
journal, March 1979

  • Stanier, Roger Y.; Deruelles, Josette; Rippka, Rosmarie
  • Microbiology, Vol. 111, Issue 1, p. 1-61
  • DOI: 10.1099/00221287-111-1-1

Adaptive and acclimative responses of cyanobacteria to far-red light: Responses of cyanobacteria to far-red light
journal, August 2015


Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

  • Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
  • DOI: 10.1107/S0907444912001308

Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered Photosystem I complexes
journal, February 2019


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

  • Jordan, Patrick; Fromme, Petra; Witt, Horst Tobias
  • Nature, Vol. 411, Issue 6840
  • DOI: 10.1038/35082000

Antenna arrangement and energy-transfer pathways of PSI–LHCI from the moss Physcomitrella patens
journal, February 2021


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

  • Ho, Ming-Yang; Niedzwiedzki, Dariusz M.; MacGregor-Chatwin, Craig
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 4
  • DOI: 10.1016/j.bbabio.2019.148064

Site-directed Mutagenesis of the PsaC Subunit of Photosystem I: F
journal, August 1999

  • Fischer, Nicolas; Sétif, Pierre; Rochaix, Jean-David
  • Journal of Biological Chemistry, Vol. 274, Issue 33
  • DOI: 10.1074/jbc.274.33.23333

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

  • Zivanov, Jasenko; Nakane, Takanori; Forsberg, Björn O.
  • eLife, Vol. 7
  • DOI: 10.7554/eLife.42166

Structural basis for energy and electron transfer of the photosystem I–IsiA–flavodoxin supercomplex
journal, February 2020


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

  • Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul
  • Nature Methods, Vol. 14, Issue 4
  • DOI: 10.1038/nmeth.4193

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


Down-regulation of the PSI-F Subunit of Photosystem I (PSI) in Arabidopsis thaliana
journal, October 2000

  • Haldrup, Anna; Simpson, David John; Scheller, Henrik Vibe
  • Journal of Biological Chemistry, Vol. 275, Issue 40
  • DOI: 10.1074/jbc.M002933200

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

  • Afonine, Pavel V.; Poon, Billy K.; Read, Randy J.
  • Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 6
  • DOI: 10.1107/S2059798318006551

Evidence that chlorophyll f functions solely as an antenna pigment in far-red-light photosystem I from Fischerella thermalis PCC 7521
journal, June 2020

  • Cherepanov, Dmitry A.; Shelaev, Ivan V.; Gostev, Fedor E.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 5-6
  • DOI: 10.1016/j.bbabio.2020.148184

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

  • Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
  • Journal of Computational Chemistry, Vol. 25, Issue 13
  • DOI: 10.1002/jcc.20084

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

  • Nürnberg, Dennis J.; Morton, Jennifer; Santabarbara, Stefano
  • Science, Vol. 360, Issue 6394
  • DOI: 10.1126/science.aar8313

Unique organization of photosystem I–light-harvesting supercomplex revealed by cryo-EM from a red alga
journal, April 2018

  • Pi, Xiong; Tian, Lirong; Dai, Huai-En
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 17
  • DOI: 10.1073/pnas.1722482115

Far-red light allophycocyanin subunits play a role in chlorophyll d accumulation in far-red light
journal, November 2019


Structure of a minimal photosystem I from the green alga Dunaliella salina
journal, March 2020


The structure of photosystem I from a high-light-tolerant cyanobacteria
journal, August 2021


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

  • Tros, Martijn; Bersanini, Luca; Shen, Gaozhong
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 8
  • DOI: 10.1016/j.bbabio.2020.148206

The structure of a triple complex of plant photosystem I with ferredoxin and plastocyanin
journal, October 2020


Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits
journal, March 2019


A cyanobacterium that contains chlorophyll f - a red-absorbing photopigment
journal, July 2012


Deletion of the PsaF Polypeptide Modifies the Environment of the Redox-Active Phylloquinone (A 1 ). Evidence for Unidirectionality of Electron Transfer in Photosystem I
journal, August 1998

  • Yang, Fan; Shen, Gaozhong; Schluchter, Wendy M.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 42
  • DOI: 10.1021/jp981952i

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


Molecular interactions between photosystem I and ferredoxin: an integrated energy frustration and experimental model: MOLECULAR INTERACTIONS BETWEEN PHOTOSYSTEM I AND FERREDOXIN
journal, August 2014

  • Cashman, Derek J.; Zhu, Tuo; Simmerman, Richard F.
  • Journal of Molecular Recognition, Vol. 27, Issue 10
  • DOI: 10.1002/jmr.2384

Dynamics and energetics of cyanobacterial photosystem I:ferredoxin complexes in different redox states
journal, July 2017

  • Sétif, Pierre; Mutoh, Risa; Kurisu, Genji
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 7
  • DOI: 10.1016/j.bbabio.2017.04.001

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

  • Gisriel, Christopher; Shen, Gaozhong; Kurashov, Vasily
  • Science Advances, Vol. 6, Issue 6
  • DOI: 10.1126/sciadv.aay6415

Characterization of cyanobacterial allophycocyanins absorbing far-red light
journal, July 2020

  • Soulier, Nathan; Laremore, Tatiana N.; Bryant, Donald A.
  • Photosynthesis Research, Vol. 145, Issue 3
  • DOI: 10.1007/s11120-020-00775-2

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex
journal, April 2018


A niche for cyanobacteria producing chlorophyll f within a microbial mat
journal, June 2017


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

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I
journal, June 2019


The structure of the stress-induced photosystem I–IsiA antenna supercomplex
journal, May 2019

  • Toporik, Hila; Li, Jin; Williams, Dewight
  • Nature Structural & Molecular Biology, Vol. 26, Issue 6
  • DOI: 10.1038/s41594-019-0228-8

Ferredoxin and flavodoxin reduction by photosystem I
journal, October 2001


Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite
journal, October 2017

  • Jurrus, Elizabeth; Engel, Dave; Star, Keith
  • Protein Science, Vol. 27, Issue 1
  • DOI: 10.1002/pro.3280

Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

Structure of the plant photosystem I supercomplex at 2.6 Å resolution
journal, March 2017


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


Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis
journal, September 2018

  • Malavath, Tirupathi; Caspy, Ido; Netzer-El, Sigal Y.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 9
  • DOI: 10.1016/j.bbabio.2018.02.002

A new bioinformatics analysis tools framework at EMBL-EBI
journal, May 2010

  • Goujon, M.; McWilliam, H.; Li, W.
  • Nucleic Acids Research, Vol. 38, Issue Web Server
  • DOI: 10.1093/nar/gkq313

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


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

  • Hu, Chen; Nawrocki, Wojciech J.; Croce, Roberta
  • Plant, Cell & Environment
  • DOI: 10.1111/pce.14032

Binding of ferredoxin to algal photosystem I involves a single binding site and is composed of two thermodynamically distinct events
journal, April 2018

  • Marco, Pini; Kozuleva, Marina; Eilenberg, Haviva
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 4
  • DOI: 10.1016/j.bbabio.2018.01.001

Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light
journal, January 2021


Function and organization of photosystem I in a cyanobacterial mutant strain that lacks PsaF and PsaJ subunits.
journal, February 1994