The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis
Abstract
Phototrophic organisms are superbly adapted to different light environments but often must acclimate to challenging competition for visible light wavelengths in their niches. Some cyanobacteria overcome this challenge by expressing paralogous photosynthetic proteins and by synthesizing and incorporating ~8% chlorophyll f into their Photosystem I (PSI) complexes, enabling them to grow under far-red light (FRL). We solved the structure of FRL-acclimated PSI from the cyanobacteriumFischerella thermalisPCC 7521 by single-particle, cryo–electron microscopy to understand its structural and functional differences. Four binding sites occupied by chlorophyll f are proposed. Subtle structural changes enable FRL-adapted PSI to extend light utilization for oxygenic photosynthesis to nearly 800 nm. This structure provides a platform for understanding FRL-driven photosynthesis and illustrates the robustness of adaptive and acclimation mechanisms in nature.
- Authors:
-
[1];
[2];
[3];
[4];
[5];
[1];
[6]
- Arizona State Univ., Mesa, AZ (United States). Biodesign Ctr for Applied Structural Discovery; Arizona State Univ., Mesa, AZ (United States). School of Molecular Sciences
- Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology
- Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology; Pennsylvania State Univ., University Park, PA (United States). Intercollege Graduate Program in Plant Biology
- Arizona State Univ., Mesa, AZ (United States). Biodesign Ctr for Applied Structural Discovery
- Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology; Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemistry
- Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology; Pennsylvania State Univ., University Park, PA (United States). Intercollege Graduate Program in Plant Biology; Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
- Publication Date:
- Research Org.:
- Washington Univ., St. Louis, MO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1626049
- Grant/Contract Number:
- SC0001035
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Science Advances
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 6; Journal ID: ISSN 2375-2548
- Publisher:
- AAAS
- Country of Publication:
- United States
- Language:
- English
- Subject:
- Science & Technology - Other Topics
Citation Formats
Gisriel, Christopher, Shen, Gaozhong, Kurashov, Vasily, Ho, Ming-Yang, Zhang, Shangji, Williams, Dewight, Golbeck, John H., Fromme, Petra, and Bryant, Donald A.. The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis. United States: N. p., 2020.
Web. doi:10.1126/sciadv.aay6415.
Gisriel, Christopher, Shen, Gaozhong, Kurashov, Vasily, Ho, Ming-Yang, Zhang, Shangji, Williams, Dewight, Golbeck, John H., Fromme, Petra, & Bryant, Donald A.. The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis. United States. https://doi.org/10.1126/sciadv.aay6415
Gisriel, Christopher, Shen, Gaozhong, Kurashov, Vasily, Ho, Ming-Yang, Zhang, Shangji, Williams, Dewight, Golbeck, John H., Fromme, Petra, and Bryant, Donald A.. Sat .
"The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis". United States. https://doi.org/10.1126/sciadv.aay6415. https://www.osti.gov/servlets/purl/1626049.
@article{osti_1626049,
title = {The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis},
author = {Gisriel, Christopher and Shen, Gaozhong and Kurashov, Vasily and Ho, Ming-Yang and Zhang, Shangji and Williams, Dewight and Golbeck, John H. and Fromme, Petra and Bryant, Donald A.},
abstractNote = {Phototrophic organisms are superbly adapted to different light environments but often must acclimate to challenging competition for visible light wavelengths in their niches. Some cyanobacteria overcome this challenge by expressing paralogous photosynthetic proteins and by synthesizing and incorporating ~8% chlorophyll f into their Photosystem I (PSI) complexes, enabling them to grow under far-red light (FRL). We solved the structure of FRL-acclimated PSI from the cyanobacteriumFischerella thermalisPCC 7521 by single-particle, cryo–electron microscopy to understand its structural and functional differences. Four binding sites occupied by chlorophyll f are proposed. Subtle structural changes enable FRL-adapted PSI to extend light utilization for oxygenic photosynthesis to nearly 800 nm. This structure provides a platform for understanding FRL-driven photosynthesis and illustrates the robustness of adaptive and acclimation mechanisms in nature.},
doi = {10.1126/sciadv.aay6415},
journal = {Science Advances},
number = 6,
volume = 6,
place = {United States},
year = {2020},
month = {2}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Estimates of global cyanobacterial biomass and its distribution
journal, August 2003
- Garcia-Pichel, Ferran; Belnap, Jayne; Neuer, Susanne
- Algological Studies, Vol. 109, Issue 1
Contribution of cryptogamic covers to the global cycles of carbon and nitrogen
journal, June 2012
- Elbert, Wolfgang; Weber, Bettina; Burrows, Susannah
- Nature Geoscience, Vol. 5, Issue 7
Adaptive and acclimative responses of cyanobacteria to far-red light: Responses of cyanobacteria to far-red light
journal, August 2015
- Gan, Fei; Bryant, Donald A.
- Environmental Microbiology, Vol. 17, Issue 10
Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light
journal, August 2014
- Gan, F.; Zhang, S.; Rockwell, N. C.
- Science, Vol. 345, Issue 6202
Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria
journal, December 2014
- Gan, Fei; Shen, Gaozhong; Bryant, Donald
- Life, Vol. 5, Issue 1
Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered Photosystem I complexes
journal, February 2019
- Kurashov, Vasily; Ho, Ming-Yang; Shen, Gaozhong
- Photosynthesis Research, Vol. 141, Issue 2
Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II.Characterization of phycobiliproteins produced during acclimation to far-red light
journal, September 2016
- Ho, Ming-Yang; Gan, Fei; Shen, Gaozhong
- Photosynthesis Research, Vol. 131, Issue 2
Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II
journal, July 2016
- Ho, M. -Y.; Shen, G.; Canniffe, D. P.
- Science, Vol. 353, Issue 6302
Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002
journal, January 2019
- Shen, Gaozhong; Canniffe, Daniel P.; Ho, Ming-Yang
- Photosynthesis Research, Vol. 140, Issue 1
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
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
Structure of photosystem I
journal, October 2001
- Fromme, Petra; Jordan, Patrick; Krauß, Norbert
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3
Structure of cyanobacterial Photosystem I
journal, July 2005
- Grotjohann, Ingo; Fromme, Petra
- Photosynthesis Research, Vol. 85, Issue 1
Crystal structures of virus-like photosystem I complexes from the mesophilic cyanobacterium Synechocystis PCC 6803
journal, January 2014
- Mazor, Yuval; Nataf, Daniel; Toporik, Hila
- eLife, Vol. 3
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
Crystal Structure of Photosystem I Monomer From Synechocystis PCC 6803
journal, January 2019
- Netzer-El, Sigal Yoli; Caspy, Ido; Nelson, Nathan
- Frontiers in Plant Science, Vol. 9
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
Structure of a symmetric photosynthetic reaction center–photosystem
journal, July 2017
- Gisriel, Christopher; Sarrou, Iosifina; Ferlez, Bryan
- Science, Vol. 357, Issue 6355
JPred4: a protein secondary structure prediction server
journal, April 2015
- Drozdetskiy, Alexey; Cole, Christian; Procter, James
- Nucleic Acids Research, Vol. 43, Issue W1
Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids
journal, March 2017
- MacGregor-Chatwin, Craig; Sener, Melih; Barnett, Samuel F. H.
- The Plant Cell, Vol. 29, Issue 5
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
A niche for cyanobacteria producing chlorophyll f within a microbial mat
journal, June 2017
- Ohkubo, Satoshi; Miyashita, Hideaki
- The ISME Journal, Vol. 11, Issue 10
Widespread occurrence and unexpected diversity of red‐shifted chlorophyll producing cyanobacteria in humid subtropical forest ecosystems
journal, March 2019
- Zhang, Zhong‐Chun; Li, Zheng‐Ke; Yin, Yan‐Chao
- Environmental Microbiology, Vol. 21, Issue 4
Femtosecond Visible Transient Absorption Spectroscopy of Chlorophyll f -Containing Photosystem I
journal, January 2017
- Kaucikas, Marius; Nürnberg, Dennis; Dorlhiac, Gabriel
- Biophysical Journal, Vol. 112, Issue 2
Fourier transform visible and infrared difference spectroscopy for the study of P700 in photosystem I from Fischerella thermalis PCC 7521 cells grown under white light and far-red light: Evidence that the A–1 cofactor is chlorophyll f
journal, June 2019
- Hastings, Gary; Makita, Hiroki; Agarwala, Neva
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 6
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
journal, March 2004
- Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin
- Nature, Vol. 428, Issue 6980
Structure and assembly mechanism of plant C 2 S 2 M 2 -type PSII-LHCII supercomplex
journal, August 2017
- Su, Xiaodong; Ma, Jun; Wei, Xuepeng
- Science, Vol. 357, Issue 6353
Crystallisation, structure and function of plant light-harvesting Complex II
journal, June 2009
- Barros, Tiago; Kühlbrandt, Werner
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 6
Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I
journal, June 2019
- Suga, Michihiro; Ozawa, Shin-Ichiro; Yoshida-Motomura, Kaori
- Nature Plants, Vol. 5, Issue 6
Antenna arrangement and energy transfer pathways of a green algal photosystem-I–LHCI supercomplex
journal, March 2019
- Su, Xiaodong; Ma, Jun; Pan, Xiaowei
- Nature Plants, Vol. 5, Issue 3
Expanding the solar spectrum used by photosynthesis
journal, August 2011
- Chen, Min; Blankenship, Robert E.
- Trends in Plant Science, Vol. 16, Issue 8
Chlorophyll Modifications and Their Spectral Extension in Oxygenic Photosynthesis
journal, June 2014
- Chen, Min
- Annual Review of Biochemistry, Vol. 83, Issue 1
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
Molecular cloning and transcriptional analysis of the cpeBA operon of the cyanobacterium Pseudanabaena species PCC 7409
journal, December 1991
- Dubbs, J. M.; Bryant, D. A.
- Molecular Microbiology, Vol. 5, Issue 12
Extinction coefficient for red-shifted chlorophylls: Chlorophyll d and chlorophyll f
journal, August 2012
- Li, Yaqiong; Scales, Nicholas; Blankenship, Robert E.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8
Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris – a filamentous cyanobacterium containing chlorophyll f
journal, January 2014
- Li, Yaqiong; Lin, Yuankui; Loughlin, Patrick C.
- Frontiers in Plant Science, Vol. 5
Recruitment of a Foreign Quinone into the A 1 Site of Photosystem I : I. GENETIC AND PHYSIOLOGICAL CHARACTERIZATION OF PHYLLOQUINONE BIOSYNTHETIC PATHWAY MUTANTS IN
journal, March 2000
- Johnson, T. Wade; Shen, Gaozhong; Zybailov, Boris
- Journal of Biological Chemistry, Vol. 275, Issue 12
Automated electron microscope tomography using robust prediction of specimen movements
journal, October 2005
- Mastronarde, David N.
- Journal of Structural Biology, Vol. 152, Issue 1
Computer Visualization of Three-Dimensional Image Data Using IMOD
journal, January 1996
- Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard
- Journal of Structural Biology, Vol. 116, Issue 1
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
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
Gctf: Real-time CTF determination and correction
journal, January 2016
- Zhang, Kai
- Journal of Structural Biology, Vol. 193, Issue 1
Prevention of overfitting in cryo-EM structure determination
journal, July 2012
- Scheres, Sjors H. W.; Chen, Shaoxia
- Nature Methods, Vol. 9, Issue 9
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
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
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
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
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
Structure of the plant photosystem I supercomplex at 2.6 Å resolution
journal, March 2017
- Mazor, Yuval; Borovikova, Anna; Caspy, Ido
- Nature Plants, Vol. 3, Issue 3
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021
- Tillu, Vikas A.; Rae, James; Gao, Ya
- Nature Communications, Vol. 12, Issue 1
Insights into the physiology of Chlorella vulgaris cultivated in sweet sorghum bagasse hydrolysate for sustainable algal biomass and lipid production
journal, March 2021
- Arora, Neha; Philippidis, George P.
- Scientific Reports, Vol. 11, Issue 1
Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules.
text, January 2019
- Roth, Ronelle; Hillmer, Stefan; Funaya, Charlotta
- Apollo - University of Cambridge Repository
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
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
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
Computer Visualization of Three-Dimensional Image Data Using IMOD
journal, January 1996
- Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard
- Journal of Structural Biology, Vol. 116, Issue 1
Structure of cyanobacterial Photosystem I
journal, July 2005
- Grotjohann, Ingo; Fromme, Petra
- Photosynthesis Research, Vol. 85, Issue 1
Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II.Characterization of phycobiliproteins produced during acclimation to far-red light
journal, September 2016
- Ho, Ming-Yang; Gan, Fei; Shen, Gaozhong
- Photosynthesis Research, Vol. 131, Issue 2
Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002
journal, January 2019
- Shen, Gaozhong; Canniffe, Daniel P.; Ho, Ming-Yang
- Photosynthesis Research, Vol. 140, Issue 1
Extinction coefficient for red-shifted chlorophylls: Chlorophyll d and chlorophyll f
journal, August 2012
- Li, Yaqiong; Scales, Nicholas; Blankenship, Robert E.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8
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
Automated electron microscope tomography using robust prediction of specimen movements
journal, October 2005
- Mastronarde, David N.
- Journal of Structural Biology, Vol. 152, Issue 1
Expanding the solar spectrum used by photosynthesis
journal, August 2011
- Chen, Min; Blankenship, Robert E.
- Trends in Plant Science, Vol. 16, Issue 8
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
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
journal, March 2004
- Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin
- Nature, Vol. 428, Issue 6980
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
Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I
journal, June 2019
- Suga, Michihiro; Ozawa, Shin-Ichiro; Yoshida-Motomura, Kaori
- Nature Plants, Vol. 5, Issue 6
Femtosecond infrared spectroscopy of chlorophyll f-containing photosystem I
journal, January 2019
- Zamzam, Noura; Kaucikas, Marius; Nürnberg, Dennis J.
- Physical Chemistry Chemical Physics, Vol. 21, Issue 3
Widespread occurrence and unexpected diversity of red‐shifted chlorophyll producing cyanobacteria in humid subtropical forest ecosystems
journal, March 2019
- Zhang, Zhong‐Chun; Li, Zheng‐Ke; Yin, Yan‐Chao
- Environmental Microbiology, Vol. 21, Issue 4
Molecular cloning and transcriptional analysis of the cpeBA operon of the cyanobacterium Pseudanabaena species PCC 7409
journal, December 1991
- Dubbs, J. M.; Bryant, D. A.
- Molecular Microbiology, Vol. 5, Issue 12
Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II
journal, July 2016
- Ho, M. -Y.; Shen, G.; Canniffe, D. P.
- Science, Vol. 353, Issue 6302
The complex that conquered the land
journal, August 2017
- Croce, Roberta; van Amerongen, Herbert
- Science, Vol. 357, Issue 6353
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris – a filamentous cyanobacterium containing chlorophyll f
journal, January 2014
- Li, Yaqiong; Lin, Yuankui; Loughlin, Patrick C.
- Frontiers in Plant Science, Vol. 5