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Title: Changes in supramolecular organization of cyanobacterial thylakoid membrane complexes in response to far-red light photoacclimation

Journal Article · · Science Advances
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [3]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [7]; ORCiD logo [9]; ORCiD logo [3]
  1. Univ. of Sheffield (United Kingdom); Diamond Light Source (United Kingdom); The Pennsylvania State University
  2. Imperial College, London (United Kingdom); Freie Univ. Berlin (Germany)
  3. Univ. of Sheffield (United Kingdom)
  4. Pennsylvania State Univ., University Park, PA (United States); National Taiwan Univ., Taipei (Taiwan)
  5. Pennsylvania State Univ., University Park, PA (United States
  6. Arizona State Univ., Tempe, AZ (United States); Yale Univ., New Haven, CT (United States)
  7. Imperial College, London (United Kingdom)
  8. Freie Univ. Berlin (Germany)
  9. Pennsylvania State Univ., University Park, PA (United States)

Cyanobacteria are ubiquitous in nature and have developed numerous strategies that allow them to live in a diverse range of environments. Certain cyanobacteria synthesize chlorophylls d and f to acclimate to niches enriched in far-red light (FRL) and incorporate paralogous photosynthetic proteins into their photosynthetic apparatus in a process called FRL-induced photoacclimation (FaRLiP). We characterized the macromolecular changes involved in FRL-driven photosynthesis and used atomic force microscopy to examine the supramolecular organization of photosystem I associated with FaRLiP in three cyanobacterial species. Mass spectrometry showed the changes in the proteome of Chroococcidiopsis thermalis PCC 7203 that accompany FaRLiP. Fluorescence lifetime imaging microscopy and electron microscopy reveal an altered cellular distribution of photosystem complexes and illustrate the cell-to-cell variability of the FaRLiP response.

Research Organization:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Organization:
H2020 European Research Council; U.S. National Science Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0001035
OSTI ID:
1871338
Journal Information:
Science Advances, Journal Name: Science Advances Journal Issue: 6 Vol. 8; ISSN 2375-2548
Publisher:
AAASCopyright Statement
Country of Publication:
United States
Language:
English

References (86)

Plant and algal chlorophyll synthases function in Synechocystis and interact with the YidC/Alb3 membrane insertase journal September 2018
Leptolyngbya CCM 4, a cyanobacterium with far-red photoacclimation from Cuatro Ciénegas Basin, México journal January 2018
Photosynthetic Apparatus of Antenna-reaction Centres Supercomplexes in Oxyphotobacteria: Insight through Significance of Pcb/IsiA Proteins journal November 2005
Chlorophyll d and Acaryochloris marina: current status journal April 2013
Toward the complete proteome of Synechocystis sp. PCC 6803 journal April 2015
The siderophilic cyanobacterium Leptolyngbya sp. strain JSC-1 acclimates to iron starvation by expressing multiple isiA-family genes journal April 2016
Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II.Characterization of phycobiliproteins produced during acclimation to far-red light journal September 2016
Subcellular pigment distribution is altered under far-red light acclimation in cyanobacteria that contain chlorophyll f journal September 2017
Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002 journal January 2019
Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered Photosystem I complexes journal February 2019
Far-red light allophycocyanin subunits play a role in chlorophyll d accumulation in far-red light journal November 2019
Characterization of cyanobacterial allophycocyanins absorbing far-red light journal July 2020
The structural basis of far-red light absorbance by allophycocyanins journal October 2020
PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803 journal December 1993
[3] Culturing methods for cyanobacteria book January 1988
Characterization of red-shifted phycobilisomes isolated from the chlorophyll f -containing cyanobacterium Halomicronema hongdechloris journal January 2016
Far-red light photoacclimation: Chromophorylation of FR induced α- and β-subunits of allophycocyanin from Chroococcidiopsis thermalis sp. PCC7203 journal September 2016
Cryo-EM structure of a tetrameric cyanobacterial photosystem I complex reveals novel subunit interactions journal September 2016
Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis journal September 2018
Extensive remodeling of the photosynthetic apparatus alters energy transfer among photosynthetic complexes when cyanobacteria acclimate to far-red light journal April 2020
Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002 journal August 2020
Small monomeric and highly stable near-infrared fluorescent markers derived from the thermophilic phycobiliprotein, ApcF2 journal October 2017
A cyanobacterium that contains chlorophyll f - a red-absorbing photopigment journal July 2012
Chlorophyll f and chlorophyll d are produced in the cyanobacterium Chlorogloeopsis fritschii when cultured under natural light and near-infrared radiation journal August 2014
Dissecting the Native Architecture and Dynamics of Cyanobacterial Photosynthetic Machinery journal November 2017
Light and photosynthesis in aquatic ecosystems book December 1993
Biosynthesis of Chlorophyll a in a Purple Bacterial Phototroph and Assembly into a Plant Chlorophyll–Protein Complex journal May 2016
Function of Chlorophyll d in Reaction Centers of Photosystems I and II of the Oxygenic Photosynthesis of Acaryochloris marina journal October 2007
Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution journal June 2001
Chlorophyll d as a major pigment journal October 1996
A niche for cyanobacteria containing chlorophyll d journal February 2005
Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium journal February 2015
A niche for cyanobacteria producing chlorophyll f within a microbial mat journal June 2017
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å journal April 2011
Global quantification of mammalian gene expression control journal May 2011
Mass-spectrometry-based draft of the human proteome journal May 2014
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification journal November 2008
The Perseus computational platform for comprehensive analysis of (prote)omics data journal June 2016
Tricine–SDS-PAGE journal May 2006
Global distribution of a chlorophyll f cyanobacterial marker journal May 2020
Structure of a cyanobacterial photosystem I tetramer revealed by cryo-electron microscopy journal October 2019
Structural basis for the adaptation and function of chlorophyll f in photosystem I journal January 2020
X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex journal April 2018
Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane journal April 2019
Membrane organization of photosystem I complexes in the most abundant phototroph on Earth journal July 2019
Structural and functional insights into the tetrameric photosystem I from heterocyst-forming cyanobacteria journal October 2019
Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria journal December 2019
Distinct structural modulation of photosystem I and lipid environment stabilizes its tetrameric assembly journal March 2020
Chlorophyll f synthesis by a super-rogue photosystem II complex journal March 2020
Structural variability, coordination and adaptation of a native photosynthetic machinery journal July 2020
Far-red absorption and light-use efficiency trade-offs in chlorophyll f photosynthesis journal July 2020
Structural basis of energy transfer in Porphyridium purpureum phycobilisome journal February 2020
Opportunities and challenges for assigning cofactors in cryo-EM density maps of chlorophyll-containing proteins journal July 2020
Chromophorylation (in Escherichia coli) of allophycocyanin B subunits from far-red light acclimated Chroococcidiopsis thermalis sp. PCC7203 journal January 2017
The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina journal January 2005
Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing journal December 2012
Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus journal May 2013
Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria journal February 2014
Femtosecond visible transient absorption spectroscopy of chlorophyll- f -containing photosystem II journal August 2020
Monomeric and trimeric forms of photosystem I reaction center of Mastigocladus laminosus: crystallization and preliminary characterization. journal June 1991
Absolute Quantification of Proteins by LCMS E : A Virtue of Parallel ms Acquisition journal October 2005
Novel Supercomplex Organization of Photosystem I in Anabaena and Cyanophora paradoxa journal November 2010
Photosynthetic Pigment Localization and Thylakoid Membrane Morphology Are Altered in Synechocystis 6803 Phycobilisome Mutants journal February 2012
Proteome Mapping of a Cyanobacterium Reveals Distinct Compartment Organization and Cell-Dispersed Metabolism journal October 2019
Characterization and Evolution of Tetrameric Photosystem I from the Thermophilic Cyanobacterium Chroococcidiopsis sp TS-821 journal March 2014
Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids journal March 2017
Adaptive and acclimative responses of cyanobacteria to far-red light: Responses of cyanobacteria to far-red light journal August 2015
Widespread occurrence and unexpected diversity of red‐shifted chlorophyll producing cyanobacteria in humid subtropical forest ecosystems journal March 2019
Life in the dark: far‐red absorbing cyanobacteria extend photic zones deep into terrestrial caves journal August 2019
Characterization of psal and psaL Mutants of Synechococcus sp. Strain PCC 7002: A New Model for State Transitions in Cyanobacteria journal July 1996
Chlorophyll f distribution and dynamics in cyanobacterial beachrock biofilms journal September 2016
Branching and intercellular communication in the Section V cyanobacterium M astigocladus laminosus , a complex multicellular prokaryote: Intercellular communication in Mastigocladus laminosus journal January 2014
Developmental acclimation of the thylakoid proteome to light intensity in Arabidopsis journal November 2020
The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis journal February 2020
A Red-Shifted Chlorophyll: Fig. 1 journal August 2010
Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light journal August 2014
Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II journal July 2016
Photochemistry beyond the red limit in chlorophyll f–containing photosystems journal June 2018
Estimates of global cyanobacterial biomass and its distribution journal August 2003
Polyphasic Characterization of a Thermotolerant Siderophilic Filamentous Cyanobacterium That Produces Intracellular Iron Deposits journal August 2010
Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptative proteomic shifts under different light conditions journal March 2019
Visualization of Cell Complexity in the Filamentous Cyanobacterium Mastigocladus laminosus by Transmission Electron Microscopy (TEM) journal January 2014
RfpA, RfpB, and RfpC are the Master Control Elements of Far-Red Light Photoacclimation (FaRLiP) journal November 2015
Global Transcriptional Profiling of the Cyanobacterium Chlorogloeopsis fritschii PCC 9212 in Far-Red Light: Insights Into the Regulation of Chlorophyll d Synthesis journal March 2019
Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria journal December 2014
Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptative proteomic shifts under different light conditions collection January 2019