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

Tros, Martijn; Bersanini, Luca; Shen, Gaozhong; Ho, Ming-Yang; van Stokkum, Ivo H. M.; Bryant, Donald A.; Croce, Roberta

doi:10.1016/j.bbabio.2020.148206

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

Abstract

The heterologous expression of the far-red absorbing chlorophyll (Chl) f in organisms that do not synthesize this pigment has been suggested as a viable solution to expand the solar spectrum that drives oxygenic photosynthesis. In this study, we investigate the functional binding of Chl f to the Photosystem I (PSI) of the cyanobacterium Synechococcus 7002, which has been engineered to express the Chl f synthase gene. By optimizing growth light conditions, one-to-four Chl f pigments were found in the complexes. By using a range of spectroscopic techniques, isolated PSI trimeric complexes were investigated to determine how the insertion of Chl f affects excitation energy transfer and trapping efficiency. The results show that the Chls f are functionally connected to the reaction center of the PSI complex and their presence does not change the overall pigment organization of the complex. Chl f substitutes Chl a (but not the Chl a red forms) while maintaining efficient energy transfer within the PSI complex. At the same time, the introduction of Chl f extends the photosynthetically active radiation of the new hybrid PSI complexes up to 750 nm, which is advantageous in far-red light enriched environments. Finally, these conclusions provide insights to engineer themore »« less

Authors:: Tros, Martijn; Bersanini, Luca; Shen, Gaozhong; Ho, Ming-Yang; van Stokkum, Ivo H. M.; Bryant, Donald A.; Croce, Roberta

Publication Date:: Sat Aug 01 00:00:00 EDT 2020

Research Org.:: Washington Univ., St. Louis, MO (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); Dutch Organization for Scientific Research; National Science Foundation (NSF)

OSTI Identifier:: 1645146

Alternate Identifier(s):: OSTI ID: 1616356; OSTI ID: 1801410

Grant/Contract Number:: SC 0001035; SC0001035; 714.018.001; MCB-1613022

Resource Type:: Published Article

Journal Name:: Biochimica et Biophysica Acta - Bioenergetics

Additional Journal Information:: Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1861 Journal Issue: 8; Journal ID: ISSN 0005-2728

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; biochemistry & molecular biology; biophysics; photosynthesis; light harvesting; pigments; time-resolved fluorescence; excitation energy transfer

Citation Formats


                    Tros, Martijn, Bersanini, Luca, Shen, Gaozhong, Ho, Ming-Yang, van Stokkum, Ivo H. M., Bryant, Donald A., and Croce, Roberta. Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002.  Netherlands: N. p., 2020. 
Web.  doi:10.1016/j.bbabio.2020.148206.

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                    Tros, Martijn, Bersanini, Luca, Shen, Gaozhong, Ho, Ming-Yang, van Stokkum, Ivo H. M., Bryant, Donald A., & Croce, Roberta. Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002.  Netherlands.  https://doi.org/10.1016/j.bbabio.2020.148206

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                    Tros, Martijn, Bersanini, Luca, Shen, Gaozhong, Ho, Ming-Yang, van Stokkum, Ivo H. M., Bryant, Donald A., and Croce, Roberta. Sat .  
"Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002".  Netherlands.  https://doi.org/10.1016/j.bbabio.2020.148206.

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@article{osti_1645146,

  title        = {Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002},

  author       = {Tros, Martijn and Bersanini, Luca and Shen, Gaozhong and Ho, Ming-Yang and van Stokkum, Ivo H. M. and Bryant, Donald A. and Croce, Roberta},

  abstractNote = {The heterologous expression of the far-red absorbing chlorophyll (Chl) f in organisms that do not synthesize this pigment has been suggested as a viable solution to expand the solar spectrum that drives oxygenic photosynthesis. In this study, we investigate the functional binding of Chl f to the Photosystem I (PSI) of the cyanobacterium Synechococcus 7002, which has been engineered to express the Chl f synthase gene. By optimizing growth light conditions, one-to-four Chl f pigments were found in the complexes. By using a range of spectroscopic techniques, isolated PSI trimeric complexes were investigated to determine how the insertion of Chl f affects excitation energy transfer and trapping efficiency. The results show that the Chls f are functionally connected to the reaction center of the PSI complex and their presence does not change the overall pigment organization of the complex. Chl f substitutes Chl a (but not the Chl a red forms) while maintaining efficient energy transfer within the PSI complex. At the same time, the introduction of Chl f extends the photosynthetically active radiation of the new hybrid PSI complexes up to 750 nm, which is advantageous in far-red light enriched environments. Finally, these conclusions provide insights to engineer the photosynthetic machinery of crops to include Chl f and therefore increase the light-harvesting capability of photosynthesis.},

  doi          = {10.1016/j.bbabio.2020.148206},

  journal      = {Biochimica et Biophysica Acta - Bioenergetics},

  number       = 8,

  volume       = 1861,

  place        = {Netherlands},

  year         = {Sat Aug 01 00:00:00 EDT 2020},

  month        = {Sat Aug 01 00:00:00 EDT 2020}

}

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

Abstract

Citation Formats

Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis journal, June 2015

Glotaran : A Java -Based Graphical User Interface for the R Package TIMP journal, January 2012

Transcription Profiling of the Model Cyanobacterium Synechococcus sp. Strain PCC 7002 by Next-Gen (SOLiD™) Sequencing of cDNA journal, January 2011

Expanding the solar spectrum used by photosynthesis journal, August 2011

Spectral expansion and antenna reduction can enhance photosynthesis for energy production journal, June 2013

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

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

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

Principles, Efficiency, and Blueprint Character of Solar-Energy Conversion in Photosynthetic Water Oxidation journal, December 2009

Energy Transfer and Trapping in Red-Chlorophyll-Free Photosystem I from Synechococcus WH 7803 journal, April 2013

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

Excited state properties of chlorophyll f in organic solvents at ambient and cryogenic temperatures journal, February 2014

Assembly of Photosystem I: I. INACTIVATION OF THE journal, March 2002

Chlorophyll d as a major pigment journal, October 1996

Light-harvesting in photosystem I journal, May 2013

Time-Resolved Fluorescence Emission Measurements of Photosystem I Particles of Various Cyanobacteria: A Unified Compartmental Model journal, July 2001

Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II journal, July 2016

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PSI–LHCI of Chlamydomonas reinhardtii : Increasing the absorption cross section without losing efficiency journal, April 2015

Elements of a dynamic systems model of canopy photosynthesis journal, June 2012

Structure of cyanobacterial Photosystem I journal, July 2005

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

Photosystem I book, January 1991

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

Efficiency of photosynthesis in a Chl d-utilizing cyanobacterium is comparable to or higher than that in Chl a-utilizing oxygenic species journal, September 2011

Extinction coefficient for red-shifted chlorophylls: Chlorophyll d and chlorophyll f journal, August 2012

Natural strategies for photosynthetic light harvesting journal, June 2014

Chlorophyll d and Acaryochloris marina: current status journal, April 2013

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

Spectroscopic Properties of Chlorophyll f journal, April 2013

Excitation Wavelength Dependence of the Fluorescence Kinetics in Photosystem I Particles from Synechocystis PCC 6803 and Synechococcus elongatus journal, December 2003

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

Functional Compartmental Modeling of the Photosystems in the Thylakoid Membrane at 77 K journal, April 2013

A Red-Shifted Chlorophyll: Fig. 1 journal, August 2010

Chlorophyll d, a Green Pigment of red Algae journal, November 1943

The siderophilic cyanobacterium Leptolyngbya sp. strain JSC-1 acclimates to iron starvation by expressing multiple isiA-family genes journal, April 2016

Discovery of Chlorophyll d in Acaryochloris marina and Chlorophyll f in a Unicellular Cyanobacterium, Strain KC1, Isolated from Lake Biwa journal, January 2014

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

Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria journal, December 2014

Trapping kinetics in isolated cyanobacterial PS I complexes journal, February 2009

Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O 2 journal, January 2012

Red antenna states of photosystem I from Synechococcus sp. PCC 7002 journal, October 2007

A viewpoint: Why chlorophyll a? journal, January 2009

Global and target analysis of time-resolved spectra journal, July 2004

Plant Photosystem I – The Most Efficient Nano-Photochemical Machine journal, March 2009

Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis
journal, June 2015

Glotaran : A Java -Based Graphical User Interface for the R Package TIMP
journal, January 2012

Transcription Profiling of the Model Cyanobacterium Synechococcus sp. Strain PCC 7002 by Next-Gen (SOLiD™) Sequencing of cDNA
journal, January 2011

Expanding the solar spectrum used by photosynthesis
journal, August 2011

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journal, June 2013

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

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

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

Principles, Efficiency, and Blueprint Character of Solar-Energy Conversion in Photosynthetic Water Oxidation
journal, December 2009

Energy Transfer and Trapping in Red-Chlorophyll-Free Photosystem I from Synechococcus WH 7803
journal, April 2013

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

Excited state properties of chlorophyll f in organic solvents at ambient and cryogenic temperatures
journal, February 2014

Assembly of Photosystem I: I. INACTIVATION OF THE
journal, March 2002

Chlorophyll d as a major pigment
journal, October 1996

Light-harvesting in photosystem I
journal, May 2013

Time-Resolved Fluorescence Emission Measurements of Photosystem I Particles of Various Cyanobacteria: A Unified Compartmental Model
journal, July 2001

Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II
journal, July 2016

Redesigning photosynthesis to sustainably meet global food and bioenergy demand
journal, June 2015

PSI–LHCI of Chlamydomonas reinhardtii : Increasing the absorption cross section without losing efficiency
journal, April 2015

Elements of a dynamic systems model of canopy photosynthesis
journal, June 2012

Structure of cyanobacterial Photosystem I
journal, July 2005

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

Photosystem I
book, January 1991

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

Efficiency of photosynthesis in a Chl d-utilizing cyanobacterium is comparable to or higher than that in Chl a-utilizing oxygenic species
journal, September 2011

Extinction coefficient for red-shifted chlorophylls: Chlorophyll d and chlorophyll f
journal, August 2012

Natural strategies for photosynthetic light harvesting
journal, June 2014

Chlorophyll d and Acaryochloris marina: current status
journal, April 2013

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

Spectroscopic Properties of Chlorophyll f
journal, April 2013

Excitation Wavelength Dependence of the Fluorescence Kinetics in Photosystem I Particles from Synechocystis PCC 6803 and Synechococcus elongatus
journal, December 2003

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

Functional Compartmental Modeling of the Photosystems in the Thylakoid Membrane at 77 K
journal, April 2013

A Red-Shifted Chlorophyll: Fig. 1
journal, August 2010

Chlorophyll d, a Green Pigment of red Algae
journal, November 1943

The siderophilic cyanobacterium Leptolyngbya sp. strain JSC-1 acclimates to iron starvation by expressing multiple isiA-family genes
journal, April 2016

Discovery of Chlorophyll d in Acaryochloris marina and Chlorophyll f in a Unicellular Cyanobacterium, Strain KC1, Isolated from Lake Biwa
journal, January 2014

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

Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria
journal, December 2014

Trapping kinetics in isolated cyanobacterial PS I complexes
journal, February 2009

Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O ₂
journal, January 2012

Red antenna states of photosystem I from Synechococcus sp. PCC 7002
journal, October 2007

A viewpoint: Why chlorophyll a?
journal, January 2009

Global and target analysis of time-resolved spectra
journal, July 2004

Plant Photosystem I – The Most Efficient Nano-Photochemical Machine
journal, March 2009