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Title: Phycobilisome protein ApcG interacts with PSII and regulates energy transfer in Synechocystis

Abstract

Abstract Photosynthetic organisms harvest light using pigment–protein complexes. In cyanobacteria, these are water-soluble antennae known as phycobilisomes (PBSs). The light absorbed by PBS is transferred to the photosystems in the thylakoid membrane to drive photosynthesis. The energy transfer between these complexes implies that protein–protein interactions allow the association of PBS with the photosystems. However, the specific proteins involved in the interaction of PBS with the photosystems are not fully characterized. Here, we show in Synechocystis sp. PCC 6803 that the recently discovered PBS linker protein ApcG (sll1873) interacts specifically with PSII through its N-terminal region. Growth of cyanobacteria is impaired in apcG deletion strains under light-limiting conditions. Furthermore, complementation of these strains using a phospho-mimicking version of ApcG causes reduced growth under normal growth conditions. Interestingly, the interaction of ApcG with PSII is affected when a phospho-mimicking version of ApcG is used, targeting the positively charged residues interacting with the thylakoid membrane, suggesting a regulatory role mediated by phosphorylation of ApcG. Low-temperature fluorescence measurements showed decreased PSI fluorescence in apcG deletion and complementation strains. The PSI fluorescence was the lowest in the phospho-mimicking complementation strain, while the pull-down experiment showed no interaction of ApcG with PSI under any tested condition.more » Our results highlight the importance of ApcG for selectively directing energy harvested by the PBS and imply that the phosphorylation status of ApcG plays a role in regulating energy transfer from PSII to PSI.« less


Citation Formats

Espinoza-Corral, Roberto, Iwai, Masakazu, Zavřel, Tomáš, Lechno-Yossef, Sigal, Sutter, Markus, Červený, Jan, Niyogi, Krishna K., and Kerfeld, Cheryl A. Phycobilisome protein ApcG interacts with PSII and regulates energy transfer in Synechocystis. United States: N. p., 2023. Web. doi:10.1093/plphys/kiad615.
Espinoza-Corral, Roberto, Iwai, Masakazu, Zavřel, Tomáš, Lechno-Yossef, Sigal, Sutter, Markus, Červený, Jan, Niyogi, Krishna K., & Kerfeld, Cheryl A. Phycobilisome protein ApcG interacts with PSII and regulates energy transfer in Synechocystis. United States. https://doi.org/10.1093/plphys/kiad615
Espinoza-Corral, Roberto, Iwai, Masakazu, Zavřel, Tomáš, Lechno-Yossef, Sigal, Sutter, Markus, Červený, Jan, Niyogi, Krishna K., and Kerfeld, Cheryl A. Thu . "Phycobilisome protein ApcG interacts with PSII and regulates energy transfer in Synechocystis". United States. https://doi.org/10.1093/plphys/kiad615.
@article{osti_2222550,
title = {Phycobilisome protein ApcG interacts with PSII and regulates energy transfer in Synechocystis},
author = {Espinoza-Corral, Roberto and Iwai, Masakazu and Zavřel, Tomáš and Lechno-Yossef, Sigal and Sutter, Markus and Červený, Jan and Niyogi, Krishna K. and Kerfeld, Cheryl A.},
abstractNote = {Abstract Photosynthetic organisms harvest light using pigment–protein complexes. In cyanobacteria, these are water-soluble antennae known as phycobilisomes (PBSs). The light absorbed by PBS is transferred to the photosystems in the thylakoid membrane to drive photosynthesis. The energy transfer between these complexes implies that protein–protein interactions allow the association of PBS with the photosystems. However, the specific proteins involved in the interaction of PBS with the photosystems are not fully characterized. Here, we show in Synechocystis sp. PCC 6803 that the recently discovered PBS linker protein ApcG (sll1873) interacts specifically with PSII through its N-terminal region. Growth of cyanobacteria is impaired in apcG deletion strains under light-limiting conditions. Furthermore, complementation of these strains using a phospho-mimicking version of ApcG causes reduced growth under normal growth conditions. Interestingly, the interaction of ApcG with PSII is affected when a phospho-mimicking version of ApcG is used, targeting the positively charged residues interacting with the thylakoid membrane, suggesting a regulatory role mediated by phosphorylation of ApcG. Low-temperature fluorescence measurements showed decreased PSI fluorescence in apcG deletion and complementation strains. The PSI fluorescence was the lowest in the phospho-mimicking complementation strain, while the pull-down experiment showed no interaction of ApcG with PSI under any tested condition. Our results highlight the importance of ApcG for selectively directing energy harvested by the PBS and imply that the phosphorylation status of ApcG plays a role in regulating energy transfer from PSII to PSI.},
doi = {10.1093/plphys/kiad615},
journal = {Plant Physiology (Bethesda)},
number = ,
volume = ,
place = {United States},
year = {Thu Nov 16 00:00:00 EST 2023},
month = {Thu Nov 16 00:00:00 EST 2023}
}

Works referenced in this record:

Diffusion of Phycobilisomes on the Thylakoid Membranes of the Cyanobacterium Synechococcus 7942
journal, December 2001

  • Sarcina, Mary; Tobin, Mark J.; Mullineaux, Conrad W.
  • Journal of Biological Chemistry, Vol. 276, Issue 50
  • DOI: 10.1074/jbc.M107111200

A Method for DNA Extraction from the Desert Cyanobacterium Chroococcidiopsis and Its Application to Identification of ftsZ
journal, October 1998


Positive Regulation of psbA Gene Expression by cis-Encoded Antisense RNAs in Synechocystis sp. PCC 6803
journal, August 2012

  • Sakurai, Isamu; Stazic, Damir; Eisenhut, Marion
  • Plant Physiology, Vol. 160, Issue 2
  • DOI: 10.1104/pp.112.202127

Effects of Phosphorylation of β Subunits of Phycocyanins on State Transition in the Model CyanobacteriumSynechocystissp. PCC 6803
journal, August 2015

  • Chen, Zhuo; Zhan, Jiao; Chen, Ying
  • Plant and Cell Physiology, Vol. 56, Issue 10
  • DOI: 10.1093/pcp/pcv118

In situ cryo-ET structure of phycobilisome–photosystem II supercomplex from red alga
journal, September 2021


State 1-State 2 Transitions in a Unicellular Green Algae
journal, August 1983


A model for early events in the assembly pathway of cyanobacterial phycobilisomes
journal, November 1998


The structure of allophycocyanin B from Synechocystis PCC 6803 reveals the structural basis for the extreme redshift of the terminal emitter in phycobilisomes
journal, September 2014

  • Peng, Pan-Pan; Dong, Liang-Liang; Sun, Ya-Fang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10
  • DOI: 10.1107/S1399004714015776

Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena
journal, December 1993


A gene required for the regulation of photosynthetic light harvesting in the cyanobacterium Synechocystis 6803
journal, September 1999


Structure of a monomeric photosystem I core associated with iron-stress-induced-A proteins from Anabaena sp. PCC 7120
journal, February 2023


The structure of cyanobacterial phycobilisomes: a model
journal, November 1979

  • Bryant, Donald A.; Guglielmi, Gérard; de Marsac, Nicole Tandeau
  • Archives of Microbiology, Vol. 123, Issue 2
  • DOI: 10.1007/BF00446810

Core mutations of Synechococcus sp. PCC 7002 phycobilisomes: A spectroscopic study
journal, August 1992

  • Gindt, Yvonne M.; Zhou, Jianhui; Bryant, Donald A.
  • Journal of Photochemistry and Photobiology B: Biology, Vol. 15, Issue 1-2
  • DOI: 10.1016/1011-1344(92)87007-V

The state transition mechanism—simply depending on light-on and -off in Spirulina platensis
journal, November 2006

  • Li, Heng; Li, Donghui; Yang, Shuzhen
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 11
  • DOI: 10.1016/j.bbabio.2006.08.009

Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy
journal, May 2008


Reconstruction of the absorption spectrum of Synechocystis sp. PCC 6803 optical mutants from the in vivo signature of individual pigments
journal, November 2020

  • Fuente, David; Lazar, Dusan; Oliver-Villanueva, Jose Vicente
  • Photosynthesis Research, Vol. 147, Issue 1
  • DOI: 10.1007/s11120-020-00799-8

In situ structure of the red algal phycobilisome–PSII–PSI–LHC megacomplex
journal, March 2023


Quantitative insights into the cyanobacterial cell economy
journal, February 2019


Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels
journal, January 1987


Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803
journal, March 2003

  • Havaux, Michel; Guedeney, Geneviève; He, Qingfang
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1557
  • DOI: 10.1016/S0005-2728(02)00391-2

Highly accurate protein structure prediction with AlphaFold
journal, July 2021


Kinetics and dynamics for light state transition in cyanobacterium Spirulina platensis cells
journal, June 2012

  • Xu, Xiuling; Yang, Shuzhen; Xie, Jie
  • Biochemical and Biophysical Research Communications, Vol. 422, Issue 2
  • DOI: 10.1016/j.bbrc.2012.04.131

Functional in situ evaluation of photosynthesis-protecting carotenoids in mutants of the cyanobacterium Synechocystis PCC6803
journal, March 2005

  • Schäfer, Lutz; Vioque, Agustin; Sandmann, Gerhard
  • Journal of Photochemistry and Photobiology B: Biology, Vol. 78, Issue 3
  • DOI: 10.1016/j.jphotobiol.2004.11.007

ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002
journal, September 2009

  • Dong, Chunxia; Tang, Aihui; Zhao, Jindong
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 9
  • DOI: 10.1016/j.bbabio.2009.04.007

Tocopherols Protect Synechocystis sp. Strain PCC 6803 from Lipid Peroxidation
journal, June 2005

  • Maeda, Hiroshi; Sakuragi, Yumiko; Bryant, Donald A.
  • Plant Physiology, Vol. 138, Issue 3
  • DOI: 10.1104/pp.105.061135

Measurement of Chlorophyll a and Carotenoids Concentration in Cyanobacteria
journal, January 2015


Evaluation of promoters and ribosome binding sites for biotechnological applications in the unicellular cyanobacterium Synechocystis sp. PCC 6803
journal, November 2016

  • Englund, Elias; Liang, Feiyan; Lindberg, Pia
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep36640

Inactivation of Genes Encoding Plastoglobulin-Like Proteins in Synechocystis sp. PCC 6803 Leads to a Light-Sensitive Phenotype
journal, January 2010

  • Cunningham, Francis X.; Tice, Ashley B.; Pham, Christina
  • Journal of Bacteriology, Vol. 192, Issue 6
  • DOI: 10.1128/JB.01434-09

An internal antisense RNA regulates expression of the photosynthesis gene isiA
journal, April 2006

  • Duhring, U.; Axmann, I. M.; Hess, W. R.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 18
  • DOI: 10.1073/pnas.0600927103

Phycobilisome structure in the cyanobacteria Mastigocladus laminosus and Anabaena sp. PCC 7120
journal, May 1992


Light-induced excitation energy redistribution in Spirulina platensis cells: “spillover” or “mobile PBSs”?
journal, February 2004

  • Li, Donghui; Xie, Jie; Zhao, Jingquan
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1608, Issue 2-3
  • DOI: 10.1016/j.bbabio.2003.11.002

Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form
journal, December 1991


Mobility of photosynthetic complexes in thylakoid membranes
journal, November 1997

  • Mullineaux, Conrad W.; Tobin, Mark J.; Jones, Gareth R.
  • Nature, Vol. 390, Issue 6658
  • DOI: 10.1038/37157

Electron transport and light-harvesting switches in cyanobacteria
journal, January 2014


WebLogo: A Sequence Logo Generator
journal, May 2004

  • Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
  • Genome Research, Vol. 14, Issue 6, p. 1188-1190
  • DOI: 10.1101/gr.849004

Phycobilisomes Supply Excitations to Both Photosystems in a Megacomplex in Cyanobacteria
journal, November 2013


Ultrastructure of Blue-Green Algae1
journal, January 1969


Structures of a phycobilisome in light-harvesting and photoprotected states
journal, August 2022

  • Domínguez-Martín, María Agustina; Sauer, Paul V.; Kirst, Henning
  • Nature, Vol. 609, Issue 7928
  • DOI: 10.1038/s41586-022-05156-4

The Highly Abundant Chlorophyll-Protein Complex of Iron-Deficient Synechococcus sp. PCC7942 (CP43[prime]) Is Encoded by the isiA Gene
journal, November 1993

  • Burnap, R. L.; Troyan, T.; Sherman, L. A.
  • Plant Physiology, Vol. 103, Issue 3
  • DOI: 10.1104/pp.103.3.893

Molecular composition of cyanobacterial phycobilisomes.
journal, April 1977

  • de Marsac, N. T.; Cohen-bazire, G.
  • Proceedings of the National Academy of Sciences, Vol. 74, Issue 4
  • DOI: 10.1073/pnas.74.4.1635

Demonstration of phycobilisome mobility by the time- and space-correlated fluorescence imaging of a cyanobacterial cell
journal, January 2007

  • Yang, Shuzhen; Su, Zuqi; Li, Heng
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 1
  • DOI: 10.1016/j.bbabio.2006.11.012

Revisiting cyanobacterial state transitions
journal, May 2020

  • Calzadilla, Pablo I.; Kirilovsky, Diana
  • Photochemical & Photobiological Sciences, Vol. 19, Issue 5
  • DOI: 10.1039/c9pp00451c

Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane
journal, April 2019


A 12 A carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection
journal, June 2015


Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803
journal, April 1993

  • Mohamed, Abdalla; Eriksson, Jan; Osiewacz, Heinz D.
  • Molecular and General Genetics MGG, Vol. 238-238, Issue 1-2
  • DOI: 10.1007/BF00279543

Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs
journal, July 2017

  • Kerfeld, Cheryl A.; Melnicki, Matthew R.; Sutter, Markus
  • New Phytologist, Vol. 215, Issue 3
  • DOI: 10.1111/nph.14670

State transitions in cyanobacteria studied with picosecond fluorescence at room temperature
journal, October 2020

  • Bhatti, Ahmad Farhan; Choubeh, Reza Ranjbar; Kirilovsky, Diana
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 10
  • DOI: 10.1016/j.bbabio.2020.148255

Fluorescence and oxygen evolution from Chlorella pyrenoidosa
journal, December 1969


Three-dimensional Model and Characterization of the Iron Stress-induced CP43′-Photosystem I Supercomplex Isolated from the Cyanobacterium Synechocystis PCC 6803
journal, August 2001

  • Bibby, Thomas S.; Nield, Jon; Barber, James
  • Journal of Biological Chemistry, Vol. 276, Issue 46
  • DOI: 10.1074/jbc.M106541200

Increased Production of Zeaxanthin and Other Pigments by Application of Genetic Engineering Techniques to Synechocystis sp. Strain PCC 6803
journal, January 2000


Pigment-protein complexes are organized into stable microdomains in cyanobacterial thylakoids
journal, December 2019

  • Strašková, A.; Steinbach, G.; Konert, G.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 12
  • DOI: 10.1016/j.bbabio.2019.07.008

Study of O -Phosphorylation Sites in Proteins Involved in Photosynthesis-Related Processes in Synechocystis sp. Strain PCC 6803: Application of the SRM Approach
journal, November 2016


Association of Psb28 and Psb27 Proteins with PSII-PSI Supercomplexes upon Exposure of Synechocystis sp. PCC 6803 to High Light
journal, January 2017


Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803
journal, December 1989

  • Mohamed, Abdalla; Jansson, Christer
  • Plant Molecular Biology, Vol. 13, Issue 6
  • DOI: 10.1007/BF00016024

Blue light induces major changes in the gene expression profile of the cyanobacterium Synechocystis sp. PCC 6803
journal, March 2020

  • Luimstra, Veerle M.; Schuurmans, J. Merijn; Hellingwerf, Klaas J.
  • Physiologia Plantarum, Vol. 170, Issue 1
  • DOI: 10.1111/ppl.13086

Specific Glucoside Transporters Influence Septal Structure and Function in the Filamentous, Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120
journal, January 2017

  • Nieves-Morión, Mercedes; Lechno-Yossef, Sigal; López-Igual, Rocío
  • Journal of Bacteriology, Vol. 199, Issue 7
  • DOI: 10.1128/JB.00876-16

Different Regulatory Modes of Synechocystis sp. PCC 6803 in Response to Photosynthesis Inhibitory Conditions
journal, December 2021


Fluorescence Anisotropy Detection of Barrier Crossing and Ultrafast Conformational Dynamics in the S 2 State of β-Carotene
journal, September 2020

  • Gurchiek, J. K.; Rose, Justin B.; Guberman-Pfeffer, Matthew J.
  • The Journal of Physical Chemistry B, Vol. 124, Issue 41
  • DOI: 10.1021/acs.jpcb.0c06961

Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria
journal, August 2001

  • Bibby, Thomas S.; Nield, Jon; Barber, James
  • Nature, Vol. 412, Issue 6848
  • DOI: 10.1038/35089098

Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis PCC 6803
journal, April 1997

  • Olive, Jacqueline; Ajlani, Ghada; Astier, Chantal
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1319, Issue 2-3
  • DOI: 10.1016/S0005-2728(96)00168-5