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 »
- Authors:
- Publication Date:
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 2222550
- Grant/Contract Number:
- 449B
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Plant Physiology (Bethesda)
- Additional Journal Information:
- Journal Name: Plant Physiology (Bethesda); Journal ID: ISSN 0032-0889
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
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}
}
https://doi.org/10.1093/plphys/kiad615
Works referenced in this record:
Cyanobacterial Phycobilisome Allostery as Revealed by Quantitative Mass Spectrometry
journal, March 2023
- Liu, Haijun
- Biochemistry, Vol. 62, Issue 7
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
A Method for DNA Extraction from the Desert Cyanobacterium
Chroococcidiopsis
and Its Application to Identification of
ftsZ
journal, October 1998
- Billi, Daniela; Grilli Caiola, Maria; Paolozzi, Luciano
- Applied and Environmental Microbiology, Vol. 64, Issue 10
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
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
In situ cryo-ET structure of phycobilisome–photosystem II supercomplex from red alga
journal, September 2021
- Li, Meijing; Ma, Jianfei; Li, Xueming
- eLife, Vol. 10
State 1-State 2 Transitions in a Unicellular Green Algae
journal, August 1983
- Hodges, Michael; Barber, James
- Plant Physiology, Vol. 72, Issue 4
A model for early events in the assembly pathway of cyanobacterial phycobilisomes
journal, November 1998
- Anderson, Lamont K.; Toole, Colleen M.
- Molecular Microbiology, Vol. 30, Issue 3
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
Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena
journal, December 1993
- Black, Todd A.; Cai, Yuping; Wolk, C. Peter
- Molecular Microbiology, Vol. 10, Issue 5
Regulation of the Distribution of Chlorophyll and Phycobilin-Absorbed Excitation Energy in Cyanobacteria. A Structure-Based Model for the Light State Transition
journal, October 2002
- McConnell, M. D.
- PLANT PHYSIOLOGY, Vol. 130, Issue 3
A gene required for the regulation of photosynthetic light harvesting in the cyanobacterium Synechocystis 6803
journal, September 1999
- Emlyn‐Jones, Daniel; Ashby, Mark K.; Mullineaux, Conrad W.
- Molecular Microbiology, Vol. 33, Issue 5
Structure of a monomeric photosystem I core associated with iron-stress-induced-A proteins from Anabaena sp. PCC 7120
journal, February 2023
- Nagao, Ryo; Kato, Koji; Hamaguchi, Tasuku
- Nature Communications, Vol. 14, Issue 1
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
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
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
Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy
journal, May 2008
- Folea, I. Mihaela; Zhang, Pengpeng; Aro, Eva-Mari
- FEBS Letters, Vol. 582, Issue 12
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
In situ structure of the red algal phycobilisome–PSII–PSI–LHC megacomplex
journal, March 2023
- You, Xin; Zhang, Xing; Cheng, Jing
- Nature, Vol. 616, Issue 7955
Quantitative insights into the cyanobacterial cell economy
journal, February 2019
- Zavřel, Tomáš; Faizi, Marjan; Loureiro, Cristina
- eLife, Vol. 8
Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels
journal, January 1987
- Blum, Helmut; Beier, Hildburg; Gross, Hans J.
- Electrophoresis, Vol. 8, Issue 2
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
Highly accurate protein structure prediction with AlphaFold
journal, July 2021
- Jumper, John; Evans, Richard; Pritzel, Alexander
- Nature
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
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
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
Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant
journal, July 2005
- Adir, Noam
- Photosynthesis Research, Vol. 85, Issue 1
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
Assessment of Protein Content and Phosphorylation Level in Synechocystis sp. PCC 6803 under Various Growth Conditions Using Quantitative Phosphoproteomic Analysis
journal, August 2020
- Toyoshima, Masakazu; Tokumaru, Yuma; Matsuda, Fumio
- Molecules, Vol. 25, Issue 16
Measurement of Chlorophyll a and Carotenoids Concentration in Cyanobacteria
journal, January 2015
- Zavrel, Tom�; Sinetova, Maria; Cerven�, Jan
- BIO-PROTOCOL, Vol. 5, Issue 9
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
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
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
Phycobilisome structure in the cyanobacteria Mastigocladus laminosus and Anabaena sp. PCC 7120
journal, May 1992
- Glauser, Manuel; Bryant, Donald A.; Frank, Gerhard
- European Journal of Biochemistry, Vol. 205, Issue 3
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
Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form
journal, December 1991
- Schägger, Hermann; von Jagow, Gebhard
- Analytical Biochemistry, Vol. 199, Issue 2
Mobility of photosynthetic complexes in thylakoid membranes
journal, November 1997
- Mullineaux, Conrad W.; Tobin, Mark J.; Jones, Gareth R.
- Nature, Vol. 390, Issue 6658
Electron transport and light-harvesting switches in cyanobacteria
journal, January 2014
- Mullineaux, Conrad W.
- Frontiers in Plant Science, Vol. 5
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
Phycobilisomes Supply Excitations to Both Photosystems in a Megacomplex in Cyanobacteria
journal, November 2013
- Liu, H.; Zhang, H.; Niedzwiedzki, D. M.
- Science, Vol. 342, Issue 6162
Ultrastructure of Blue-Green Algae1
journal, January 1969
- Gantt, E.; Conti, S. F.
- Journal of Bacteriology, Vol. 97, Issue 3
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
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
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
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
Revisiting cyanobacterial state transitions
journal, May 2020
- Calzadilla, Pablo I.; Kirilovsky, Diana
- Photochemical & Photobiological Sciences, Vol. 19, Issue 5
Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane
journal, April 2019
- Rast, Anna; Schaffer, Miroslava; Albert, Sahradha
- Nature Plants, Vol. 5, Issue 4
A 12 A carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection
journal, June 2015
- Leverenz, R. L.; Sutter, M.; Wilson, A.
- Science, Vol. 348, Issue 6242
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
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
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
Fluorescence and oxygen evolution from Chlorella pyrenoidosa
journal, December 1969
- Bonaventura, Celia; Myers, Jack
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 189, Issue 3
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
Increased Production of Zeaxanthin and Other Pigments by Application of Genetic Engineering Techniques to Synechocystis sp. Strain PCC 6803
journal, January 2000
- Lagarde, D.; Beuf, L.; Vermaas, W.
- Applied and Environmental Microbiology, Vol. 66, Issue 1
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
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
- Angeleri, Martina; Muth-Pawlak, Dorota; Aro, Eva-Mari
- Journal of Proteome Research, Vol. 15, Issue 12
Association of Psb28 and Psb27 Proteins with PSII-PSI Supercomplexes upon Exposure of Synechocystis sp. PCC 6803 to High Light
journal, January 2017
- Bečková, Martina; Gardian, Zdenko; Yu, Jianfeng
- Molecular Plant, Vol. 10, Issue 1
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
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
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
Different Regulatory Modes of
Synechocystis
sp. PCC 6803 in Response to Photosynthesis Inhibitory Conditions
journal, December 2021
- Cho, Sang-Hyeok; Jeong, Yujin; Hong, Seong-Joo
- mSystems, Vol. 6, Issue 6
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
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
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