Reversible inhibition and reactivation of electron transfer in photosystem I
Abstract
In photosystem I (PSI) complexes at room temperature light induced electron transfer can proceed down multiple protein-cofactor branches, and the process can be an order of magnitude faster on one branch compared to the other. One factor that might contribute to this branch asymmetry is a tryptophan amino acid at position 673 on the psaB protein. This amino acid is located between two of the pigments involved in electron transfer on the psaB protein branch. The corresponding residue on the psaA protein branch is a glycine amino acid. Microsecond time-resolved step-scan FTIR difference spectroscopy at 77 K has been used to study isolated PSI complexes from wild type and a mutant where the tryptophan residue was changed to phenylalanine. Photoaccumulated FTIR difference spectra indicate changes in the protein structure upon mutation. In the mutant we also find that the electron transfer processes is inhibited following long periods of repetitive flash illumination at room temperature. This is due to double protonation of the pigment involved in electron transfer. However, we show that we can restore electron transfer functionality by incubating the light-treated mutant PSI samples in the presence of newly added (not protonated) pigment.
- Authors:
-
- Georgia State Univ., Atlanta, GA (United States)
- Univ. of Louisville at Lafayette, LA (United States)
- Publication Date:
- Research Org.:
- Georgia State Univ., Atlanta, GA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- Contributing Org.:
- Georgia State University University of Louisiana At Lafayette
- OSTI Identifier:
- 1774547
- Grant/Contract Number:
- SC0017937
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Photosynthesis Research
- Additional Journal Information:
- Journal Volume: 145; Journal Issue: 2; Journal ID: ISSN 0166-8595
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Photosynthesis; Photosystem I; Time-resolved step-scan FTIR difference spectroscopy; Site directed mutant
Citation Formats
Agarwala, Neva, Makita, Hiroki, Luo, Lujun, Xu, Wu, and Hastings, Gary. Reversible inhibition and reactivation of electron transfer in photosystem I. United States: N. p., 2020.
Web. doi:10.1007/s11120-020-00760-9.
Agarwala, Neva, Makita, Hiroki, Luo, Lujun, Xu, Wu, & Hastings, Gary. Reversible inhibition and reactivation of electron transfer in photosystem I. United States. https://doi.org/10.1007/s11120-020-00760-9
Agarwala, Neva, Makita, Hiroki, Luo, Lujun, Xu, Wu, and Hastings, Gary. Sat .
"Reversible inhibition and reactivation of electron transfer in photosystem I". United States. https://doi.org/10.1007/s11120-020-00760-9. https://www.osti.gov/servlets/purl/1774547.
@article{osti_1774547,
title = {Reversible inhibition and reactivation of electron transfer in photosystem I},
author = {Agarwala, Neva and Makita, Hiroki and Luo, Lujun and Xu, Wu and Hastings, Gary},
abstractNote = {In photosystem I (PSI) complexes at room temperature light induced electron transfer can proceed down multiple protein-cofactor branches, and the process can be an order of magnitude faster on one branch compared to the other. One factor that might contribute to this branch asymmetry is a tryptophan amino acid at position 673 on the psaB protein. This amino acid is located between two of the pigments involved in electron transfer on the psaB protein branch. The corresponding residue on the psaA protein branch is a glycine amino acid. Microsecond time-resolved step-scan FTIR difference spectroscopy at 77 K has been used to study isolated PSI complexes from wild type and a mutant where the tryptophan residue was changed to phenylalanine. Photoaccumulated FTIR difference spectra indicate changes in the protein structure upon mutation. In the mutant we also find that the electron transfer processes is inhibited following long periods of repetitive flash illumination at room temperature. This is due to double protonation of the pigment involved in electron transfer. However, we show that we can restore electron transfer functionality by incubating the light-treated mutant PSI samples in the presence of newly added (not protonated) pigment.},
doi = {10.1007/s11120-020-00760-9},
journal = {Photosynthesis Research},
number = 2,
volume = 145,
place = {United States},
year = {Sat May 23 00:00:00 EDT 2020},
month = {Sat May 23 00:00:00 EDT 2020}
}
Works referenced in this record:
Bidirectional electron transfer in photosystem I: Replacement of the symmetry-breaking tryptophan close to the PsaB-bound phylloquinone (A1B) with a glycine residue alters the redox properties of A1B and blocks forward electron transfer at cryogenic temperatures
journal, December 2006
- Ali, Kulsam; Santabarbara, Stefano; Heathcote, Peter
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 12
Mutations in algal and cyanobacterial Photosystem I that independently affect the yield of initial charge separation in the two electron transfer cofactor branches
journal, January 2018
- Badshah, Syed Lal; Sun, Junlei; Mula, Sam
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 1
Exploring the Electron Transfer Pathways in Photosystem I by High-Time-Resolution Electron Paramagnetic Resonance: Observation of the B-Side Radical Pair P 700 + A 1B – in Whole Cells of the Deuterated Green Alga Chlamydomonas reinhardtii at Cryogenic Temperatures
journal, March 2012
- Berthold, Thomas; Donner von Gromoff, Erika; Santabarbara, Stefano
- Journal of the American Chemical Society, Vol. 134, Issue 12
FTIR Study of the Primary Electron Donor of Photosystem I (P700) Revealing Delocalization of the Charge in P700 + and Localization of the Triplet Character in 3 P700
journal, September 1999
- Breton, Jacques; Nabedryk, Eliane; Leibl, Winfried
- Biochemistry, Vol. 38, Issue 36
Electron transfer and arrangement of the redox cofactors in photosystem I
journal, February 1997
- Brettel, Klaus
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1318, Issue 3
Assignment of a kinetic component to electron transfer between iron–sulfur clusters FX and FA/B of Photosystem I
journal, November 2006
- Byrdin, Martin; Santabarbara, Stefano; Gu, Feifei
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 11
Electron–Phonon Coupling in Cyanobacterial Photosystem I
journal, August 2018
- Cherepanov, Dmitry A.; Milanovsky, Georgy E.; Gopta, Oksana A.
- The Journal of Physical Chemistry B, Vol. 122, Issue 33
Triplet states in photosystem I of spinach chloroplasts and subchloroplast particles.
journal, October 1979
- Frank, H. A.; McLean, M. B.; Sauer, K.
- Proceedings of the National Academy of Sciences, Vol. 76, Issue 10
Structure of photosystem I
journal, October 2001
- Fromme, Petra; Jordan, Patrick; Krauß, Norbert
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3
Evidence for a new early acceptor in Photosystem I of plants. An ESR investigation of reaction center triplet yield and of the reduced intermediary acceptors
journal, January 1983
- Gast, P.; Swarthoff, T.; Ebskamp, F. C. R.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 722, Issue 1
Evidence for two active branches for electron transfer in photosystem I
journal, March 2001
- Guergova-Kuras, M.; Boudreaux, B.; Joliot, A.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 8
Modification of quinone electrochemistry by the proteins in the biological electron transfer chains: examples from photosynthetic reaction centers
journal, October 2008
- Gunner, M. R.; Madeo, Jennifer; Zhu, Zhenyu
- Journal of Bioenergetics and Biomembranes, Vol. 40, Issue 5
Vibrational spectroscopy of photosystem I
journal, January 2015
- Hastings, Gary
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 1
Universality of Energy and Electron Transfer Processes in Photosystem I
journal, November 1995
- Hastings, Gary; Hoshina, Satoshi; Webber, Andrew N.
- Biochemistry, Vol. 34, Issue 47
Observation of the Reduction and Reoxidation of the Primary Electron Acceptor in Photosystem I
journal, March 1994
- Hastings, Gary; Kleinherenbrink, Frank A. M.; Lin, Su
- Biochemistry, Vol. 33, Issue 11
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
Redox Potential of Quinones in Both Electron Transfer Branches of Photosystem I
journal, September 2003
- Ishikita, Hiroshi; Knapp, Ernst-Walter
- Journal of Biological Chemistry, Vol. 278, Issue 52
Electron transfer pathways in photosystem I reaction centers
journal, July 2003
- Ivashin, Nikolaj; Larsson, Sven
- Chemical Physics Letters, Vol. 375, Issue 3-4
In Vivo Analysis of the Electron Transfer within Photosystem I: Are the Two Phylloquinones Involved? †
journal, August 1999
- Joliot, Pierre; Joliot, Anne
- Biochemistry, Vol. 38, Issue 34
Cyclic electron flow in C3 plants
journal, May 2006
- Joliot, Pierre; Joliot, Anne
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 5-6
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
Contributions of the Protein Environment to the Midpoint Potentials of the A 1 Phylloquinones and the F X Iron−Sulfur Cluster in Photosystem I †
journal, September 2007
- Karyagina, Irina; Pushkar, Yulia; Stehlik, Dietmar
- Biochemistry, Vol. 46, Issue 38
Structural Factors That Alter the Redox Potential of Quinones in Cyanobacterial and Plant Photosystem I
journal, May 2017
- Kawashima, Keisuke; Ishikita, Hiroshi
- Biochemistry, Vol. 56, Issue 24
Loss of Phylloquinone in Chlamydomonas Affects Plastoquinone Pool Size and Photosystem II Synthesis
journal, March 2007
- Lefebvre-Legendre, Linnka; Rappaport, Fabrice; Finazzi, Giovanni
- Journal of Biological Chemistry, Vol. 282, Issue 18
Spectroscopic characterization of PS I core complexes from thermophilic Synechococcus sp : Identical reoxidation kinetics of A
journal, January 1994
- Lüneberg, Jürgen; Fromme, Petra; Jekow, Petra
- FEBS Letters, Vol. 338, Issue 2
Directionality of electron transfer in cyanobacterial photosystem I at 298 and 77 K
journal, May 2015
- Makita, Hiroki; Hastings, Gary
- FEBS Letters, Vol. 589, Issue 13
Modeling electron transfer in photosystem I
journal, June 2016
- Makita, Hiroki; Hastings, Gary
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 6
Time-resolved visible and infrared absorption spectroscopy data obtained using photosystem I particles with non-native quinones incorporated into the A1 binding site
journal, June 2016
- Makita, Hiroki; Hastings, Gary
- Data in Brief, Vol. 7
Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency
journal, August 2017
- Makita, Hiroki; Hastings, Gary
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 35
Photosystem I with benzoquinone analogues incorporated into the A1 binding site
journal, January 2018
- Makita, Hiroki; Hastings, Gary
- Photosynthesis Research, Vol. 137, Issue 1
Quinones in the A1 binding site in photosystem I studied using time-resolved FTIR difference spectroscopy
journal, September 2017
- Makita, Hiroki; Rohani, Leyla; Zhao, Nan
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 9
Time-resolved visible and infrared difference spectroscopy for the study of photosystem I with different quinones incorporated into the A1 binding site
journal, March 2015
- Makita, Hiroki; Zhao, Nan; Hastings, Gary
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 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
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
Double Reduction of Plastoquinone to Plastoquinol in Photosystem 1
journal, December 2011
- McConnell, Michael D.; Cowgill, John B.; Baker, Patricia L.
- Biochemistry, Vol. 50, Issue 51
Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors
journal, March 2017
- Milanovsky, Georgy E.; Petrova, Anastasia A.; Cherepanov, Dmitry A.
- Photosynthesis Research, Vol. 133, Issue 1-3
Proton and electron transfer in bacterial reaction centers
journal, May 2000
- Okamura, M. Y.; Paddock, M. L.; Graige, M. S.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1458, Issue 1
5'-Monohydroxyphylloquinone is the Dominant Naphthoquinone of PSI in the Green Alga Chlamydomonas reinhardtii
journal, December 2011
- Ozawa, S. -i.; Kosugi, M.; Kashino, Y.
- Plant and Cell Physiology, Vol. 53, Issue 1
Spin-Correlated Radical Pairs as Quantum Sensors of Bidirectional ET Mechanisms in Photosystem I
journal, August 2019
- Poluektov, Oleg G.; Niklas, Jens; Utschig, Lisa M.
- The Journal of Physical Chemistry B, Vol. 123, Issue 35
Directionality of Electron Transfer in Type I Reaction Center Proteins: High-Frequency EPR Study of PS I with Removed Iron–Sulfur Centers
journal, April 2015
- Poluektov, Oleg G.; Utschig, Lisa M.
- The Journal of Physical Chemistry B, Vol. 119, Issue 43
Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits
journal, March 2019
- Qin, Xiaochun; Pi, Xiong; Wang, Wenda
- Nature Plants, Vol. 5, Issue 3
Calculated vibrational properties of semiquinones in the A1 binding site in photosystem I
journal, September 2019
- Rohani, Leyla; Makita, Hiroki; Levitz, Andrew
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 9
Orientation of P700, the primary electron donor of Photosystem I
journal, August 1990
- Rutherford, A. W.; Sétif, P.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1019, Issue 2
Mechanism of proton-coupled quinone reduction in Photosystem II
journal, December 2012
- Saito, K.; Rutherford, A. W.; Ishikita, H.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 3
Kinetics and Energetics of Phylloquinone Reduction in Photosystem I: Insight From Modeling of the Site Directed Mutants
journal, July 2019
- Santabarbara, Stefano; Casazza, Anna Paola
- Frontiers in Plant Science, Vol. 10
Modelling electron transfer in photosystem I: limits and perspectives
journal, March 2019
- Santabarbara, Stefano; Casazza, Anna Paola; Hastings, Gary
- Physiologia Plantarum, Vol. 166, Issue 1
Modelling of the electron transfer reactions in Photosystem I by electron tunnelling theory: The phylloquinones bound to the PsaA and the PsaB reaction centre subunits of PS I are almost isoenergetic to the iron–sulfur cluster FX
journal, July 2005
- Santabarbara, Stefano; Heathcote, Peter; Evans, Michael C. W.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1708, Issue 3
Interquinone Electron Transfer in Photosystem I As Evidenced by Altering the Hydrogen Bond Strength to the Phylloquinone(s)
journal, July 2010
- Santabarbara, Stefano; Reifschneider, Kiera; Jasaitis, Audrius
- The Journal of Physical Chemistry B, Vol. 114, Issue 28
Temperature Dependence of Forward and Reverse Electron Transfer from A 1 - , the Reduced Secondary Electron Acceptor in Photosystem I †
journal, June 1998
- Schlodder, Eberhard; Falkenberg, Klaus; Gergeleit, Martin
- Biochemistry, Vol. 37, Issue 26
Forward electron transfer from phylloquinone A1 to iron-sulfur centers in spinach photosystem I
journal, August 1993
- Setif, Pierre; Brettel, Klaus
- Biochemistry, Vol. 32, Issue 31
Assembly of Photosystem I: II. RUBREDOXIN IS REQUIRED FOR THE
journal, March 2002
- Shen, Gaozhong; Antonkine, Mikhail L.; van der Est, Art
- Journal of Biological Chemistry, Vol. 277, Issue 23
Modeling of the P700+ Charge Recombination Kinetics with Phylloquinone and Plastoquinone-9 in the A1 Site of Photosystem I
journal, December 2002
- Shinkarev, Vladimir P.; Zybailov, Boris; Vassiliev, Ilya R.
- Biophysical Journal, Vol. 83, Issue 6
Transient electron paramagnetic resonance of the triplet state of P700 in photosystem I: Evidence for triplet delocalization at room temperature
journal, May 1993
- Sieckmann, Ina; Brettel, Klaus; Bock, Christian
- Biochemistry, Vol. 32, Issue 18
A 1 Reduction in Intact Cyanobacterial Photosystem I Particles Studied by Time-Resolved Step-Scan Fourier Transform Infrared Difference Spectroscopy and Isotope Labeling †
journal, February 2005
- Sivakumar, Velautham; Wang, Ruili; Hastings, Gary
- Biochemistry, Vol. 44, Issue 6
Glotaran : A Java -Based Graphical User Interface for the R Package TIMP
journal, January 2012
- Snellenburg, Joris J.; Laptenok, Sergey P.; Seger, Ralf
- Journal of Statistical Software, Vol. 49, Issue 3
Protein–cofactor interactions in bioenergetic complexes: The role of the A1A and A1B phylloquinones in Photosystem I
journal, September 2009
- Srinivasan, Nithya; Golbeck, John H.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 9
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
FTIR Difference Spectroscopy in Combination with Isotope Labeling for Identification of the Carbonyl Modes of P700 and P700+ in Photosystem I
journal, February 2004
- Wang, Ruili; Sivakumar, Velautham; Wade Johnson, T.
- Biophysical Journal, Vol. 86, Issue 2
Electron Transfer in Cyanobacterial Photosystem I
journal, July 2003
- Xu, Wu; Chitnis, Parag; Valieva, Alfia
- Journal of Biological Chemistry, Vol. 278, Issue 30