Light-Induced Charge Separation in Photosystem I from Different Biological Species Characterized by Multifrequency Electron Paramagnetic Resonance Spectroscopy

Bindra, Jasleen K.; Malavath, Tirupathi; Teferi, Mandefro Y.; Kretzschmar, Moritz; Kern, Jan; Niklas, Jens; Utschig, Lisa M.; Poluektov, Oleg G.

doi:10.3390/ijms25158188

Light-Induced Charge Separation in Photosystem I from Different Biological Species Characterized by Multifrequency Electron Paramagnetic Resonance Spectroscopy

Journal Article · Fri Jul 26 00:00:00 EDT 2024 · International Journal of Molecular Sciences (Online)

DOI:https://doi.org/10.3390/ijms25158188· OSTI ID:2440665

Bindra, Jasleen K. ^[1]; Malavath, Tirupathi ^[1]; Teferi, Mandefro Y. ^[1]; Kretzschmar, Moritz ^[2]; Kern, Jan ^[2]; Niklas, Jens ^[1]; ^[1]; Poluektov, Oleg G. ^[1]

Argonne National Laboratory (ANL), Argonne, IL (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Photosystem I (PSI) serves as a model system for studying fundamental processes such as electron transfer (ET) and energy conversion, which are not only central to photosynthesis but also have broader implications for bioenergy production and biomimetic device design. In this study, we employed electron paramagnetic resonance (EPR) spectroscopy to investigate key light-induced charge separation steps in PSI isolated from several green algal and cyanobacterial species. Following photoexcitation, rapid sequential ET occurs through either of two quasi-symmetric branches of donor/acceptor cofactors embedded within the protein core, termed the A and B branches. Using high-frequency (130 GHz) time-resolved EPR (TR-EPR) and deuteration techniques to enhance spectral resolution, we observed that at low temperatures prokaryotic PSI exhibits reversible ET in the A branch and irreversible ET in the B branch, while PSI from eukaryotic counterparts displays either reversible ET in both branches or exclusively in the B branch. Furthermore, we observed a notable correlation between low-temperature charge separation to the terminal [4Fe-4S] clusters of PSI, termed F_A and F_B, as reflected in the measured F_A/F_B ratio. These findings enhance our understanding of the mechanistic diversity of PSI’s ET across different species and underscore the importance of experimental design in resolving these differences. Though further research is necessary to elucidate the underlying mechanisms and the evolutionary significance of these variations in PSI charge separation, this study sets the stage for future investigations into the complex interplay between protein structure, ET pathways, and the environmental adaptations of photosynthetic organisms.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: AC02-05CH11231; AC02-06CH11357

OSTI ID:: 2440665

Journal Information:: International Journal of Molecular Sciences (Online), Journal Name: International Journal of Molecular Sciences (Online) Journal Issue: 15 Vol. 25; ISSN 1422-0067

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (55)

Molecular Mechanisms of Photosynthesis Blankenship, Robert E. https://doi.org/10.1002/9780470758472	book	December 2002
Mass cultivation of algae in pure heavy water Daboll, Homer F.; Crespi, Henry L.; Katz, Joseph J. Biotechnology and Bioengineering, Vol. 4, Issue 3 https://doi.org/10.1002/bit.260040304	journal	September 1962
Photosystem I Golbeck, John H. Advances in Photosynthesis and Respiration https://doi.org/10.1007/978-1-4020-4256-0	book	January 2006
The Directionality of Electron Transport in Photosystem I Redding, Kevin; van der Est, Art Photosystem I https://doi.org/10.1007/978-1-4020-4256-0_25	book	January 2006
Pulsed EPR in 2-mm band Bresgunov, A. Yu.; Dubinskii, A. A.; Krimov, V. N. Applied Magnetic Resonance, Vol. 2, Issue 4 https://doi.org/10.1007/BF03166078	journal	December 1991
EPR spectroscopy of complex biological iron–sulfur systems Hagen, Wilfred R. JBIC Journal of Biological Inorganic Chemistry, Vol. 23, Issue 4 https://doi.org/10.1007/s00775-018-1543-y	journal	February 2018
Structure of cyanobacterial Photosystem I Grotjohann, Ingo; Fromme, Petra Photosynthesis Research, Vol. 85, Issue 1 https://doi.org/10.1007/s11120-005-1440-4	journal	July 2005
Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms Mamedov, Mahir; Nadtochenko, Victor Photosynthesis Research, Vol. 125, Issue 1-2 https://doi.org/10.1007/s11120-015-0088-y	journal	February 2015
Solar energy conversion by photosystem II: principles and structures Shevela, Dmitry; Kern, Jan F.; Govindjee, Govindjee Photosynthesis Research, Vol. 156, Issue 3 https://doi.org/10.1007/s11120-022-00991-y	journal	February 2023
Symmetry breaking in photosystem I: ultrafast optical studies of variants near the accessory chlorophylls in the A- and B-branches of electron transfer cofactors Cherepanov, Dmitry A.; Shelaev, Ivan V.; Gostev, Fedor E. Photochemical & Photobiological Sciences, Vol. 20, Issue 9 https://doi.org/10.1007/s43630-021-00094-y	journal	September 2021
The growth of algae in deuterium oxide Chorney, William; Scully, Norbert J.; Crespi, Henry L. Biochimica et Biophysica Acta, Vol. 37, Issue 2 https://doi.org/10.1016/0006-3002(60)90235-3	journal	January 1960
Electron paramagnetic resonance of spin-correlated radical pairs in photosynthetic reactions Hore, P. J.; Hunter, D. A.; McKie, C. D. Chemical Physics Letters, Vol. 137, Issue 6 https://doi.org/10.1016/0009-2614(87)80617-6	journal	July 1987
Identification of multiple components in the intermediary electron carrier complex of photosystem I Bonnerjea, J.; Evans, M. C. W. FEBS Letters, Vol. 148, Issue 2 https://doi.org/10.1016/0014-5793(82)80831-4	journal	November 1982
Iron–sulfur clusters/semiquinones in Complex I Ohnishi, Tomoko Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1364, Issue 2 https://doi.org/10.1016/S0005-2728(98)00027-9	journal	May 1998
Ultrafast Transient Absorption Studies on Photosystem I Reaction Centers from Chlamydomonas reinhardtii. 1. A New Interpretation of the Energy Trapping and Early Electron Transfer Steps in Photosystem I Müller, Marc G.; Niklas, Jens; Lubitz, Wolfgang Biophysical Journal, Vol. 85, Issue 6 https://doi.org/10.1016/S0006-3495(03)74804-8	journal	December 2003
Evidence from time resolved studies of the P700 ⁺ /A ₁ ⁻ radical pair for photosynthetic electron transfer on both the PsaA and PsaB branches of the photosystem I reaction centre Muhiuddin, I. P.; Heathcote, P.; Carter, S. FEBS Letters, Vol. 503, Issue 1 https://doi.org/10.1016/S0014-5793(01)02696-5	journal	August 2001
Structure and function of photosystem I: interaction with its soluble electron carriers and external antenna systems Fromme, Petra; Melkozernov, Alexander; Jordan, Patrick FEBS Letters, Vol. 555, Issue 1 https://doi.org/10.1016/S0014-5793(03)01124-4	journal	October 2003
EPR Spectroscopy of Iron—Sulfur Proteins Hagen, Wilfred R. Advances in Inorganic Chemistry, Vol. 38, p. 165-222 https://doi.org/10.1016/S0898-8838(08)60064-1	book	January 1992
Application of EPR Spectroscopy to the Structural and Functional Study of Iron-Sulfur Proteins Guigliarelli, Bruno; Bertrand, Patrick Advances in Inorganic Chemistry, p. 421 - 497 https://doi.org/10.1016/S0898-8838(08)60084-7	book	January 1999
EasySpin, a comprehensive software package for spectral simulation and analysis in EPR Stoll, Stefan; Schweiger, Arthur Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55 https://doi.org/10.1016/j.jmr.2005.08.013	journal	January 2006
Native-like Photosystem II Superstructure at 2.44 Å Resolution through Detergent Extraction from the Protein Crystal Hellmich, Julia; Bommer, Martin; Burkhardt, Anja Structure, Vol. 22, Issue 11 https://doi.org/10.1016/j.str.2014.09.007	journal	November 2014
Quantum Sensing of Electron Transfer Pathways in Natural Photosynthesis Using Time-Resolved High-Field Electron Paramagnetic Resonance/Electron–Nuclear Double Resonance Spectroscopy Poluektov, Oleg G.; Utschig, Lisa M. The Journal of Physical Chemistry B, Vol. 125, Issue 16 https://doi.org/10.1021/acs.jpcb.1c00946	journal	April 2021
Coherences of Photoinduced Electron Spin Qubit Pair States in Photosystem I Bindra, Jasleen K.; Niklas, Jens; Jeong, Yeonjun The Journal of Physical Chemistry B, Vol. 127, Issue 47 https://doi.org/10.1021/acs.jpcb.3c06658	journal	November 2023
Directionality of Electron Transfer in Type I Reaction Center Proteins: High-Frequency EPR Study of PS I with Removed Iron–Sulfur Centers Poluektov, Oleg G.; Utschig, Lisa M. The Journal of Physical Chemistry B, Vol. 119, Issue 43 https://doi.org/10.1021/acs.jpcb.5b04063	journal	April 2015
Spin-Correlated Radical Pairs as Quantum Sensors of Bidirectional ET Mechanisms in Photosystem I Poluektov, Oleg G.; Niklas, Jens; Utschig, Lisa M. The Journal of Physical Chemistry B, Vol. 123, Issue 35 https://doi.org/10.1021/acs.jpcb.9b06636	journal	August 2019
Characterization of a photosystem I core containing P700 and intermediate electron acceptor A1 Warren, Patrick V.; Parrett, Kevin G.; Warden, Joseph T. Biochemistry, Vol. 29, Issue 28 https://doi.org/10.1021/bi00480a001	journal	July 1990
Bidirectional Electron Transfer in Photosystem I: Determination of Two Distances between P ₇₀₀ ⁺ and A ₁ ^- in Spin-Correlated Radical Pairs ^† Santabarbara, Stefano; Kuprov, Ilya; Fairclough, Wendy V. Biochemistry, Vol. 44, Issue 6 https://doi.org/10.1021/bi048445d	journal	February 2005
Analysis of the Spin-Polarized Electron Spin Echo of the [P ₇₀₀ ⁺ A ₁ ^- ] Radical Pair of Photosystem I Indicates That Both Reaction Center Subunits Are Competent in Electron Transfer in Cyanobacteria, Green Algae, and Higher Plants ^† Santabarbara, Stefano; Kuprov, Ilya; Hore, P. J. Biochemistry, Vol. 45, Issue 23 https://doi.org/10.1021/bi060330h	journal	June 2006
Discovery of Native Metal Ion Sites Located on the Ferredoxin Docking Side of Photosystem I ^† Utschig, Lisa M.; Chen, Lin X.; Poluektov, Oleg G. Biochemistry, Vol. 47, Issue 12 https://doi.org/10.1021/bi800038d	journal	March 2008
Temperature Dependence of Forward and Reverse Electron Transfer from A ₁ ^- , the Reduced Secondary Electron Acceptor in Photosystem I ^† Schlodder, Eberhard; Falkenberg, Klaus; Gergeleit, Martin Biochemistry, Vol. 37, Issue 26 https://doi.org/10.1021/bi973182r	journal	June 1998
In Vivo Analysis of the Electron Transfer within Photosystem I: Are the Two Phylloquinones Involved? ^† Joliot, Pierre; Joliot, Anne Biochemistry, Vol. 38, Issue 34 https://doi.org/10.1021/bi990857c	journal	August 1999
Spin-polarized electron paramagnetic resonance spectra of radical pairs in micelles: observation of electron spin-spin interactions Closs, Gerhard L.; Forbes, Malcolm D. E.; Norris, James R. The Journal of Physical Chemistry, Vol. 91, Issue 13 https://doi.org/10.1021/j100297a026	journal	June 1987
Electron Transfer Pathways and Protein Response to Charge Separation in Photosynthetic Reaction Centers: Time-Resolved High-Field ENDOR of the Spin-Correlated Radical Pair P ₈₆₅ ⁺ Q _A ^- Poluektov, Oleg G.; Utschig, Lisa M.; Dubinskij, Alexander A. Journal of the American Chemical Society, Vol. 127, Issue 11 https://doi.org/10.1021/ja043063g	journal	March 2005
Bidirectional Electron Transfer in Photosystem I: Direct Evidence from High-Frequency Time-Resolved EPR Spectroscopy Poluektov, Oleg G.; Paschenko, Sergei V.; Utschig, Lisa M. Journal of the American Chemical Society, Vol. 127, Issue 34 https://doi.org/10.1021/ja053315t	journal	August 2005
Photogenerated Spin-Correlated Radical Pairs: From Photosynthetic Energy Transduction to Quantum Information Science Harvey, Samantha M.; Wasielewski, Michael R. Journal of the American Chemical Society, Vol. 143, Issue 38 https://doi.org/10.1021/jacs.1c07706	journal	September 2021
A Structural Model for the Charge Separated State in Photosystem I from the Orientation of the Magnetic Interaction Tensors Zech, Stephan G.; Hofbauer, Wulf; Kamlowski, Andreas The Journal of Physical Chemistry B, Vol. 104, Issue 41 https://doi.org/10.1021/jp002125w	journal	October 2000
Electronic Structure of the P₇₀₀ Special Pair from High-Frequency Electron Paramagnetic Resonance Spectroscopy Poluektov, Oleg G.; Utschig, Lisa M.; Schlesselman, Sandra L. The Journal of Physical Chemistry B, Vol. 106, Issue 35 https://doi.org/10.1021/jp021465+	journal	August 2002
Interquinone Electron Transfer in Photosystem I As Evidenced by Altering the Hydrogen Bond Strength to the Phylloquinone(s) Santabarbara, Stefano; Reifschneider, Kiera; Jasaitis, Audrius The Journal of Physical Chemistry B, Vol. 114, Issue 28 https://doi.org/10.1021/jp1038656	journal	July 2010
Directionality of Electron-Transfer Reactions in Photosystem I of Prokaryotes: Universality of the Bidirectional Electron-Transfer Model Santabarbara, Stefano; Kuprov, Ilya; Poluektov, Oleg The Journal of Physical Chemistry B, Vol. 114, Issue 46 https://doi.org/10.1021/jp1044018	journal	November 2010
Orientation Resolving Dipolar High-Field EPR Spectroscopy on Disordered Solids: II. Structure of Spin-Correlated Radical Pairs in Photosystem I Savitsky, A.; Niklas, J.; Golbeck, J. H. The Journal of Physical Chemistry B, Vol. 117, Issue 38 https://doi.org/10.1021/jp401573z	journal	April 2013
Time-Resolved X-, K-, and W-Band EPR of the Radical Pair State of Photosystem I in Comparison with in Bacterial Reaction Centers van der Est, A.; Prisner, T.; Bittl, R. The Journal of Physical Chemistry B, Vol. 101, Issue 8 https://doi.org/10.1021/jp9622086	journal	February 1997
Culture of Algae and other Micro-organisms in Deuterium oxide Crespi, Henry L.; Archer, Sylvia M.; Katz, Joseph J. Nature, Vol. 184, Issue 4687 https://doi.org/10.1038/184729a0	journal	August 1959
Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution Jordan, Patrick; Fromme, Petra; Witt, Horst Tobias Nature, Vol. 411, Issue 6840 https://doi.org/10.1038/35082000	journal	June 2001
Structure of the plant photosystem I supercomplex at 2.6 Å resolution Mazor, Yuval; Borovikova, Anna; Caspy, Ido Nature Plants, Vol. 3, Issue 3 https://doi.org/10.1038/nplants.2017.14	journal	March 2017
Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits Qin, Xiaochun; Pi, Xiong; Wang, Wenda Nature Plants, Vol. 5, Issue 3 https://doi.org/10.1038/s41477-019-0379-y	journal	March 2019
Antenna arrangement and energy transfer pathways of a green algal photosystem-I–LHCI supercomplex Su, Xiaodong; Ma, Jun; Pan, Xiaowei Nature Plants, Vol. 5, Issue 3 https://doi.org/10.1038/s41477-019-0380-5	journal	March 2019
Primary processes in photosynthesis: what do we learn from high-field EPR spectroscopy? Möbius, Klaus Chemical Society Reviews, Vol. 29, Issue 2 https://doi.org/10.1039/a706426h	journal	January 2000
Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center Muller, M. G.; Slavov, C.; Luthra, R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 9 https://doi.org/10.1073/pnas.0905407107	journal	February 2010
Magnetoreception in birds Wiltschko, Roswitha; Wiltschko, Wolfgang Journal of The Royal Society Interface, Vol. 16, Issue 158 https://doi.org/10.1098/rsif.2019.0295	journal	September 2019
Bidirectional Electron Transfer in the Reaction Centre of Photosystem I Santabarbara, Stefano; Galuppini, Luca; Casazza, Anna Paola Journal of Integrative Plant Biology, Vol. 52, Issue 8 https://doi.org/10.1111/j.1744-7909.2010.00977.x	journal	June 2010
Cultivation of Microorganisms in Heavy Water* Crespi, Henry L.; Conrad, Sylvia M.; Uphaus, Robert A. Annals of the New York Academy of Sciences, Vol. 84, Issue 16 https://doi.org/10.1111/j.1749-6632.1960.tb39098.x	journal	November 1960
The Radical-Pair Mechanism of Magnetoreception Hore, P. J.; Mouritsen, Henrik Annual Review of Biophysics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-biophys-032116-094545	journal	July 2016
P HOTOSYSTEM I: Function and Physiology Chitnis, Parag R. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev.arplant.52.1.593	journal	June 2001
Shedding Light on Primary Donors in Photosynthetic Reaction Centers Gorka, Michael; Baldansuren, Amgalanbaatar; Malnati, Amanda Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.735666	journal	October 2021
Structural Diversity of Photosystem I and Its Light-Harvesting System in Eukaryotic Algae and Plants Bai, Tianyu; Guo, Lin; Xu, Mingyu Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.781035	journal	November 2021

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Light-Induced Charge Separation in Photosystem I from Different Biological Species Characterized by Multifrequency Electron Paramagnetic Resonance Spectroscopy

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