Computational Approach for Probing Redox Potential for Iron-Sulfur Clusters in Photosystem I

Ali, Fedaa; Shafaa, Medhat W.; Amin, Muhamed

doi:10.3390/biology11030362

Title: Computational Approach for Probing Redox Potential for Iron-Sulfur Clusters in Photosystem I

Journal Article · 24 February 2022 · Biology

DOI: https://doi.org/10.3390/biology11030362 · OSTI ID:1981111

^[1]; Shafaa, Medhat W. ^[2];

^[3]

Helwan University, Cairo (Egypt); University of Tennessee, Knoxville, TN (United States); Univ. of Groningen (Netherlands)
Helwan University, Cairo (Egypt)
University of Groningen (Netherlands); City University of New York (CUNY), NY (United States)

Photosystem I is a light-driven electron transfer device. Available X-ray crystal structure from Thermosynechococcus elongatus showed that electron transfer pathways consist of two nearly symmetric branches of cofactors converging at the first iron–sulfur cluster F_X, which is followed by two terminal iron–sulfur clusters F_A and F_B. Experiments have shown that F_X has lower oxidation potential than F_A and F_B, which facilitates the electron transfer reaction. Here, we use density functional theory and Multi-Conformer Continuum Electrostatics to explain the differences in the midpoint Em potentials of the F_X, F_A and F_B clusters. Our calculations show that F_X has the lowest oxidation potential compared to F_A and F_B due to strong pairwise electrostatic interactions with surrounding residues. These interactions are shown to be dominated by the bridging sulfurs and cysteine ligands, which may be attributed to the shorter average bond distances between the oxidized Fe ion and ligating sulfurs for F_X compared to F_A and F_B. Moreover, the electrostatic repulsion between the 4Fe-4S clusters and the positive potential of the backbone atoms is lowest for F_X compared to both F_A and F_B. These results agree with the experimental measurements from the redox titrations of low-temperature EPR signals and of room temperature recombination kinetics.

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Research Organization:: City University of New York (CUNY), NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0001423

OSTI ID:: 1981111

Journal Information:: Biology, Journal Name: Biology Journal Issue: 3 Vol. 11; ISSN 2079-7737

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (56)

The dielectric constant of a folded protein Gilson, Michael K.; Honig, Barry H. Biopolymers, Vol. 25, Issue 11 https://doi.org/10.1002/bip.360251106	journal	November 1986
MCCE2: Improving protein p K _a calculations with extensive side chain rotamer sampling Song, Yifan; Mao, Junjun; Gunner, M. R. Journal of Computational Chemistry https://doi.org/10.1002/jcc.21222	journal	January 2009
Force field development for cofactors in the photosystem II Zhang, Lu; Silva, Daniel-Adriano; Yan, YiJing Journal of Computational Chemistry, Vol. 33, Issue 25 https://doi.org/10.1002/jcc.23016	journal	June 2012
A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation Nicholls, Anthony; Honig, Barry Journal of Computational Chemistry, Vol. 12, Issue 4 https://doi.org/10.1002/jcc.540120405	journal	May 1991
Analysis of the electrochemistry of hemes with E _m s spanning 800 mV Zheng, Zhong; Gunner, M. R. Proteins: Structure, Function, and Bioinformatics, Vol. 75, Issue 3 https://doi.org/10.1002/prot.22282	journal	May 2009
Origin and early evolution of photosynthesis Blankenship, Robert E. Photosynthesis Research, Vol. 33, Issue 2 https://doi.org/10.1007/BF00039173	journal	August 1992
Iron–sulfur protein folds, iron–sulfur chemistry, and evolution Meyer, Jacques JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 2 https://doi.org/10.1007/s00775-007-0318-7	journal	November 2007
Combined QM/MM and Monte Carlo study for redox leveling in Mn and Fe superoxide dismutase Amin, Muhamed; Mohamed, Zainab; El-Sayed, Mohamed JBIC Journal of Biological Inorganic Chemistry, Vol. 23, Issue 2 https://doi.org/10.1007/s00775-017-1530-8	journal	December 2017
Semi-continuum electrostatic calculations of redox potentials in photosystem I Ptushenko, Vasily V.; Cherepanov, Dmitry A.; Krishtalik, Lev I. Photosynthesis Research, Vol. 97, Issue 1 https://doi.org/10.1007/s11120-008-9309-y	journal	May 2008
Light-harvesting in photosystem I Croce, Roberta; van Amerongen, Herbert Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9838-x	journal	May 2013
Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors Milanovsky, Georgy E.; Petrova, Anastasia A.; Cherepanov, Dmitry A. Photosynthesis Research, Vol. 133, Issue 1-3 https://doi.org/10.1007/s11120-017-0366-y	journal	March 2017
Effect of temperature on the photoreduction of centres A and B in Photosystem I, and the kinetics of recombination Chamorovsky, S. K.; Cammack, R. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 679, Issue 1 https://doi.org/10.1016/0005-2728(82)90266-3	journal	January 1982
Photosystem I charge separation in the absence of center A and B. III. Biochemical characterization of a reaction center particle containing P-700 and FX Golbeck, John H.; Parrett, Kevin G.; McDermott, Ann E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 893, Issue 2 https://doi.org/10.1016/0005-2728(87)90034-X	journal	September 1987
Determination of the oxidation-reduction potential of the bound iron-sulphur proteins of the primary electron acceptor complex of photosystem I in spinach chloroplasts Evans, M. C. W. FEBS Letters, Vol. 49, Issue 1 https://doi.org/10.1016/0014-5793(74)80644-7	journal	December 1974
Photosynthetic reaction centres: variations on a common structural theme? Nitschke, Wolfgang; William Rutherford, A. Trends in Biochemical Sciences, Vol. 16 https://doi.org/10.1016/0968-0004(91)90095-D	journal	January 1991
Why do thylakoid membranes from higher plants form grana stacks? Trissl, Hans-Wilhelm; Wilhelm, Christian Trends in Biochemical Sciences, Vol. 18, Issue 11 https://doi.org/10.1016/0968-0004(93)90136-B	journal	November 1993
Role of subunits in eukaryotic Photosystem I Scheller, Henrik Vibe; Jensen, Poul Erik; Haldrup, Anna Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3 https://doi.org/10.1016/S0005-2728(01)00196-7	journal	October 2001
Iron–sulfur clusters in type I reaction centers Vassiliev, Ilya R.; Antonkine, Mikhail L.; Golbeck, John H. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3 https://doi.org/10.1016/S0005-2728(01)00197-9	journal	October 2001
Electron transfer in photosystem I Brettel, Klaus; Leibl, Winfried Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3 https://doi.org/10.1016/S0005-2728(01)00202-X	journal	October 2001
Ferredoxin and flavodoxin reduction by photosystem I Sétif, Pierre Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3 https://doi.org/10.1016/S0005-2728(01)00205-5	journal	October 2001
Proteins of the cyanobacterial photosystem I Xu, Wu; Tang, Huadong; Wang, Yingchun Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3 https://doi.org/10.1016/S0005-2728(01)00208-0	journal	October 2001
The ferredoxin docking site of photosystem I Sétif, Pierre; Fischer, Nicolas; Lagoutte, Bernard Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1555, Issue 1-3 https://doi.org/10.1016/S0005-2728(02)00279-7	journal	September 2002
Purification and properties of the intact P-700 and F x-containing Photosystem I core protein Parrett, Kevin G.; Mehari, Tetemke; Warren, Patrick G. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 973, Issue 2 https://doi.org/10.1016/S0005-2728(89)80439-6	journal	February 1989
Electron transfer and arrangement of the redox cofactors in photosystem I Brettel, Klaus Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1318, Issue 3 https://doi.org/10.1016/S0005-2728(96)00112-0	journal	February 1997
A Kinetic Assessment of the Sequence of Electron Transfer from FX to FA and Further to FB in Photosystem I: The Value of the Equilibrium Constant between FX and FA Shinkarev, Vladimir P.; Vassiliev, Ilya R.; Golbeck, John H. Biophysical Journal, Vol. 78, Issue 1 https://doi.org/10.1016/S0006-3495(00)76599-4	journal	January 2000
Combining Conformational Flexibility and Continuum Electrostatics for Calculating pKas in Proteins Georgescu, Roxana E.; Alexov, Emil G.; Gunner, Marilyn R. Biophysical Journal, Vol. 83, Issue 4 https://doi.org/10.1016/S0006-3495(02)73940-4	journal	October 2002
Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties Alexov, E. G.; Gunner, M. R. Biophysical Journal, Vol. 72, Issue 5 https://doi.org/10.1016/S0006-3495(97)78851-9	journal	May 1997
PsaC Subunit of Photosystem I Is Oriented with Iron-Sulfur Cluster FB as the Immediate Electron Donor to Ferredoxin and Flavodoxin Vassiliev, Ilya R.; Jung, Yean-Sung; Yang, Fan Biophysical Journal, Vol. 74, Issue 4 https://doi.org/10.1016/S0006-3495(98)77909-3	journal	April 1998
Factors influencing the energetics of electron and proton transfers in proteins. What can be learned from calculations Gunner, M. R.; Mao, Junjun; Song, Yifan Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 8 https://doi.org/10.1016/j.bbabio.2006.06.005	journal	August 2006
The structure of genetically modified iron–sulfur cluster Fx in photosystem I as determined by X-ray absorption spectroscopy Gong, Xiao-Min; Hochman, Yehoshua; Lev, Tal Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 2 https://doi.org/10.1016/j.bbabio.2008.11.006	journal	February 2009
Protein–cofactor interactions in bioenergetic complexes: The role of the A1A and A1B phylloquinones in Photosystem I Srinivasan, Nithya; Golbeck, John H. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 9 https://doi.org/10.1016/j.bbabio.2009.04.010	journal	September 2009
Femtosecond primary charge separation in Synechocystis sp. PCC 6803 photosystem I Shelaev, Ivan V.; Gostev, Fedor E.; Mamedov, Mahir D. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 8 https://doi.org/10.1016/j.bbabio.2010.02.026	journal	August 2010
Low-potential iron-sulfur centers in photosystem I: an x-ray absorption spectroscopy study McDermott, Ann E.; Yachandra, Vittal K.; Guiles, R. D. Biochemistry, Vol. 27, Issue 11 https://doi.org/10.1021/bi00411a018	journal	May 1988
EXAFS structural study of FX, the low-potential iron-sulfur center in photosystem I McDermott, Ann E.; Yachandra, Vittal K.; Guiles, Ronald D. Biochemistry, Vol. 28, Issue 20 https://doi.org/10.1021/bi00446a013	journal	October 1989
Energetics of Quinone-Dependent Electron and Proton Transfers in Rhodobacter sphaeroides Photosynthetic Reaction Centers Zhu, Zhenyu; Gunner, M. R. Biochemistry, Vol. 44, Issue 1 https://doi.org/10.1021/bi048348k	journal	January 2005
Multiconformation Continuum Electrostatics Analysis of the Effects of a Buried Asp Introduced near Heme a in Rhodobacter sphaeroides Cytochrome c Oxidase Zhang, Jun; Gunner, M. R. Biochemistry, Vol. 49, Issue 37 https://doi.org/10.1021/bi100663u	journal	August 2010
Electron Transfer in Photosystem I Reaction Centers Follows a Linear Pathway in Which Iron−Sulfur Cluster F _B Is the Immediate Electron Donor to Soluble Ferredoxin ^† Díaz-Quintana, A.; Leibl, W.; Bottin, H. Biochemistry, Vol. 37, Issue 10 https://doi.org/10.1021/bi972469l	journal	March 1998
Calculated Protein and Proton Motions Coupled to Electron Transfer: Electron Transfer from Q _A ^- to Q _B in Bacterial Photosynthetic Reaction Centers ^† Alexov, E. G.; Gunner, M. R. Biochemistry, Vol. 38, Issue 26 https://doi.org/10.1021/bi982700a	journal	June 1999
Modeling the Effects of Mutations on the Free Energy of the First Electron Transfer from Q_A^- to Q_B in Photosynthetic Reaction Centers Alexov, E.; Miksovska, J.; Baciou, L. Biochemistry, Vol. 39, Issue 20 https://doi.org/10.1021/bi9929498	journal	April 2000
Electronic Structure Investigation and Parametrization of Biologically Relevant Iron–Sulfur Clusters Carvalho, Alexandra T. P.; Swart, Marcel Journal of Chemical Information and Modeling, Vol. 54, Issue 2 https://doi.org/10.1021/ci400718m	journal	February 2014
Synthetic Analogues of the Active Sites of Iron−Sulfur Proteins Venkateswara Rao, P.; Holm, R. H. Chemical Reviews, Vol. 104, Issue 2 https://doi.org/10.1021/cr020615+	journal	October 2003
OpenMM 4: A Reusable, Extensible, Hardware Independent Library for High Performance Molecular Simulation Eastman, Peter; Friedrichs, Mark S.; Chodera, John D. Journal of Chemical Theory and Computation, Vol. 9, Issue 1 https://doi.org/10.1021/ct300857j	journal	November 2012
Accurate Calculation of Hydration Free Energies Using Macroscopic Solvent Models Sitkoff, Doree; Sharp, Kim A.; Honig, Barry The Journal of Physical Chemistry, Vol. 98, Issue 7 https://doi.org/10.1021/j100058a043	journal	February 1994
Density Functional and Reduction Potential Calculations of Fe ₄ S ₄ Clusters Torres, Rhonda A.; Lovell, Timothy; Noodleman, Louis Journal of the American Chemical Society, Vol. 125, Issue 7 https://doi.org/10.1021/ja0211104	journal	February 2003
Extending the Applicability of the Nonlinear Poisson−Boltzmann Equation: Multiple Dielectric Constants and Multivalent Ions ^† Rocchia, W.; Alexov, E.; Honig, B. The Journal of Physical Chemistry B, Vol. 105, Issue 28 https://doi.org/10.1021/jp010454y	journal	July 2001
Electrostatic Effects on Proton Coupled Electron Transfer in Oxomanganese Complexes Inspired by the Oxygen-Evolving Complex of Photosystem II Amin, Muhamed; Vogt, Leslie; Vassiliev, Serguei The Journal of Physical Chemistry B, Vol. 117, Issue 20 https://doi.org/10.1021/jp403321b	journal	May 2013
Primary electron acceptor complex of photosystem I in spinach chloroplasts Evans, M. C. W.; Sihra, C. K.; Bolton, J. R. Nature, Vol. 256, Issue 5519 https://doi.org/10.1038/256668a0	journal	August 1975
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
Revealing the blueprint of photosynthesis Barber, J.; Andersson, B. Nature, Vol. 370, Issue 6484 https://doi.org/10.1038/370031a0	journal	July 1994
Valence bond description of antiferromagnetic coupling in transition metal dimers Noodleman, Louis The Journal of Chemical Physics, Vol. 74, Issue 10 https://doi.org/10.1063/1.440939	journal	May 1981
Ab initio effective core potentials for molecular calculations. Potentials for the transition metal atoms Sc to Hg Hay, P. Jeffrey; Wadt, Willard R. The Journal of Chemical Physics, Vol. 82, Issue 1 https://doi.org/10.1063/1.448799	journal	January 1985
Oxidation-Reduction Potentials of Bound Iron-Sulfur Proteins of Photosystem I Ke, B.; Hansen, R. E.; Beinert, H. Proceedings of the National Academy of Sciences, Vol. 70, Issue 10 https://doi.org/10.1073/pnas.70.10.2941	journal	October 1973
Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems. Liebl, U.; Mockensturm-Wilson, M.; Trost, J. T. Proceedings of the National Academy of Sciences, Vol. 90, Issue 15 https://doi.org/10.1073/pnas.90.15.7124	journal	August 1993
Spectral Signatures of Photosynthesis. I. Review of Earth Organisms Kiang, Nancy Y.; Siefert, Janet Astrobiology, Vol. 7, Issue 1 https://doi.org/10.1089/ast.2006.0105	journal	February 2007
Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis Nelson, Nathan; Junge, Wolfgang Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-092914-041942	journal	June 2015
Structure and Function of Photosystems i and ii Nelson, Nathan; Yocum, Charles F. Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105350	journal	June 2006

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59 BASIC BIOLOGICAL SCIENCES
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electron transfer
iron–sulfur cluster
photosystem I

Title: Computational Approach for Probing Redox Potential for Iron-Sulfur Clusters in Photosystem I

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