CALCULATING REDOX POTENTIAL FOR IRON
SULFUR CLUSTERS IN
PHOTOSYSTEM I
Fedaa Ali1 ; Medhat W.Shafaa1 and Muhamed Amin2,3*
†Medical biophysics division, Department of Physics, Faculty of
Science, Helwan university, Cairo, Egypt.
‡ a Department of Sciences, University College Groningen, University of
Groningen, Hoendiepskade 23/24, 9718 BG Groningen, Netherlands
Universiteit Groningen Biomolecular Sciences and Biotechnology
Institute, University of Groningen, Groningen, Netherlands
*E-mail: m.a.a.amin@rug.nl
ABSTRACT.
Photosystem I is an electron transfer protein complex. Available Xray
crystal structures showed that electron transfer pathways consist of
two nearly symmetric branches of co-factors converging at the first iron
sulfur cluster FX, which is followed by two terminal iron sulfur clusters
FA and FB. In the present study, redox potentials of three iron sulfur
clusters in Photosystem I are calculated by means continuum electrostatic
methods. Structures of three clusters surrounded by ~ 10 A° nearby
amino acids, are extracted from the X-ray crystal structure for
Cyanobacterial photosystem I (PDB ID: 1JB0) and the midpoint
potentials Ems are determined by MCCE model. Our calculations show
that the first iron-sulfur cluster Fx has the lowest oxidation potential
among three iron-sulfur clusters, while FA is shown to has the highest
oxidation potential which agree with the experimental ordering.
INTRODUCTION
The photosynthesis process is the process that guarantees the
existence of our life. In photosynthesis, the solar energy is harvested by
pigments associated with the photosynthetic machinery and stored as
energy rich compounds according to the fundamental equation below,
→
Initial energy conversion reactions take place in special protein
complexes known as Type I and Type II reaction centers1. Which are
classified according to the type of terminal electron acceptor used, ironsulfur
clusters (Fe-S) and mobile quinine for type I and type II,
respectively. Type I reaction center found in green sulfur bacteria,
heliobacteria, and as photosystem I (PS I) in chloroplasts and
Egypt. J. of Appl. Sci., 35 (9) 2020 115-125
cyanobacteria. While Type II reaction center exists in purple bacteria,
chloroflexus, and as photosystem II in chloroplasts and cyanobacteria 2–6.
PS I is an electron transfer machine which converts the solar
energy to a reducing power with a quantum yield close to 1.07–9. Upon
excitation of the primary donor in PS I, charge separation will be induced
and electron will transfer through Electron Transfer Chains (ETCs),
terminated by iron-sulfur Fe-S clusters, to ferredoxin which reduce
NADP+ to NADPH10–13. X-ray crystal structure, 2.5 Å resolution14, of a
monomeric cyanobacterial PS I revealed 12 protein domains, which noncovalently
bound ~90 chlorophyll a molecules ( Chl a), 2
phylloquinones, 20 β-carotene, 2 lipids, and 3 [4Fe-4S] clusters (FX, FA
and FB)13–15, (Fig. 1.A). In PS I, there are three main, highly conserved
domains PsaA, PsaB, and PsaC proteins, Fig. 1(B, left). The first two
subunits form the heterodimeric core, which comprises most of the
antenna pigments and the redox co-factors employed in Electron transfer
chains ETCs16–18.While, PsaC comprises the two terminal Fe-S clusters
FA and FB, and with PsaE and PsaD subunits it form the stromal hump
providing docking site for ferredoxin10,19. ETCs in PS I consists of two
nearly symmetric branches of co-factors coordinated by the PsaA/PsaB
core protein and converging at the first Fe-S cluster FX, which is
followed by the two terminal Fe-S clusters FA and FB
20–22, (Fig. 1.B,
right). Upon the excitation of the primary donor P700, which is a
chlorophyll dimer, an initial charge separation will occur and stabilized
by further reduction reactions as shown in (Scheme 1).
Scheme 1. Approximate reduction potentials (mV) of different co-factors
in electron transfer Chains in Photosystem I (vs SHE) a,b
a Em values are from ref. 22
b Fd is soluble protein ferredoxin, while other Co-factors presented are
same as defined in Fig. 1
116 Egypt. J. of Appl. Sci., 35 (9) 2020
Figure 1. [PDB code 1JB014] : A) [left panel]: polypeptide structure of Cyanobacterial
PS I monomer viewed perpendicular of the plane of the thylakoid membranes. [right
panel]: Co-factors of PS I including chlorophyll molecules, -carotenes, LMG, LHG,
PQN and iron-sulfur clusters. B) [left panel]: PsaA/PsaB heterodimeric core carries
most of co-factors and pigments in PS I and PsaC protein subunit comprises FA and FB
iron sulfur clusters. [right panel]: Electron Transfer Chains ETCs in PS I, where P700
is primary electron donor (Chl a dimer), primary electron acceptors A /A0 (Chl a
molecules), secondary electron acceptor A1 ( Phylloquinone molecule PQN), tertiary
electron acceptor FX and terminal electron acceptor FA and FB
20.
With midpoint potential ranges from −200 to −700 mV, Fe-S proteins
clusters are considered as an important co-factor, which provides the
fundamental basis to understand different factors affecting the redox
properties in-situ20,22. Fe-S clusters in biosystems are known to have
different roles such as catalysis, structural stability, nitrogen fixation, sulfide
and iron storage and electron transfer23,24. It can exist in different spin states
due to the ferromagnetic and antiferromagnetic couplings between Fe-
Islands23,25,26. In PS I, the Fe-S clusters are a distorted cube of 4 Iron atoms
linked by 4 bridging sulfur atoms and covalently bound by 4 cysteine sulfur
atoms as shown in Fig. 2. They are known to be low potential [4Fe-4S] +2/+1
clusters27–29. In their oxidized state, FX, FA and FB possess a net spin of zero
due to the paramagnetic pairing between two mixed valence states
Fe+2.5−Fe+2.5. While, in their reduced states, only one Fe+3 ion exists.
Egypt. J. of Appl. Sci., 35 (9) 2020 117
Figure 2. Distorted cube of [4Fe-4S] cluster, where that Iron and sulfur atoms are
indicated by brown and yellow spheres respectively. The non-bridging sulfur atoms is
the Thiol sulfurs. And the blue atoms are backbone carbons of ligating cysteine residue.
Implying the presence of paramagnetic pairing between an equalvalence
pair Fe+2−Fe+2 and a mixed-valence pair Fe+2.5−Fe+2.5, giving rise to
a net spin of ½. Depending on these magnetic properties, low-temperature
Electron Paramagnetic Resonance EPR spectroscopy was used to determine
midpoint potentials for these clusters which had been reported to be -705 ±
15 , -530 and -580 mV for FX, FA and FB respectively20,22. However, other
studies suggesting that the midpoint potentials of these clusters would be
positively shifted , at room temperature11,30–32. The redox potential
calculations of iron-sulfur clusters in PS I and other proteins were
investigated in the literature33–35. In the present study, we are calculating the
redox potentials of the three iron sulfur clusters in PS I and investigating
different interactions in situ. For this, we are employing a continuum
electrostatic analysis coupled to Monte Carlo methods and parameterized at
the DFT level of theory as in the multi-conformer continuum electrostatics (
MCCE )36.
COMPUTATIONAL METHODS
A set of methods are used to investigate the electron transfer,
structural properties and energetics of interactions stabilizing the
ionization state of iron sulfur clusters in PS I. Where that bond distances
in these clusters are estimated using density functional theory (DFT).
While the effect of solvent and protein environment on the value of
midpoint potential is studied with the continuum solvent model, followed
by Monte-Carlo sampling of microstates to model the Em titration of
ionizable groups in protein.
Initial coordinates are defined according to Crystal structure for
Thermosynechococcus elongatus (Ref. code: 1JB014) ), at resolution 2.5
Å , from the Protein Data Bank (PDB). Structures for [4Fe-4S] clusters
118 Egypt. J. of Appl. Sci., 35 (9) 2020
FX, FA and FB, surrounded by ~10 Å nearby residues (Fig. 3), are taken
from the crystal structure and subjected to geometry optimization at
DFT/B3LYP level of theory, using LANL2DZ core potential for Fe and
6-31G* basis Set for other atoms, using Gaussian09 package. The broken
symmetry wave function is used to represent the antiferromagnetic
coupling between iron Islands in the reduced state of [4Fe-4S] clusters
with total spin of
37. Investigating the nature of electrostatic
interactions in Protein is crucial for determining its function and
structure. Protein environment changes the free energy of ionization due
the pair-wise interactions between protein charges and dipoles with
different ionization states and the desolvation upon moving a charged
group from solvent (water) to protein38. Interaction energies in the
protein are estimated by the Classical
Figure 3. Structural models used in this study. 1, 2 and 3. Are the iron-sulfur clusters
in PS I surrounded by near aminoacids (~10 Å ) from PsaA/PsaB and PsaC subunits.
Where that the letters A, B and C refers to the subunits PsaA, PsaB
and PsaC, respectively. 1. All amino acids near the FX active site from
both protein domains PsaA and PsaB. 2. and 3. The stromal iron-sulfur
Egypt. J. of Appl. Sci., 35 (9) 2020 119
cluster FA and FB, respectively, surrounded by near residues from PsaC
subunit. continuum calculations as implemented in MCCE program,
where that the redox reactions in ligated Fe-S clusters are modeled by
treating each Fe, bridging S ions and each residue as separate fragments
with integer charges, which are interacting with each other by the means
of electrostatic and Lennard-Jones potentials39. Within MCCE, the
DELPHI software40 is used to numerically solve the Poisson-Boltzmann
(PB) equation to calculate electrostatic interactions. Where that the
solvent (water) is treated as a continuum model with high dielectric
constant ( ), and the protein is considered as low dielectric
region ( ). Upon energy calculations, the energy look-up table
is built, and theoretical titration is modeled by obtaining Boltzmann
distribution of microstates, using Monte-Carlo approach. Where that
microstates of the structures are defined depending on oxidation states of
Fe ions and the protonation states of the surrounding organic ligands39,41.
The energy of microstate Gx with M conformers is computed according
to the equation below42:
Σ
*( ( ) ( ))
( ) Σ
+
Where that is equal to 0 if microstate , lacks conformer and 1
otherwise. While takes the values 0, 1 and -1 for neutral, bases and acid
conformers, respectively. is the number of electrons transferred upon
redox reactions. and are the reference and for
each fragment in the reference dielectric medium (e.g. water). F is the
faraday constant, while Kb is the Boltzmann constant and T is temperature
(298 K in our calculations). is the desolvation energy of moving
conformer i from solution to its position in protein. is the pair-wise
interaction between different conformers i and j. While is the pairwise
interaction of conformer i with other groups with zero conformational
degrees of freedom (e.g. Backbone atoms).
In MCCE, transferring the redox co-factor from the solvent to the protein
will shift the value of relative to the , and the free energy of
ionization at a given Eh is estimated from the following equation 43,
( ) (
) (3)
Where that
is mean field interaction between the co-factor in
study and the average occupancy of conformers of all other residues in the
protein in the Boltzmann distribution at this Eh.
120 Egypt. J. of Appl. Sci., 35 (9) 2020
RESULTS AND DISSCUSSION
Structural Models.
Molecular structures for [4Fe-4S] clusters in PS I have been resolved by
X-ray diffraction (PDB code: 1Jb0) . Iron sulfur clusters surrounded by
~10 angstrom residues are extracted from the x-ray crystal structure as
shown in Figure. 3. and subjected to the continuum electrostatic
calculations.
Calculation of for [4Fe-4S] clusters in PS I. The reference
midpoint potential
for Fe ions used in the calculations is -1000 mV.
Midpoint potentials, Em’s, were calculated at pH 10 for each cluster, FX,
FA and FB (Table 1). The Em value of the first cluster FX was reported to
be is -894 mV which is ~189 mV more negative than experimental values.
Low-temperature EPR experiments determined midpoint potentials of FA
and FB to be -540 and -580, respectively22. Our calculated midpoint
potentials of FA and FB are -587 and -624 mV, respectively. Which are
shown to be within the range of experimentally determined values.
Although, calculated Ems are shown to deviate from the experimentally
reported values, our results are shown to agree with the reported
experimental ordering20,22. This result may be attributed to the lack of
long-range electrostatic interactions with other residues in the PS I
protein complex. And a reduction calculation includes all protien
complex, may be needed.
Table 1. Calculated Midpoint potential for redox couples
[4Fe4S]+2/+1 in PS I
Cal. Emsa Exp. Emsa
FX -894 -705h
FA -587 -540h
FB -624 -580h
a value is in mV
h ref(20,22)
CONCLUSION
We have documented for the first time the reduction calculation of
iron-sulfur clusters in PS I using the MCCE Model. The values obtained
are approximately within the range of experimental reported potentials.
This methodology can be applied for the for iron-sulfur cluster in
PS I protein complex including all prosthetic group to analyze electron-
Egypt. J. of Appl. Sci., 35 (9) 2020 121
proton coupled transfer and different interactions with nearby charged
amino acids.
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حساب جهد الأکسدة الإخت ا زلیة لمجموعات الحدید و الکبریت فی النظام
الضوئی الأول
فداء عمی 1 ، مدحت وهبة شفاعة 2 ، محمد امین 3
-1 شعبة الفیزیاء الحیویة – قسم الفیزیاء – کمیة العموم – جامعة حموان
-2 قسم العموم- جامعة جروننجن – جروننجن ىولندا
-3 معید العموم الجزیئیة الحیویة و التکنولوجیا الحیویة – جامعة جروننجن - جروننجن ىولندا
النظام الضوئی الأول ىو معقد بروتینی ناقل للإلکترونات. أوضحت نماذج الییاکل
الثلاثیة الأبعاد لممعقد البروتینی و المعتمدة عمى بنیة البمو ا رت بالآشعة السینیة أن سمسمة نقل
الالکترونات تحتوی عمى ررعین شبو متناظرین من الحوامل اإللکترونیو حیث تمتقی نیایة کلا
ری . FB و FA و التی یتبعیا مجموعتان طرریتان FX الفرعین عند أول مجموعو حدید و کبریت
الد ا رسة الحالیة تم حساب جید الأکسدة اإلخت ا زلیة لمجموعات الحدید و الکبریت باستخدام
الطرق المبنیة عمی الکیربیة الستاتیکیة الکلاسیکیة. تم استخ ا رج الشکل الثلاثی الابعاد لمکتل
الثلاثة محاطة بالأحماض الأمینیة ری حدود 11 انجستروم من نموذج بنیة البمو ا رت بالآشعة
و تم حساب جید )PDB ID: 1JB السینیة لمنظام الضوئی الأول ری البکتیریا الزرقاء ) 0
أوضحات الحسابات أن جید الأکسده .MCCE الأکسدة اإلخت ا زلة بإستخدام النموذج الحسابی
لو أقل قیمة بالمقارنة بقیم الجید لممجموعات الأخرى FX اإلخت ا زلة لأول مجموعة حدید و کبریت
ری النظام الضوئی الأول بینما اکبر قیمة لجید الأکسدة و اإلخت ا زل کانت لمجموعة الحدید و
مما یتفق مع الترتیب الذی قد تم رصده معممیا. FA الکبریت
Egypt. J. of Appl. Sci., 35 (9) 2020 125
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