Model of the Oxygen Evolving Complex Which Is Highly Predisposed

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Biophysical Chemistry, Biomolecules, and Biomaterials; Surfactants and Membranes

Model of the Oxygen Evolving Complex Which is Highly Predisposed to O–O Bond Formation. Yulia Pushkar, Katherine M. Davis, and Mark C Palenik J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.8b00800 • Publication Date (Web): 04 Jun 2018 Downloaded from http://pubs.acs.org on June 4, 2018

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The Journal of Physical Chemistry Letters

Model of the Oxygen Evolving Complex Which is Highly Predisposed to O–O Bond Formation Yulia Pushkar , Katherine M. Davis , Mark Palenik 1*

1

2

3

Department of Physics and Astronomy, Purdue University, West Lafayette, Indiana 47907, United States

2

Department of Chemistry, Princeton University, Princeton, New Jersey 08544, United States

3

NRC research associate, Code 6189, Chemistry Division, Naval Research Laboratory, 4555 Overlook Avenue SW, Washington, DC, 20375

AUTHOR INFORMATION Corresponding Author *[email protected]

ACS Paragon Plus Environment

1

The Journal of Physical Chemistry Letters 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 20

Light driven water oxidation is a fundamental reaction in the biosphere. The Mn Ca cluster of 4

Photosystem II cycles through five redox states termed S -S after which, oxygen is evolved. 0

4

Critically, the timing of O–O bond formation within the Kok cycle remains unknown. Combining recent crystallographic, spectroscopic and DFT results, we demonstrate an atomistic S -state model with the possibility of a low barrier to O–O bond formation prior to the final 3

oxidation step. Furthermore, the associated one electron oxidized S -state does not provide more 4

advantages in terms of spin alignment or the energy of O–O bond formation. We propose that a high energy peroxide isoform of the S -state can preferentially be oxidized by Tyr in the course ox z

3

of final electron transfer leading to O evolution. Such a mechanism may explain the peculiar 2

kinetic behavior as well as serve as an evolutionary adaptation which avoids release of the harmful peroxides.

TOC GRAPHICS

KEYWORDS Density Functional Theory (DFT), photosystem II, S -state, O-O bond formation, 3

oxygen evolving complex.


2

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Oxygenic photosynthesis is responsible for the conversion of water and carbon dioxide to carbohydrates and molecular oxygen.

1-2

The initial steps of photosynthesis take place in

photosystem II (PS II) (Figure 1A) a multi-subunit metalloenzyme complex embedded in the thylakoid membranes of green plants, algae, and cyanobacteria. Produced upon light excitation 3

that oxidizes the reaction center, P

•+ 680

is reduced via a tyrosine residue (Tyr ) by the oxygen Z

evolving complex (OEC), Mn Ca cluster. Water oxidation relies on a delicately orchestrated 4

sequence of proton and electron transfer steps. While this reaction has great promise for 3-4

practical applications in the field of artificial photosynthesis, key components of the mechanism remain elusive.

Figure 1. A) Schematic of electron transport in photosystem II. B) A current model of the Kok cycle depicting incident visible light photons and electron/proton release.


3


Page 4 of 20

Significant breakthroughs have been achieved in the elucidation of the PS II structure with a focus on the Mn O Ca cluster embedded in a functionally relevant protein matrix. Its operation 5-11

4

5

depends on its ability to accumulate four oxidizing equivalents by cycling through five intermediate states, known as the S -S states of the Kok cycle, Figure 1B.

12-14

0

4

When the cluster

reaches the highly reactive S state(s), O is released, and the system decays back to S . Currently, 4

2

0

S is the most oxidized state reliably trapped for analysis, Figure 1B.

10, 15-20

3

In comparison with other

S-states its formation is significantly more sensitive to ligand modifications and changes to the local protein environment.

21-22

Furthermore, S -state generation has a significant activation barrier

23

3

and involves extensive structural re-arrangements characterized previously by extended x-ray absorption fine structure (EXAFS), Table S1.

10, 20, 24

A number of hypotheses have even suggested

transient O–O bond formation may already occur in the S state and the redox isomerism of this 4, 25

3

state has been analyzed by DFT methods.

26-28

Here, we analyze models of the S state in light of newly available time-resolved 3

crystallography (TR-XRD) results visualizing the putative S -state. 3

5, 8, 29

We show that the S -state 3

model put forward by our research group in 2015 is in good agreement with TR-XRD results 30

and displays a predisposition to O–O bond formation via a radical coupling mechanism. The associated S -state model, obtained by proton coupled electron transfer (PCET), does not provide 4

the same advantages to O–O bond formation. Our DFT modeling shows that the S -state can have 3

an admixture of the higher energy (~ +0.2 eV) peroxo isoform. Two conflicting structures of the OEC in the putative S -state have been published recently, 3

Figure 2A.

5, 8

In one, additional electron density was observed in the isomorphous Fourier

difference map between the dark stable S state and that following 2-flash illumination – 1

nominally S , which was interpreted as an additional oxygen atom in the cluster. This change 5

3


4

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was not detected by Young et al., Figure 2A. We compared these TR-XRD coordinates with 8

previously constructed models of the S state, Figures 2 and 3. Consistent views on the 3

mechanism of O–O bond formation and structures of the reactive intermediates in the S-state cycle have been expressed in the works of Dr. Per Siegbahn,

31-35

and compare multitudes of possibilities.

26-28, 36-39

while others preferred to discuss

Topologically, Siegbahn’s S model depicts a 3

conversion of the Mn from five- to six-coordinated via the addition of a ligating hydroxyl group 1D

during the S to S transition. The S -state model derived from advanced EPR analysis by Cox et 34

2

3

3

al. and by QM/MM in combination with EXAFS and XRD are in good agreement with the 18

40

Siegbahn’s model, as these too contain a hydroxyl group on the Mn center. However, EPR 1D

results do not exclude other S models in which all Mn centers are in the Mn oxidation state or IV

3

even a peroxo intermediate in which the Mn oxidation state is different.

41


5


Page 6 of 20

Figure 2. Alignments of the recent crystallographic S -state model proposed by Suga et al. (PDB 3

ID: 5WS6) with (A) the analogous crystallographic model proposed contemporaneously by Young et al. (PDB ID: 5TIS) and (B) the Siegbahn DFT-derived model for the S state. Models 3

were aligned using the atoms of the Mn CaO cluster with an RMSD of 0.14 Å and 0.22 Å, 4

5

respectively. Inclusion of O6 in the alignment of (B) results in an RMSD of 0.31 Å. In each case, the Suga et al. model is rendered in grey, with the comparative model colored by element. Movies SI1-SI2 provide 360°-views of each comparison respectively. The positions of surrounding amino acids were not used in the alignment.


6

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Figure 3. A, B) Alignments of our DFT-derived model for the S state (shown in grey) with (A) 3

30

the crystallographic S -state model reported by Suga et al. (PDB ID: 5WS6) and (B) our DFT3

optimized coordinates for the Suga et al. model. (C) Alignment of the DFT-derived model for the peroxo isoform S OO state obtained with B3LYP* geometry minimization (colored) to the 42

3

crystallographic S -state model reported by Suga et al. (PDB ID: 5WS6) (shown in grey). All 3

models were aligned using the atoms of the Mn CaO cluster to yield RMSDs of 0.28 Å (0.39 Å, 4

5

including O6), 0.11 Å (0.12 Å, including O6), and 0.25 Å (~0.27 Å, including O6), respectively. Movies SI3-SI5 provide 360°-views of each comparison respectively. The positions of surrounding amino acids were not used in the alignment. Young et al. did not observe the aforementioned –OH in their TR-XRD experiments. They 8

argue that Mn -OH containing models are inconsistent with their results as the additional 1D


7


Page 8 of 20

oxygen in the hydroxyl group should appear at sufficient distance from the OEC core to be resolved at the reported crystallographic resolution. In contrast, the Siegbahn structural model containing Mn –OH provides good agreement with the XRD results by Suga et al. (Figure 2B).

5

1D

However, some caution should be exercised here as, in comparison with typical Mn –OH IV

bonds,

43-46

the Mn–OH bond length (~1.77 Å) in Siegbahn’s 2013 model is on the short side, 34

while the O O bond distance is ~2.48 Å. Our DFT calculations of this topology yielded a more …

typical Mn-OH distance of 1.85-1.82 Å,

and O O distance of ~2.6-2.5 Å depending on the Mn

43-46

…

protonation state (see SI). While experimental results indicate that O evolution and the final 2

electron transfer step are simultaneous, the energy diagrams presented by Siegbahn for the S to 4, 25

3

S transition where oxygen is evolved mandate at least two barriers after the final electron 0

removal and prior to O–O bond formation.

34-35

Recent extended screening of O-O bond formation

pathways in the S -state, modeled to contain one oxyl-radical species, confirmed Siegbahn’s 4

results and likewise support two sequential barriers prior to O evolution. To account for 38

2

inconsistencies in available DFT models of the S to S transition and spectroscopic results for the 3

0

S to S transition, our group proposed a different S -state model containing a unique Mn =O-Ca 3

0

IV

3

bridge in 2015, Figure 3.

30

Our fundamental hypothesis included the S -state formation of a Mn =O fragment on the last 3

IV

Mn center to be oxidized, Mn . This proposal supports a mechanism in which Mn cannot be 30

1D

1D

oxidized during lower S-state transitions, as it lacks a ligand capable of PCET. To ensure equivalency between energy inputs for each S-state transition in our model, we describe each Sstate transition as a PCET event, Figure 4A. We further verified that the energetics of the S-state transitions are consistent with the driving force available from the Tyr-OH=Tyr-O× + e + H -

+

couple, Table S2, Figure 4. The high activation energy measured for the S to S transition is in 2


3

23

8

Page 9 of 20

good agreement with the need for substrate binding to Mn and substantial structural changes to 1D

create a reactive Mn =O fragment. IV

A

B

2F

1F

0F

~1.46 Å

d

S4

3F

Energy

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


S=1

S3OO

∆G = 0.19 eV

- e- H+

d

S3

- e- H+

S=3

S2

- e- H+

C

S3 ~1.53 Å

d

S1

- e- H+

~2.52 Å

S=1

S3OO

∆G = 0.14 eV

S0

d

ΔTyr = 17.55 eV S=3

~2.5 Å

S3

~1.45 Å

d 1

S= /2 S4OO ∆G = 0.81 eV

BP86

~2.4 Å

d

S4

S = 1/2

~1.54 Å

d

S= 5/2 S4OO ∆G = 0.38 eV

B3LYP*

~2.54 Å

d

S4

S= 3/2

Figure 4. (A) Energy diagram of S-state transitions. Red ticks represent the energy change (D ) Tyr

due to TyrY × reduction in the PCET process: (Tyr-OH=Tyr-O× + e + H ). Green ticks show the -

Z

+

changes in energy due to S-state transitions, Figure S2. (B, C) Scheme comparing the energies of the S or S state with energies of the corresponding peroxides computed with broken symmetry 3

4

approach using BP86

47-48

or B3LYP* functional, Table S3.

Equally, our model predicts significant shortening of one Mn-Ca vector, previously observed experimentally. The presence of a substrate oxygen as a Mn =O-Ca bridge is also in agreement 10

IV

with the order of magnitude increase in substrate exchange rate of the S state upon Ca to Sr 3

substitution. Involvement of Mn =O in the catalytic cycle is consistent with the observation 49

IV 1D

that the first oxidative modification happens at His332, which is a direct ligand to Mn . We 50

1D

have shown that Ru =O is active in oxygen atom transfer and that N-oxides can be generated as IV

side products in catalytic water oxidation by Ru complexes.

51-52

The S -state model presented 3

herein provides ample opportunity for O-O bond formation between the Mn -O-Mn + 4A


3B

9


Page 10 of 20

Mn =O (O…O = 2.52 Å) the next closest distance is Mn =O + H O-Ca (O…O = 3.22 Å). IV 1D

IV 1D

2

Furthermore, the presence of the Mn =O-Ca bridge makes our S model (Figure 3A) more IV

3

compact than the original Mn -hydroxyl model, which is a likely intermediate to the Mn-oxo 1D

group formation, Table 1, perhaps explaining why it is difficult to resolve the additional oxygen via XRD. Mn-Mn distances in our model are in agreement with both XRD structures and EXAFS results, Table S1. Note that EXAFS-detected changes observed during the S to S transition are 2

consistent with elongation of the Mn-Mn distance to ~2.8 Å.

10, 20, 24

3

Overlaying our 2015 S -state 3

model with the most recent XRD model (RMSD of 11 atoms in cluster ~0.39 Å, exclusion of O6 yields ~0.28 Å),

5, 30

Figure 3A. Surprisingly, DFT optimization of the Suga et al. coordinates, 5

truncated in the same manner, also converged to our model (RMSD of 11 atoms in cluster ~0.12 Å, exclusion of O6 yields ~0.11 Å), Figure 3B. Recently another group reported peroxide as a result of DFT optimization from the coordinates of Suga et al. From the provided structural 41

comparisons and energy analysis, we conclude that our S model is a very viable representation 3

of the S -state of the oxygen evolving complex in Photosystem II. 3

Furthermore, our atomic model shows the presence of motifs highly predisposed to O-O bond formation. Most obvious is the radicaloid character of the oxygen in the Mn =O-Ca fragment IV

with spin density of r =0.36. This radical fragment is complemented by the bridging oxygen in O

the Mn -Mn di-µ-oxo bridge with r =0.10, Figure 5A. Another OEC-specific requirement that 4A

3B

O

would ensure a low barrier to O-O bond formation was proposed by Siegbahn in 2006 and necessitates “spin alignment”, defined as alternating spins with antiferromagnetic coupling 53

between the Mn and Mn centers. Our S -state model (S=3) shows robust spin alignment, Figure 1

4

3

5A. S=3 spin was established by EPR

18-19, 54

and it is also one of low energy states according to the


10

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ground state of a Heisenberg exchange Hamiltonian fitted to broken symmetry calculations (Table S3). Addition of the water coordinated to the Mn -Mn di-µ-oxo bridge observed in 4A

3B

recent XRD coordinates, does not affect the spin alignment. We also considered the role of protonation state during O-O bond formation, presented in the SI (1.1).

Figure 5. Models of the S (A) and S (B) states comparing spin densities on the key oxygens and 3

4

Mn centers along the path of radical coupling. Values in brackets are given for S-state models without water coordinated to the Mn -Mn bridge. C) spin alignment observed in the transition 4A

3B

state in the Ru-based catalysts for water oxidation. To validate this analysis further, we applied the same logic to assess whether the spin alignment paradigm works for other systems such as Ru-based water oxidation catalysts. We have recently discovered that a simple cis-[(bpy) Ru(H O) ] catalyst acts via a radical coupling 2

mechanism.

55-56

2

2

2+

O-O bond formation is facilitated by the H-bond-stabilized dimer of

[(bpy) Ru =O,OH] , Figure 5C. In a transition state computed for conversion to peroxide (DG » V

2+

2

1 eV, transition state (TS) energy of only ~0.27 eV), spin alignment was prominent, with r =O

0.48 and r =+0.82 on the two oxygens forming the O-O bond, and TS (O O) ~1.8Å, Figure 5C. …

O


11


Page 12 of 20

Thus, we conclude that radical coupling provides a low barrier to O-O bond formation and demonstrate the potential of spin alignment as an activation barrier lowering mechanism. Given support for the spin alignment criterion in a related system, it is then reasonable to question whether oxidation of the S -state by one electron to form the transient S -state would 3

4

result in significantly better spin densities/alignments in comparison to those of our S -state 3

model. We therefore conducted oxidation of our S model via PCET to form the S -state (S=1/2), 3

4

Tables 1 and 2, Figure 4A. The generated S intermediate features one Mn ion in the Mn V

4

1D

position with quite modest spin density of r =0.07 on the Mn oxo (Mn-O ~1.65Å, an O O O

...

1D

distance ~2.38 Å, Figure 5B). Previously, Borovik and co-authors demonstrated that a coordination compound with a high spin (S=1) Mn =O fragment displays relatively modest O V

17

hyperfine splitting (hfs), A ~10 Mz. This splitting is significantly smaller than that reported for 57

z

Ru complexes active in water oxidation, hfs ~24-60 G. Thus, it is not clear a priori that an V

58

additional oxidation step via electron removal during the S to S transition can generate a state 3

4

more pre-disposed to O-O bond formation than the current S model. Earlier discussion of the S 3

4

state as likely having mostly diamagnetic (low spin) Mn =O is in good agreement with our DFT V

59

results for the S -state summarized in Figure 4B. Discussion of the spin density distribution of 4

Siegbahn’s S model is given in the SI (1.2). 4

With S and S state models in hand, we proceed to form an O-O bond, Figure 4B, C. In the 3

4

interest of transparency, we prefer not to introduce any empirical energy corrections as in, but 34

instead, compare the energy difference between the peroxo isoform and the parent S-state. We first generated the peroxo isoform at the S level. Our S model forms the peroxo intermediate 4

4

with a positive DG = +0.95 eV, Table 1. The energy difference from broken symmetry calculations is also ~+0.8eV, Table S3, Figure 4B. The energy difference between the S -state 4


12

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and its peroxo isoform decreases to +0.29 eV when computed using B3LYP*/Def2TZVP (Table 60

1), while the broken symmetry value is slightly higher at ~0.38 eV, Table S3. Thus, the increase of Hartree-Fock exchange appears to stabilize the peroxo isoform in the case of the S -state. The 4

same tendency was noted earlier by Dr. H. Isobe and co-workers. Note that both functionals 27

were recommended for computation of Mn compounds.

61

Table 1. DFT energies and spin states derived using Def2TZVP basis set. S-state Computational method BP86 Spin E, eV

G, eV

S

1

1

S

2

1/2 -226125.352 -226106.905

S *

3

3

Broken Symmetry ** BP86

B3LYP*

Spin

Spin

E, eV

E, eV

-226141.681 -226123.123

-228188.912 -228170.158 0

3

-228192.096 -227323.611 S OO

1

3

-228188.019 -228169.355 1

3

-228191.908 -8353.470 S

1/2 -228171.897 -228153.442 1/2

4

1/2

-228175.083 -227306.677 S OO

1/2 -228170.931 -228152.495 3/2

4

1/2

-228174.278 -227306.302 S

1/2 -226157.554 -226138.740

0

* S structure was obtained by geometry optimization starting from Suga et al. coordinates (PDB ID: 5WS6). Different protonation pattern with one proton moved from the Mn water to Mn =O oxo-group with formation of the Mn -OH resulted in E=-228189.678 eV. 3

4A

1D

1D

** Broken symmetry calculations only available for S and S states. Energies are computed by diagonalizing a Heisenberg exchange Hamiltonian fitted to broken symmetry energies. 3


4

13


Page 14 of 20

Using BP86/Def2TZVP to optimize the peroxo isoform of the S state (termed here S OO), we 3

3

noted the following behavior: i) at spin greater than S=1, the model tends to converge to the S

3

state; ii) at S=1, the model tends to converge to the peroxide, however, either His332 loss from Mn , or water relocation from Mn to the oxygen bridge between Mn and Mn occur. Both lead 1D

4A

4A

3B

to formation of a 5-coordinated Mn center. Formation of the associated peroxo intermediate was uphill (DG ~0.9 eV) similar to the generation of O-O from the S state, Figure 4B and Table 1. 4

Broken symmetry analysis decreased this difference to +0.19 eV, Table S3.

Use of the

B3LYP*/Def2TZVP permits geometry optimization of the peroxo isoform without major structural re-arrangements, which is in agreement with another report . The peroxo isoform is 41

now only +0.6 eV higher in energy, Table 1, while broken symmetry calculations produced a +0.14 eV difference (for consistency, the structure with 5-coordinated Mn, optimized using BP86/Def2TZVP, was used in BS calculations). Overall, generation of the S -state does not 4

appear to lower the energy required for O-O bond formation while the selection of computational approach has a significant effect. These data are similar to results of the spin density analysis and show no major advantages for the S -state over S in its ability to form the 4

3

O-O bond. In this study, we present an S state model which has an accessible peroxo isoform. The 3

possibility of such a state has long been discussed in the works of Dr. Renger.

4, 62

The first

experimental evidence was indirect and the existence of so-called trigger reactions and/or trigger intermediates was proposed based on the analysis of electron transfer kinetics.

4, 62

The theoretical

models discussed herein allow for the identification of two putative trigger reaction states. For the S to S transition, the trigger state receives H O/OH onto the 5-coordinate Mn center. The -

2

3

2

1D

subset of centers which bound the new ligand can now proceed with oxidation to form S . 3


14

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Our computational analysis shows that the S -state can have an energetically accessible peroxo3

isoform, termed S OO. The ability of near-infrared (NIR) light to induce new EPR signals from 3

the OEC S state at cryogenic temperatures, provides further indirect evidence for potential high 3

energy intermediates of the S -state. Mn complexes, in particularly those containing a Mn =O 63

IV

IV

3

fragment, often have absorption peaks in the NIR.

43, 64

The exact nature of the states formed by

cryogenic NIR excitation is not known, however, the energy of NIR photons (~1.5 eV) is well within the energies required for S peroxo isoform production. 3

More direct experimental evidence of the possibility for O–O bond formation prior to final electron transfer from Tyr were presented via time-resolved X-ray emission spectroscopy.

30

Z

Likewise, TR-XRD results support a potential O–O bond intermediate in the S -state, with a 3

refined O–O distance of ~1.4Å, although XRD resolution limits such an interpretation. Unusual 5

treatment of the crystals such as “shrinkage” using additional cryoprotectants may increase the prevalence of the S peroxo isophorm, which otherwise might only occur as a small population in 3

the solution state. For models of the S state which feature a Mn =O–Ca activated fragment, formation of a IV

3

higher energy peroxo isoform is energetically feasible. The exact energy difference determined strongly depends on the computational technique applied, as was also noted by Yamaguchi et al.

26

and whether broken symmetry is considered or not. Regardless of the computational approach, the energy difference between the S -state and its peroxo isoform is comparable to the energy 3

difference between the S -state and its peroxo isoform. Thus, formation of the fully oxidized S 4

4

state provides little advantage relative to the S -state for peroxide formation. DFT results do not 3

contradict the hypothesis of peroxide formation prior to the final electron transfer step, in which an electron is transferred from the peroxo intermediate to the oxidized Tyr . Z


15


Page 16 of 20

ASSOCIATED CONTENT Supporting Information. The following files are available free of charge. Additional discussion, computational methods, Tables S1-S4, DFT coordinates, movie captions (PDF) Movies S1-S5 (MPG) Coordinates for S -S , S Mn1DOH, S OOisoform, S SugaOpt (XYZ) 1

3

3

3

3

AUTHOR INFORMATION Notes The authors declare no competing financial interests. ACKNOWLEDGMENT This work was supported by the National Science Foundation, Division of Chemistry CHE1350909 (Y.P.). This work was further supported by the Arnold O. Beckman Postdoctoral Fellowship (K.M.D.). Additional support came from the Office of Naval Research, directly and through the Naval Research Laboratory, and from an NRC/NRL postdoctoral fellowship (M.C.P.). REFERENCES (1) Najafpour, M. M.; Renger, G.; Holynska, M.; Moghaddam, A. N.; Aro, E. M.; Carpentier, R.; Nishihara, H.; Eaton-Rye, J. J.; Shen, J. R.; Allakhverdiev, S. I. Manganese Compounds as Water-Oxidizing Catalysts: From the Natural Water-Oxidizing Complex to Nanosized Manganese Oxide Structures. Chem. Rev. 2016, 116, 2886-2936. (2) Karkas, M. D.; Verho, O.; Johnston, E. V.; Akermark, B. Artificial Photosynthesis: Molecular Systems for Catalytic Water Oxidation. Chem. Rev. 2014, 114, 11863-12001. (3) Wydrzynski, T.; Satoh, S., Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Springer: Dordrecht, 2005.


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Model of the Oxygen Evolving Complex Which Is Highly Predisposed

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