Comparison between Experimental and Broken Symmetry Density

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A Comparison Between Experimental and Broken Symmetry Density Functional Theory (BS-DFT) Calculated Electron Paramagnetic Resonance (EPR) Parameters of the S State of the Oxygen Evolving Complex of Photosystem II in Its Native (Calcium) and Strontium Substituted Form 2

Nathan J. Beal, Thomas A. Corry, and Patrick J. O'Malley J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.7b09498 • Publication Date (Web): 27 Nov 2017 Downloaded from http://pubs.acs.org on November 28, 2017

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The Journal of Physical Chemistry

A Comparison Between Experimental and Broken Symmetry Density Functional

Theory

(BS-DFT)

Calculated

Electron

Paramagnetic

Resonance (EPR) Parameters of the S2 State of the Oxygen Evolving Complex of Photosystem II in its Native (Calcium) and Strontium Substituted Form. Nathan J. Beal, Thomas A. Corry and Patrick J. O’Malley* School of Chemistry, The University of Manchester, Manchester M13 9PL, UK.

ABSTRACT A comparison between experimental and Broken Symmetry Density Functional Theory (BS-DFT) calculated hyperfine couplings for the S2 state of the oxygen evolving complex (OEC) has been performed. The effect of Ca substitution by Sr combined with the protonation state of two terminal hydroxo or aqua ligands, W1 and W2, on the calculated hyperfine couplings of

55

Mn,

13

C,

14

N,

17

O and 1H nuclei has been investigated. Our

findings show best agreement with experiment for OEC models which contain a hydroxide group at the W2 position and a water molecule at W1. For this model the agreement between calculated and experimental data for all hyperfine couplings is excellent. Models with a hydroxide group at W1 are particularly poor models. Sr substitution has a minor influence

on

calculated

hyperfine

couplings

in

agreement

with

experimental

determinations. The sensitivity of the hyperfine couplings to relatively minor changes in the OEC structure demonstrates the power of this methodology in refining the details of its steric and electronic structure which is an essential step in formulating a complete mechanism for water oxidation by the OEC.

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INTRODUCTION Photosystem II (PSII) is a multi-unit pigment protein complex found in the thylakoid membrane of organisms that perform oxygenic photosynthesis. One of its key functions is the accumulation of visible light driven oxidising equivalents on its donor side leading to oxidation of water to molecular oxygen in its oxygen evolving complex (OEC).1–9 Only recently has the fundamental atomic-level detailed molecular structure of this important biological complex been successfully revealed. The 2011 X-ray study by Umena et al. and the subsequent X-Ray Free Electron Laser (XFEL) crystal structure helped to provide an atomic-level high resolution structure,10,11 which provides a primary landmark for any suggested proposals regarding the molecular structure and mechanism of the OEC.1,12–14 The structure of the dark adapted state, Figure 1, showed that the OEC was a Mn4CaO5 cluster arranged in a distorted chair form with four terminal oxygen atoms presumably water or hydroxide, labelled W1-W4, directly coordinated to the OEC.10 Two of these can be confidently assigned as water molecules W3 and W4 ligated to the Ca2+ ion and the other two W1 and W2 are either water or hydroxide ligands to the MnA ion. It has been suggested that some of these OEC coordinated water or hydroxide molecules may serve as substrates for water splitting.15,16 Various studies have highlighted an important role for the calcium ion in the oxygen formation reaction with removal of the calcium ion found to block the Sn state transition beyond the S2 state resulting in a complete loss of oxygen evolving activity.17,18 Cation substitution experiments have shown that the only other cation to restore oxygen evolution was strontium albeit at a reduced activity (approximately half that of the native OEC).19–22


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Figure 1. Structure of the model used in this study for the OEC found in darkadapted PSII generated from PDB ID: 4UB6. The protein residues are labelled along with the Mn and Ca bound aqua ligands. Colour coding: manganese (pink), oxygen (red), nitrogen (purple), carbon (yellow) and calcium (white). Hydrogen atoms are omitted for clarity. Substituting

calcium for strontium has been reported to slightly modify the EPR

parameters of the S2 state,19,23 and additionally the substitution has been found to have an effect on several carboxylate stretching modes of the S2−S1 FTIR difference spectra.24–28 These results imply that the calcium ion performs more than simply a structural role in the OEC and may be mechanistically involved. The improved structural information provided by the high resolution crystal structures has provided the key and necessary underpinning for the mechanism of oxygen formation to be investigated in greater detail with theoretical methods or other experimental techniques. 6,7,29–36

This report focuses on the S2 state for both native (Ca) and Sr substituted systems. 3 ACS Paragon Plus Environment


The S2 state is the best characterised Sn state in the Kok cycle, especially in terms of EPR spectroscopy.16,37–49 X-band EPR spectra of the S2 state exhibits a multiline signal at g ≈ 2, originating from an S = 1/2 ground state, most likely with a MnIII(MnIV)3 distribution of oxidation states although other assignments have been discussed at length in the literature.29,35,50,51 Sometimes accompanying this signal at g ≈ 2 is a broad signal occurring at g ≥ 4.1 attributed to an S = 5/2 spin state of the OEC.52 The presence of the multiline signal indicates an antiferromagentically coupled mixed valence manganese cluster, resembling the multiline signal of synthetic or biological dinuclear MnIIIMnIV complexes.53–55 In addition to the metal hyperfine couplings of the S2 state, ligand hyperfine couplings, e.g.

17

O, 14N, 1H and 13C have been used to provide insight into the

molecular and electronic structure of the OEC.16,38,40,56,57 As the S2 state is the best characterised state of the Kok cycle in terms of experimental EPR data it therefore provides a good test of computational results on model complexes for both native and Sr substituted forms of the OEC. A large number of computational studies are currently being applied to OEC models but it is important to limit the suitability of such models and the conclusions drawn from them to well determined experimental parameters, something which is not widely adhered to. As we will show in this study, correct prediction of EPR parameters provides very rigorous constraints on proposed models of the S2 state and such restraints are essential before models can be used further in the S-state cycle progression. In particular, the study focuses on the protonation states of the two MnA ligated oxygen atoms, W1 and W2 using both native and Sr substituted models. As mentioned above, crystallographic studies cannot distinguish hydroxide and water ligands and while protonated states for both waters are energetically and structurally similar, we show that the protonation state can be clearly deciphered by its effect on the EPR hyperfine couplings of the manganese ions in the cluster and its associated ligands. Earlier reports44 on this


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problem for smaller Ca models have indicated that W1 and W2 are aqua and hydroxo ligands respectively in the S2 state. This was based solely on the ability of the model to reproduce the experimental 55Mn HFCs for a small model of the open cubane form. There is however not a complete consensus on this particular protonation pattern58 and further investigations are required using larger models of both the open and closed cubane forms and extending the range of comparison between calculated and experimental HFCs. In this report therefore we extend this analysis to both open and closed cubane forms of S2 using an extensive model incorporating in particular the crucial redox active YZ residue and extend the analysis beyond

55

Mn HFCs to the ligand

17

O,

14

N,

13

C and 1H nuclei. In

addition we include a similar analysis and comparison for Sr substituted S2 models.

COMPUTATIONAL DETAILS The geometries of all the models studied were optimised in their respective high spin states using the BP86 functional, 59,60 utilising the zeroth-order regular approximation (ZORA) Hamiltonian to include scalar relativistic effects.61–63 ZORA adapted segmented allelectron relativistically contracted (SARC) basis sets were employed for all atoms,64 ZORA versions of the def2-SVP basis sets were used for C and H atoms with ZORA versions of the def2-TZVP basis set used for all other atoms with f functions removed.65 The computational time of the calculations was decreased by invoking the resolution of identity approximation (RI) along with decontracted auxillary def2-TZVP/J coulomb fitting basis sets.66–68 The optimizations also included the third generation (D3) semiempirical van der waals corrections proposed by Grimme.69,70 Increased integration grids (grid 4 and grid x4 in orca convention) and tight SCF convergence criteria were used throughout the calculations. The Heisenberg exchange coupling constants, hyperfine and nuclear quadrupole coupling values were calculated for all atoms of interest using the broken symmetry DFT methodology using the hybrid meta-GGA TPSSh functional with 5 ACS Paragon Plus Environment


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the chain of spheres (RIJCOSX) approximation to exact exchange using the same decontracted auxillary basis sets that were used in the geometry optimization steps.71,72 Initial broken symmetry guesses were constructed using the ‘flipspin’ feature of ORCA.73 Calculation of the hyperfine and quadrupole tensors used basis sets developed by Neese et

al. based on the SARC def2-TZVP for the Mn, N and O atoms and def2-TZVP(-f) for all other atoms.68,74 The integration grids were increased to an integration accuracy of 11 and 9 for Mn, N and O respectively. Picture change effects were applied for the calculation of hyperfine and nuclear quadrupole tensors. Heisenberg exchange coupling constants were calculated using the methodology proposed by Pantazis et al.75 The calculated

55

Mn

isotropic hyperfine couplings were scaled by a factor of 1.47 to account for the known spin polarisation deficiency in the calculation of the Fermi contact term.76,77 This factor has been validated for 6 models of mononuclear, dinuclear and tetranuclear manganese complexes (see Table S1 in supporting information; structures are shown in Figure S1). Convergence to the correct BS and HS states in all calculations was confirmed by examination of the calculated Mulliken spin populations.

Model Systems The model systems studied were constructed using starting coordinates taken from two crystal structures of the OEC of PSII available in the literature (PDB ID: 4UB6 (native PSII isolated from Thermosynechococcus vulcanus) and 4IL6 (Sr-substituted PSII isolated from Thermosynechococcus vulcanus)).11,78


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Figure 2. Numbering scheme for the constructed cluster models of the OEC. Colour coding: manganese (pink), calcium/strontium (white), oxygen (red), nitrogen (purple), carbon (yellow). Hydrogen atoms omitted for clarity. The complete model used for the calculations is given in Figure S1 of the Supporting Information. The labelling scheme for all the models (Figure 2) is as follows: the model designators Ca and Sr correspond to the crystal structure that was used as a starting point for the calculations. The native PSII 4UB6 is denoted by Ca, while the Sr-substituted PSII 4IL6 is represented by the label Sr. A second label is used to distinguish between the various protonation patterns of the water or hydroxide groups (W1 and W2) studied which for clarity can be seen in Table 1 below. Table 1. Labelling scheme to distinguish the various protonation states of W1 and W2 in the Ca and Sr models.

Protonation state Label 1 2 3 4

W1 OH2 OH OH OH2

W2 OH OH OH2 OH2

All the OEC cluster models studied contain the seven directly coordinated amino acid residues (all found in the D1 protein chain unless otherwise indicated): Asp-170, Glu-189, His-332, Glu-333, Asp-342, Ala-344 and CP43-Glu-354. Additionally the two fully protonated water molecules coordinated to the calcium/strontium ion were also included as 7 ACS Paragon Plus Environment


well as the W1 and W2 groups coordinated to MnA. As well as this the models include the important second sphere residues: Asp-61, Tyr-161, Gln-165, His-190, Asn-298, His-337 and CP43-Arg-357. In addition to this twelve closely associated crystallographic water molecules as well as partial backbone of Glu-329 was involved, having previously found to hydrogen bond with His-332.79 Inclusion of Tyr-161(YZ) and its hydrogen bonding partner His-190 is essential for all S2 models. This is illustrated in Figure 3 where it is shown that the Highest Occupied Molecular Orbital (HOMO) is located on the phenoxyl head group of this residue with the HOMO-1 (predominantly anti-bonding dZ2) located on the MnDIII ion along the Jahn Teller axis. This is in line with the observed subsequent photooxidation sequence leading first to YZ oxidation to YZ• followed by eventual oxidation of MnDIII to MnDIV forming the S3 state. To reduce computational costs all residues were truncated after the R group, in addition all residues took their standard proton states apart from His-337 where it has been shown a fully protonated histidine is present.79 A representative model is shown in Figure S1 and coordinates of all models are given in the Supporting Information.

Figure 3. HOMO (a) and HOMO-1 (b) electron density contours for the Ca-1 model. Only selected regions are shown without hydrogen atoms.


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RESULTS AND DISCUSSION A full detailed analysis of the geometric structures and the Heisenberg exchange couplings is provided in the Supporting Information. There is little experimental data concerning the closed form of S2 other than the characteristically broad signal in the EPR spectrum. As a result, no hyperfine coupling data will be presented for this form. 55

Mn Hyperfine Couplings

Table 2 shows the spin projected isotropic and anisotropic hyperfine coupling (HFC) tensors calculated for the open cubane form Ca models along with several experimental data sets. At the present time there are numerous sets of experimental hyperfine coupling tensors obtained from various simulations of the spectra obtained from EPR and ENDOR experiments. The differences found in the experimental datasets reflect not only variations in the methodology of the simulations but also aspects of sample origin and preparation. It should be noted that a change in species from spinach to Thermosynechoccus elongatus PSII or treatment of the sample with MeOH may have a visible effect on the splitting pattern in the spectra on the order of ca. 10 MHz for a given HFC value.80 These data sets will therefore be regarded as a range to compare the calculated results with. All three data sets featured in Table 2 find one isotropic HFC around 300 MHz. Two of the data sets feature two HFC near 200 MHz with the remaining HFC being found around 250 MHz.41,81 In contrast, Charlot et al. found two HFCs near to 250 MHz and only a single HFC value around 200 MHz.82 The additional experimental value of 312 MHz found by Teutloff et al. from single crystal Q-band ENDOR refers specifically to the largest hyperfine coupling found in the OEC.80 It is important to note that no experimental studies performed so far have been able to yield sign information or to assign the HFCs to specific manganese sites with any certainty. 9 ACS Paragon Plus Environment


Considering firstly the calculated isotropic HFCs for each of the Ca models shows that Ca-

2 and Ca-3 models may be instantly rejected, as both models produce Aiso values for MnA and MnB which are significantly smaller than shown in any of the experimental datasets. The model Ca-4 produces isotropic HFCs in better agreement with the experimental values however MnB and to a lesser extent MnA are still significantly lower than any found experimentally. An explanation for this behaviour can be seen in the small on-site spin projection coefficients (see Supporting Information) calculated for these models. In contrast the model Ca-1 produces isotropic HFC values in very good agreement with the experimental values with one HFC close to 300 MHz, another HFC was found close to 250 MHz and two HFCs near to 200 MHz (the HFC value of 224 MHz could arguably be associated to either the 250 MHz or 200 MHz grouping). As has been found previously, the largest Aiso value is not found for the MnIII ion (MnD) but rather is calculated for a MnIV ion (MnA). Initially this disagreed with experimentally derived models of the S2 state which were constructed with knowledge gained from studying mixed valence models.83,84 However there is experimental evidence to support the finding of smaller than expected HFC for MnIII centres.77 Additionally the results of other computational studies of the OEC have provided an ever increasing body of computational data which show that the MnIII centre is not necessarily required to provide the largest HFC value in highly connected systems as seen in the OEC.29,44,85,86 Turning to consider the anisotropic HFCs produced by model Ca-1, it can be observed from the experimental simulation data that the anisotropy is more spread out over all the manganese centres. The computed anisotropic HFCs of MnA and MnD are considerably larger than those calculated for MnB and MnC and all of the calculated anisotropic HFCs are in poor agreement with those from experiment. A potential reason for this is the zerofield splitting related anisotropy transfer which has been neglected in the current study and 10 ACS Paragon Plus Environment

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may critically affect the calculated anisotropic HFC data. Efforts to extend the spin projections schemes to include zero field splitting and zero-field splitting anisotropy transfer has been presented in the literature but the investigations have only focused so far on dinuclear MnIIIMnIV complexes.87

Table 2. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 55Mn hyperfine couplings (in MHz) for the investigated Ca models and comparison with experimental data. Model

Ca-1

Ca-2

Ca-3

Ca-4

Kulik et al.81

Peloquin et al.41

Charlot et al.82

Teutloff et al.80

MnA MnB MnC MnD MnA MnB MnC MnD MnA MnB MnC MnD MnA MnB MnC MnD 1 2 3 4 1 2 3 4 1 2 3 4 1

Aiso −287 198 224 −253 −78 65 193 −267 −82 71 190 −280 −179 145 229 −292 193 205 248 298 200 217 245 297 186 243 257 329 312

T1 −30 −8 −5 −51 −1 −2 −3 −56 −5 −2 −4 −60 −4 −5 −5 −59 −23 −20 −13 −23 −20 −17 −13 −14 −5 −26 −32 −17 −37

T2 7 −1 −1 −45 0 0 −1 −44 0 0 −1 −41 0 −1 −1 −50 −23 −20 −13 12 −20 −17 −13 −14 −2 5 −17 −5 14

T3 23 10 6 96 1 2 5 99 5 3 5 101 4 6 7 109 47 40 27 12 40 33 25 27 7 20 49 22 22

Table 3 shows the spin projected isotropic and anisotropic HFCs for the Sr models. The strontium substituted OEC has been investigated to a lesser extent than the native form, however recent EPR experiments have probed its electronic structure. The available 11 ACS Paragon Plus Environment


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experimental data is also included in Table 3. Similar to the native OEC, both of the experimental data sets feature a HFC near to 300 MHz and a smaller HFC below 200 MHz. The data set of Cox et al. shows a second HFC slightly above 200 MHz and a final HFC near 350 MHz.23 However the data set of Lohmiller et al. shows the remaining HFCs to be close together at ca. 220/230 MHz.86 The Sr models display the similar trends to those observed previously for the Ca models. It can be seen that Sr-2 and Sr-3 display calculated Aiso values substantially smaller than those observed in the experimental datasets.

Table 3. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 55Mn hyperfine couplings (in MHz) for the investigated Sr models and comparison with experimental data. Model

Sr-1

Sr-2

Sr-3

Sr-4

Cox et al.23

Lohmiller et al.86

MnA MnB MnC MnD MnA MnB MnC MnD MnA MnB MnC MnD MnA MnB MnC MnD 1 2 3 4 1 2 3 4

Aiso −289 195 234 −253 −51 46 242 −339 −94 81 237 −327 −176 141 240 −291 173 203 243 332 187 221 232 332


T1 −10 −6 −5 −58 −1 −2 −5 −65 −7 −3 −6 −68 −2 −5 −9 −59 −21 −18 −26 −39 −26 −41 −31 −12

T2 0 −2 −2 −36 0 0 −2 −41 0 0 −2 −41 0 −1 −1 −44 −17 −3 1 11 −12 −6 −19 −4

T3 10 8 8 93 1 2 7 106 7 3 8 109 2 6 10 98 37 20 25 29 37 49 51 15

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Additionally similar to the model Ca-4, the isotropic HFCs calculated for model Sr-4 are an improvement over the Sr-2 and Sr-3 but the Aiso values for MnA and MnB are in poor agreement with those found experimentally. The poor agreement for these models can be attributed again to the small on-site spin projection coefficients found for these models. Again, the only model which provides reasonable calculated HFCs is that of Sr-1 which produces isotropic HFCs which coincide with the experimental data very well. Contrasting the isotropic HFCs calculated for both the Ca-1 and Sr-1 model shows there is little difference in the calculated HFCs following substitution of the Ca2+ ion. Historically substitution of the OEC calcium with strontium was thought to change the oxidation state distribution within the OEC cluster and therefore alter the coordination environment of the MnIII ion.88 Instead the current thinking supported by experimental and computational studies in the literature and found in this work is that strontium substitution produces minor alterations to the manganese tetramer.23,43,89 No specific

55

Mn HFCs have been reported for the closed cubane form, so a comparison

between theoretical and experimental values is not possible. The calculated spin projected 55

Mn hyperfine couplings for the closed cubane form are presented for Ca-1, Ca-4, Sr-1

and Sr-4 models in Table S11 of the Supporting Information. 14

N Hyperfine Couplings

As well as studying the 55Mn hyperfine couplings, further information and insight into the electronic structure may be provided by the hyperfine interactions of various ligating EPR active nuclei.90 One such nucleus is the 14N nucleus of the histidine residue (D1-His-332), a ligand to MnD. Experimentally the HFC for this residue have been used to probe the oxidation state assignment of the histidine bound metal.38 Additionally Pérez-Navarro et

al. found that the

14

N signal observed for the native S2 state from Thermosynechococcus 13 ACS Paragon Plus Environment


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elongatus was very similar to that seen in samples of PSII isolated from both higher plants (spinach) as well as the cyanobacteria Synechosytstis sp. PCC6803, illustrating the high structural homogeneity of the OEC.40,46,56 Table 4 shows calculated 14N HFC as well as nuclear quadrupole coupling constants for the

Ca models studied in this work. At the present time no information is available regarding the potential sign of the isotropic HFC. Although computationally the sign of the calculated 14N isotropic HFC is dependent on the sign of the projection coefficient of MnD. As a result of the dominant spin polarisation, Aiso is positive when the MnD spin is down and negative when the MnD spin is found to be up. Comparing the calculated and experimental 14N EPR parameters shows that all models produce an isotropic HFC that is in good agreement with that found from experiment. This is due to the spin projection coefficients for MnD in all the models being similar. As a result of this it is expected that all models produce an isotropic HFC value that agrees well with the experimental HFC. Turning to consider the anisotropic HFC, it can be seen from Table 4 that in particular model Ca-1 produces anisotropic HFCs, which are in excellent agreement with those determined from experiment. The other Ca model results shown in Table 4 show anisotropic HFCs which are in poorer agreement with those determined from experiment. Early ESEEM experiments typically simulated the EPR spectra using axially symmetric HFC tensors;38,40 however more modern measurements have found rhombic HFC tensors.16,56 The calculations presented here would support the finding of rhombic tensors for these HFCs.

Table 4. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 14N hyperfine couplings and nuclear quadrupole couplings for the investigated Ca models studied and comparison with experimental data. All values are given in MHz. Ca-1 Ca-2

Aiso −6.08 −5.55

T1 −1.41 −1.18

T2 0.18 0.30 14

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T3 1.23 0.88

e2Qq/h η −1.56 0.68 −1.71 0.54

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Ca-3 Ca-4 Exp.56*

−5.99 −6.12 |6.95|

−1.16 −1.11 −1.50

0.25 0.32 0.20

0.92 0.79 1.30

−1.54 −1.48 −1.98

0.63 0.78 0.82

* Similar experimental values have been reported in references 16,91

The calculated nuclear quadrupole coupling constant e2Qq/h is found to be slightly lower than the experimental value in all Ca models but is similar to those previously found for superoxidised manganese catalase or other imidazole nitrogen atoms that are coordinated to metal centres.55,92 The asymmetry parameter η is also found to be under calculated. The experimental asymmetry parameter of 0.82 is larger than that found in the superoxidised manganese catalase or other metal-coordinated imidazole ligands.92 It should be noted that the uncertainties in the asymmetry parameter in the ESEEM simulations are found to be considerably larger than those for the nuclear quadrupole coupling constant. A good example of this is the MnIII coordinated histidine in two different manganese catalase samples (purified from Lactobacillus plantarum and Thermus thermophilus), the measured asymmetry values were found to disagree significantly although the nuclear quadrupole coupling constants were found to be very close to each other.92

Table 5. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 14N hyperfine couplings and nuclear quadrupole couplings (in MHz) for the investigated Sr models studied and comparison with experimental data. Sr-1 Sr-2 Sr-3 Sr-4 Exp.86

Aiso −6.0 −5.8 −5.9 −6.1 |7.3|

T1 −1.3 −1.1 −1.1 −1.2 −1.4

T2 0.1 0.2 0.3 0.3 0.1

T3 1.1 0.9 0.8 0.9 1.2

e2Qq/h −1.72 −1.88 −1.79 −1.72 |1.98|

η 0.93 0.75 0.88 0.72 0.79

Comparing the calculated and experimental 14N EPR parameters for the Sr models shown in Table 5 allows additional insight into the electronic structure of the strontium substituted OEC. It can be seen that in a similar fashion to the Ca models, all the Sr models produce isotropic HFCs which are found to be close to the reported experimental HFC. The



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anisotropic HFC tensors of model Sr-1 were found to agree very well with those determined from experiment. However as was seen when studying the Ca models, the remaining Sr models anisotropic HFCs were found to be in poorer agreement with the experimental values. The calculated nuclear quadrupolar coupling constant is found to be calculated in good agreement for all Sr models and is actually calculated in better agreement with experimental data than the Ca models. Comparing the asymmetry parameter with the experimental value shows an improvement over the Ca model data, although Sr-1 and Sr-3 produce asymmetry values which are over calculated. Studying the

Ca-1 and Sr-1 models appears to support the earlier findings that substitution of the calcium ion with strontium does not significantly perturb the electronic structure of the MnD ion and by extension the tetranuclear manganese cluster, as there is very little difference between the calculated isotropic and anisotropic HFCs or in the nuclear quadrupole coupling constants. From the analysis of the 55Mn and 14N HFCs above, we can confidently rule out the -2 and

-3 models which contain W1 as a hydroxo group and will confine our further analysis to the -1 and -4 models. 17

O Hyperfine Couplings

Rapatskiy et al. performed W-band ELDOR detected NMR on

17

O labelled PSII samples

and found three classes of signal in the spectra which were termed strong, intermediate and matrix.16 The strong signal was found to have an isotropic HFC of magnitude 9.7 MHz and was experimentally assigned to a µ-oxo bridging oxygen on the basis of HFCs previously measured for a MnIIIMnIV µ-oxo bridged model complex.16,93 In addition Rapatskiy et al. used the relative orientations of the

14

N and

17

O experimental hyperfine tensors to assign

the exchangeable µ-oxo bridging HFC to either O4 or O5, although subsequent 16 ACS Paragon Plus Environment

14

N

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experiments by Lohmiller et al. found there to be disagreement between the

14

N datasets

questioning this assignment.16,86 The intermediate signal produced an isotropic HFC value of magnitude 4.5 MHz and was assigned to one or both of the terminal water ligands of MnA. The matrix class of signal was found to possess an isotropic HFC value of magnitude 1.4 MHz and assigned to weakly coupled matrix waters (either manganese or calcium coordinated).16 Bridging atoms currently highlight a problem in the spin projection techniques currently used to calculate hyperfine couplings for BS-DFT calculations. Non-bridging ligand nuclei are normally spin projected using the spin projection coefficients of the metal ion they are coordinated to. For bridging nuclei a number of solutions have been proposed. The first is to simply average the two projected hyperfine couplings,94,95 while an alternative approach is to sum the spin projections.96 From our investigations

of

several µ-oxo bridged

manganese complexes (see Tables S2 and S3 in Supporting Information) and the results of Rapatskiy et al. we conclude that the second spin projection technique produces results in better agreement with experiment.96 A comparison of calculated and experimental

17

O

HFCs obtained for the Ca-1 and Ca-4 models is shown in Table 6.

Table 6. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 17O hyperfine couplings (in MHz) for the investigated Ca models and comparison with experimental data.

Ca-1

Ca-4

Label W1 W2 O1 O2 O3 O4 O5 W1 W2 O1 O2 O3

Aiso −1.4 −5.5 0.2 6.0 7.3 1.6 −10.3 −1.7 0.3 0.9 7.0 7.9

T1 −1.2 −1.1 −18.9 −24.6 −12.9 −27.0 −18.6 −0.9 −1.0 −20.7 −19.9 −22.8 17


T2 0.5 0.4 −2.9 −7.5 −1.1 7.8 −10.8 0.4 0.3 −1.4 −7.6 3.4

T3 0.7 0.7 21.8 32.1 16.1 19.2 29.4 0.5 0.7 23.2 27.5 26.2


O4 O5 Exp.16

−0.4 −7.7 |9.7| |4.5| |1.4|

−13.2 −12.1 4.5 1.2 1.2

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−6.3 −3.5 -1.0 −0.5 −0.6

19.5 15.6 -3.4 −0.6 −0.7

Considering first the calculated results for the µ-oxo bridging atoms (O1 through to O5) the model Ca-1 produces isotropic HFCs in the range of 0−10 MHz. The calculated isotropic HFC for O5, -10.3 MHz agrees very well with the experimental value of |9.7| MHz supporting the experimental assignment made, by Rapatskiy et al.16 The calculated anisotropic magnitude is however significantly larger than the experimental determination reported for O5. The isotropic HFCs for the manganese bound W1 and W2 calculated for

Ca-1 are also in very good agreement with the isotropic HFC magnitudes reported for the intermediate and matrix signals. In addition the magnitude of the anisotropic HFCs, for both W1 and W2 in the Ca-1 model, were found to agree very well with those determined from experiment. The calculated isotropic HFCs for the model Ca-1 also correspond well with those reported by Rapatskiy et al. (4.7 and 1.5 MHz respectively).44 Here agreement between theory and experiment is much better for the Ca-1 model compared with Ca-4 which again adds further support to this model of the OEC in the S2 state. The calcium bound waters W3 and W4 are expected to display only small HFCs owing to the absence spin on the calcium ion. The isotropic and anisotropic HFCs for the Sr models are given in Table S12 of Supporting Information and are similar to those calculated for the Ca models. 1

H Hyperfine Couplings

Table 7 shows selected 1H HFC calculated for the Ca cluster models as well as recent HYSCORE data for the native OEC. The spectra reported by Milikisiyants et al. for the 18 ACS Paragon Plus Environment

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native OEC showed a number of signals HI – HV originating from interacting protons.91 Milikisiyants et al. assigned the HI and HIII group of protons to fully protonated water molecules, W1 and W2 directly ligated to MnA of the OEC. The HII proton group was assigned to the proximal protons of the D1-His-332 residue. The remaining detected proton signals were attributed to non-specific matrix proton interactions. Considering the calculated results for model Ca-1, Table 7, it can be seen that the W1 protons HA and HB produce isotropic and anisotropic HFCs in good agreement to those observed for the HI group of protons, with particular good agreement for HB of W1. Although the two W1 protons would be expected to be equivalent in an isolated system, the hydrogen bonding interaction between Asp-61 and HA lowers the calculated Aiso and T value. Similar behaviour is observed in experimental and computational studies of ammonia inhibition of the OEC, where ammonia has been to found to replace W1 and hydrogen bond to the Asp-61 residue.97,98 The Ca-1 model also gives isotropic and anisotropic HFCs for the W2 HC hydroxide proton in very good agreement with the experimental results found for the HIII proton group. This result differs with the experimental interpretation of Milikisiyants et al. who interpreted the HIII proton signal as arising from a fully protonated W2 water and not a hydroxide group. This interpretation was due to the observed Aiso values showing agreement to previously published 2D 1H HYSCORE spectra of a water ligated dimanganese model complex.48,99 It was speculated that a hydroxo group would give rise to a much larger isotropic HFC but this is not bourne out by our calculated values. The calculated results for Ca-4 model where W2 is a water ligand are not in as good agreement with the experimental value, lending extra support for the hydroxo nature of W2 in the S2 state as already found above. The assignment of the experimentally observed HII protons to the ring protons of the proximal D1-His332 residue



Page 20 of 33

is also supported by our calculations. Both protons have small calculated isotropic and larger anisotropic T values close to the experimental value.

Table 7. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 1H hyperfine couplings (in MHz) for the investigated Ca-1 and Ca-4 models and comparison with experimental data. T is defined as T = (T1 + T2)/2 = −T3/2

Ca-1

Ca-4

Exp.48

Label W1 HA W1 HB W2 HC W2 HD His HE His HF W1 HA W1 HB W2 HC W2 HD His HE His HF HI HII HIII HIV HV

Aiso 1.0 1.7 3.0 − 0.1 −0.8 0.7 1.6 1.0 1.3 0.1 −0.9 |1.8| |0.1| |2.6| |0.2| |0.4|

T1 −3.9 −5.0 −2.0 − −5.0 −4.2 −2.5 −3.6 −2.5 −2.5 −5.6 −4.7 − − − − −

T2 −2.7 −4.3 −1.7 − −1.1 −2.9 −1.6 −3.2 −2.1 −2.1 −1.2 −3.3 − − − − −

T3 6.6 9.3 3.8 − 6.2 7.1 4.1 6.8 4.6 4.6 6.8 8.0 − − − − −

T −3.3 −4.6 −1.9 − −3.1 −3.6 −2.0 −3.4 −2.3 −2.3 −3.4 −4.0 |4.4| |4.1| |1.9| |2.3| |1.4|

Table 8 shows the calculated 1H isotropic and anisotropic HFCs for the Sr models in addition to HYSCORE data from experimental studies of the Sr substituted OEC. Unlike the native OEC, Chatterjee et al. only found a single signal, HI, originating from direct ligation to the OEC.

100

This signal was found to have similar isotropic and anisotropic

HFCs to that seen in the native OEC and assigned to the ring protons of the D1-His-332 residue. In contrast to the native OEC, Chatterjee et al. could find no significant HFCs signals originating from either the W1 or W2 protons leading them to conclude that Sr substitution results in a strongly disordered geometry for these water ligands that perturbs these groups and causes a large modification in their HFCs.

100

The BS-DFT calculated

HFCs for the Sr models are very similar to the native form and would be expected to occur at similar positions in the experimental spectra. No significant perturbation of W1 and W2


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are observed in our models as was also found in the Sr OEC X-ray crystal structure. As can be seen in Table 8, the isotropic and anisotropic HFCs calculated for both the W1 protons (HA and HB) and the W2 hydroxo proton (HC) are similar to those calculated for the Ca-1 analogue model. These calculations in conjunction with those presented earlier would suggest that Sr substitution has little or no effect on the calculated HFCs of the W1 and W2 groups. We suggest therefore that the lack of detection of experimental signals for the W1 and W2 protons in Sr substituted OEC is due to a detection limitation rather than a major change in value introduced by Sr substitution.

Table 8. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 1H hyperfine couplings (in MHz) for the investigated Sr-1 and Sr-4 models and comparison with experimental data. T is defined as T = (T1 + T2)/2 = −T3/2

Sr-1

Sr-4

Exp.100

13

Label W1 HA W1 HB W2 HC W2 HD His HE His HF W1 HA W1 HB W2 HC W2 HD His HE His HF H1 HII HIII

Aiso 1.0 1.5 3.2 − 0.0 −0.7 0.9 1.7 0.8 1.8 0.1 −0.8 ~0 |0.2| |0.2|

T1 −4.0 −4.3 −2.3 − −4.5 −4.3 −2.4 −3.8 −2.3 −2.7 −5.1 −4.1 − − −

T2 −2.7 −4.0 −1.5 − −0.8 −3.0 −1.6 −3.0 −1.8 −1.2 −1.2 −3.3 − − −

T3 6.7 8.3 3.7 − 6.2 7.3 3.9 6.7 4.1 3.9 6.3 7.4 − − −

T −3.4 −4.2 −1.9 − −3.1 −3.6 −2.0 −3.4 −2.1 −2.0 −3.2 −3.7 |4.1| |2.2| |1.5|

C Hyperfine Couplings

Stull et al. used ENDOR spectroscopy to study the S2 state in a PSII preparation where all alanine carboxylate carbons were 13C labelled as well as a scenario where all carbon atoms were uniformly 13C labelled. These results were then compared to a bridging carboxylate in a synthetic dinuclear MnIIIMnIVcomplex.57 These results, published before the 2011



Page 22 of 33

Umena et al. crystal structure,10 led to the conclusion that the D1 polypeptide alanine Cterminus is directly bound to a manganese ion. In the simulations of the ENDOR spectra, Stull et al. were required to make a number of assumptions in order to interpret the experimental spectra, namely the dipolar hyperfine couplings were estimated using the point dipole approximation from the various X-ray structures available at the time (provided by Loll et al., Guskov et al. and Ferreira et al.).13,101,102 Table 9 summarises the computational results obtained for the Ca models studied, in comparison with the experimental data. For carboxylates which bridge two manganese sites, we have utilised the same spin projection technique used above for spin projecting bridging oxygen nuclei; the intrinsic hyperfine coupling tensors are spin projected to both of the two manganese sites and them summed. In the case of terminal or Mn−Ca bridging carboxylates, the

13

C

nuclei were spin projected to the directly bonded manganese site. In both the Loll et al. and Guskov et al. X-ray crystallographic structures, the alanine Cterminus of the D1 polypeptide chain was bonded to one manganese centre,101,102 unlike the Ferreira et al. crystal structure, which proposed the alanine C-terminus to be bonded only to the calcium atom of the OEC.13 The high resolution 2011 Umena et al. structure and 2014 XFEL structure of Suga et al. found the D1-Ala-344 residue to be bonded to both MnC and the Ca2+ ion of the OEC.10,11 Inspection of the data in Table 9 of the Ca-1 model shows that the Ala-344 residue provides an isotropic and anisotropic hyperfine coupling which is in good agreement with the experimental data. Additionally Stull et al. found that in the uniformly labelled sample there were multiple 13C containing moieties which produced hyperfine couplings similar to that observed for the Ala-344 labelled example.57 This observation is supported by the results shown in Table 9, as multiple residues in model Ca-1 provide similar isotropic and anisotropic hyperfine couplings (Asp-170 and Asp-342) within the joint uncertainties of 22 ACS Paragon Plus Environment

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computation and simulation. Schinzel et al 82 also previously compared BS-DFT calculated 13

C HFCs with the experimental values. This study was performed before the high

resolution crystal structure of the OEC was available which limited accurate assignment possibilities.

Table 9. Calculated spin projected isotropic (Aiso) and anisotropic (Ti) 13C hyperfine couplings (in MHz) for the investigated Ca models and comparison with experimental data.

Ca-1

Ca-4

Exp.57 a

Label Asp-61 Asp-170 Glu-189 Glu-333 Asp-342 Ala-344 Glu-354a Asp-61 Asp-170 Glu-189 Glu-333 Asp-342 Ala-344 Glu-354a

Aiso 0.0 1.3 2.1 2.6 −1.9 −1.6 −4.3 −0.0 1.6 3.0 1.3 −2.3 −1.7 −3.6 -1.0

T1 −0.2 −2.0 −1.3 −3.9 −4.5 −1.9 −2.6 −0.2 −1.4 −1.5 −2.4 −5.9 −1.7 −2.3 −2.4

T2 −0.1 −0.7 −1.1 0.2 −0.5 −0.7 0.3 −0.1 −0.1 −1.2 0.3 −0.4 0.8 0.4 −0.8

T3 0.3 2.6 2.4 3.7 5.0 2.6 2.3 0.2 1.5 2.7 2.2 6.3 0.9 1.9 3.2

Residue from the CP43 protein chain, all other residues from the D1 protein chain

13

C data for the Sr models are similar to the Ca models and are given in the Supporting

Information.

CONCLUSIONS In this study a thorough BS-DFT analysis of the OEC S2 state 55Mn and ligand hyperfine couplings was performed investigating the effects of altering the protonation states of the W1 and W2 ligands. In addition the effect of Sr substitution for Ca was investigated. Using large geometry optimised cluster models of high resolution dark adapted crystal structures, we show that slight changes in the structure as a result of altering the protonation state of the W1 and W2 oxygens had a profound effect on the calculated 55Mn 23 ACS Paragon Plus Environment


Page 24 of 33

HFCs. Such variations arise due to small changes in the Heisenberg exchange coupling constants which affect the spin projection coefficients. Comparison between experimental and calculated HFCs for both the native Ca OEC and Sr substituted form clearly show that W1 is present in the S2 state as a water molecule and W2 is present as a hydroxo. Substitution of the Ca for Sr has a minor effect on the calculated HFCs showing that the S2 electronic structure of the OEC is not significantly altered by this substitution. The ability to be able to distinguish between small structural differences such as protonation patterns using this combination of experimental and BS-DFT calculated EPR parameters demonstrates the unique ability of this combination of theory and spectroscopy to probe the OEC electronic structure. Such an analysis can now be confidently applied to the S3 state where it has been found that Ca/Sr substitution gives rise to large differences in its EPR properties. Probing the electronic origin of such differences can provide a key and unique insight into the final stages of the water oxidation cycle.

ACKNOWLEDGEMENTS NJB and TAC acknowledge support from the UK BBSRC Doctoral Training Partnership (DTP) program.

ASSOCIATED CONTENT Supporting Information Additional analysis and discussion of calculated exchange coupling constants, spin projection coefficients and hyperfine couplings mentioned in manuscript. Available free of charge at http://pubs.acs.org

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TOC Graphic

S2 Frontier Orbitals


Comparison between Experimental and Broken Symmetry Density

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