Comparison of Experimental and Broken Symmetry Density Functional

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A Comparison of Experimental and Broken Symmetry Density Functional Theory (BS-DFT) Calculated Electron Paramagnetic Resonance (EPR) Parameters for the Manganese Catalase Active Site in the Superoxidised Mn /Mn State III

IV

Nathan J. Beal, Thomas A. Corry, and Patrick J. O'Malley J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.7b11649 • Publication Date (Web): 22 Feb 2018 Downloaded from http://pubs.acs.org on February 25, 2018

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The Journal of Physical Chemistry

A Comparison of Experimental and Broken Symmetry Density Functional

Theory

(BS-DFT)

Calculated

Electron

Paramagnetic

Resonance (EPR) Parameters for the Manganese Catalase Active Site in the Superoxidised MnIII/MnIV State

Nathan J Beal, Thomas A Corry and Patrick J O’Malley* School of Chemistry, The University of Manchester, Manchester M13 9PL, UK E-mail: [email protected]

ABSTRACT Broken Symmetry Density Functional Theory (BS-DFT) g-tensor,

55

Mn,

14

N, and

17

O

hyperfine couplings have been calculated for active site models of superoxidised Mn(III)/Mn(IV) manganese catalase both in its native and azide inhibited form. While good agreement is found between calculated and experimental g-tensor and 55Mn hyperfine couplings for all models, the active site geometry and Mn ion oxidation state can only be readily distinguished based on comparison of calculated and experimental 17

14

N azide and

O HFCs. This comparison shows that only models containing a Jahn-Teller distorted 5-

coordinate Mn2(III) site and a 6-coordinate Mn1(IV) site, can satisfactorily reproduce the experimental 14N and 17O hyperfine couplings.

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Introduction Catalases provide the first line of defence against hydrogen peroxide and can be found in animals and plants as well as microbial life.1 The reactive oxygen species is common in nature and possess a wide variety of functions, e.g. as a cell signalling molecule, a cellular weapon or it may simply occur as a by-product of aerobic metabolism.2–4 In addition to the heme containing catalases found in animals and plants, nature uses another class of (nonheme) catalases, sometimes referred to as pseudocatalases, in various lactic acid bacteria.5 The manganese catalase (MnCat) enzymes studied here are in this second group of enzymes, which show weaker catalytic activity in comparison to the heme containing catalases.1 The MnCat enzyme has been extracted from the bacteria Lactobacillus plantarum (LP) as well as Thermus thermophilus (TT). Both enzymes have been comprehensively investigated using X-ray diffraction techniques at a resolution sufficient to reveal a binuclear manganese active site.6,7 The enzymes derived from the two different bacteria were found to be highly homologous concerning important structural characteristics.8 The complete MnCat protein consists of six subunits that form a homohexameric globular shell surrounding a central solvent filled space. The structure of MnCat extracted from LP can be seen in Figure 1 below.


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Figure 1. The MnCat enzyme structure of Lactobacillus plantarum , PDB entry 1JKU shown from a) side on and b) top down perspectives.6A single unit and its secondary structure are shown in c) with secondary structure colour coded as: αhelix (red), β-sheet (yellow) and turn (green). Manganese ions are depicted as purple spheres.

Five amino acid residues directly ligate the manganese atoms found in the active site of MnCat. The manganese atoms are connected via two µ-oxo bridging units along with a glutamic acid residue. An additional two glutamic acid residues and two histidine residues also coordinate the manganese atoms to complete the first coordination sphere of the active site. The structure of the MnCat active site in the resting (MnIII)2 oxidation state can be seen in Figure 2 for both the MnCat enzymes.



Figure 2 Structures of the MnCat active sites in the resting MnIIIMnIII state isolated from Lactobacillus plantarum (left) and Thermus thermophilus (right), structures extracted from PDB entries 1JKU and 2V8U respectively.6,7 Colour coding: manganese (purple), oxygen (red), nitrogen (blue) and carbon (grey). Hydrogen atoms are omitted for clarity.

In addition to the catalytically active oxidation states of (MnII)2 and (MnIII)2, a mixed valence state MnIIMnIII as well as a superoxidised MnIIIMnIV state may also be formed via the addition of various oxidising and reducing agents.9–11 The superoxidised MnIIIMnIV state of MnCat has received significant attention as it displays an S = 1/2 ground state, making it amenable to study via electron paramagnetic resonance (EPR) techniques.12–14 The EPR spectra of MnCat closely resembles the spectra seen when studying the oxygen evolving complex (OEC) in its S2 state, in agreement with the di-µ-oxo glutamate motif together with further glutamate and histidine ligation observed in both structures. As a result of this the superoxidised state has been studied using various experimental and theoretical techniques.15–21 The MnCat active site is found to possess the same effective S = 1/2 ground state spin as the OEC and also produces a comparable EPR spectrum, originating from the shared MnIIIMnIV structural motif found in both active sites. As a result of this the MnCat active 4 ACS Paragon Plus Environment

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site has received a considerable degree of attention owing to its usefulness as a naturally occurring model system and has consequently been studied using EPR spectroscopic techniques extensively.12–14,16,17,22,23 In sharp contrast to the more complicated case of the OEC, crystallographic data concerning the MnCat enzyme has been available in the literature for the better part of two decades which has allowed the MnCat active site to be investigated at great length.6,7 The large number of experimental EPR studies performed on MnCat have been supported by a smaller number of computational investigations. BS-DFT studies Sinnecker et al.,19,24 and Schraut et al.

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of

were performed on small model systems of the

active site and provided encouraging results concerning various structural features and prediction of EPR parameters. The current study is concerned with a more in depth and detailed analysis. Large model systems developed from the crystal structures of MnCat isolated from Lactobacillus plantarum and Thermus thermophilus are used. In addition to

g-tensor and 55Mn HFC calculations, 14N, and 17O HFCs are calculated and analysed with reference to experimental determinations. In addition azide inhibited models are also investigated. This combination leads us to definitively assign the correct oxidation states for the two Mn ions present in the active site overturning previous assignments based on experimental investigations alone. The findings clearly demonstrate the power of combining BS-DFT calculated and experimental EPR parameters to uniquely probe the detailed electronic structure of multi-transition metal enzyme active sites. A preliminary account of this study has been reported.26

Computational Details All calculations were performed using ORCA version 3.0.3.27 All model systems have been geometry optimised in the high spin (Ms = 7/2) and the broken symmetry (Ms = 1/2)



states at the DFT level using the BP86 functional,

28,29

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utilising the zeroth-order regular

approximation (ZORA) Hamiltonian to include scalar relativistic effects.30–32 ZORA adapted segmented all-electron relativistically contracted (SARC) basis sets were employed for all atoms,33 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.34 The computational time of the calculations was decreased by invoking the resolution of identity approximation (RI) along with decontracted auxiliary def2-TZVP/J coulomb fitting basis sets.35–37 Little change between high spin and low spin geometries was found and only the high spin values are reported. The optimisations also included the third generation (D3) semi-empirical van der waals corrections proposed by Grimme.38,39 The conductor like screening model (COSMO) with a dielectric constant of ε = 8.0 was used for all calculations.40 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 the chain of spheres (RIJCOSX) approximation to exact exchange using the same decontracted auxillary basis sets that were used in the geometry optimization steps.41,42 Initial broken symmetry guesses were constructed using the ‘flipspin’ feature of ORCA.27 Calculation of the hyperfine and quadrupole tensors used basis sets developed by Neese et al. based on the SARC def2TZVP for the Mn, N and O atoms which contain fully decontracted s-shells with three additional steep primitives added to the core, in addition to this def2-TZVP(-f) was used for all other atoms.37,43 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


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constants were calculated using the Yamaguchi coupling scheme which consistently covers the whole range of exchange coupling situations from the strong to the weak exchange coupling limit.44 High spin geometries were used throughout for the exchange couling analysis. The calculated hyperfine couplings of the broken symmetry state were spin projected to give effective hyperfine couplings and g-values which can be directly compared with experimental determinations. Spin projection coefficients of 2 (MnIII) and 1 (MnIV) were employed. The calculated

55

Mn isotropic hyperfine couplings were scaled

with an empirically derived factor of 1.47 to account for well known deficiencies in the DFT description of the Fermi contact term.24,45 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). The BS-DFT approach and the use of the TPSSh functional in the calculations of Heisenberg exchange coupling constants in manganese systems has been discussed and compared to the performance of other functionals in earlier studies of manganese dimer systems.24,43,46 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 were constructed using starting coordinates from three different crystal structures of manganese catalase. These are native forms 1JKU (Lactobacillus plantarum, LP), 2V8U (Thermus thermophiles, TT), and azide inhibited LP, 1JKV.6,7 The labelling and numbering scheme used is shown in Figure 3. The LP models (both native and inhibited) are designated 1 and TT models 2. A second label is used to distinguish the Mn (III/IV) oxidation state assignment: A (native) and C (azide) refers to oxidation states Mn1(IV)Mn2(III); B(native) and D (azide) refer to Mn1(III)Mn2(IV). Additionally for both



1A and 2A forms a hydroxo ligand instead of water for O6 is designated 1A(OH) and 2A(OH). The models and numbering scheme used are shown below in Figure 3.

Figure 3 Numbering scheme used for (1A, 1A(OH), 1B, 2A, 2A(OH)) and azide inhibited (1C and 1D) cluster models.

All models comprised the directly coordinated amino acid residues as well as the accompanying water/hydroxide group at the O6 position or an azide group at this position in the case of models 1C and 1D. All the amino acid residues were truncated at the αcarbon position. No B minima were found for the models constructed from the TT crystal structure, 2, i.e. only oxidation state distribution Mn1(IV)Mn2(III) was found. All model


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structures investigated are shown in Figure 4. During geometry optimisation all terminal heavy atoms are constrained at their crystallographic position.

Figure 4 Model active site structures used, see text for details. Colour coding: manganese (purple), oxygen (red), nitrogen (blue), carbon (grey) and hydrogen (white).

Results and Discussion Our analysis begins with the calculated optimised geometries for the models as well as considering the Heisenberg exchange coupling constants for each model. Following this calculated EPR parameters will subsequently be analysed, commencing with the g-tensor and the

55

Mn hyperfine coupling parameters. The nuclear quadrupolar couplings and

hyperfine couplings for several ligating nuclei (14N, 17O) are then presented and analysed. 9 ACS Paragon Plus Environment


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Geometries The MnCat active site is believed to remain structurally intact when the resting MnIIIMnIII state is oxidised to form the superoxidised state.15,19 Tables 1 and 2 feature an overview of selected calculated optimised interatomic bond lengths for the MnCat models and the azide inhibited MnCat models respectively. As a result of the MnIV ion being present in the active site models, the superoxidised state features a shorter Mn−Mn distance to that seen in the crystallographic MnIIIMnIII structures. All of the model systems in Tables 1 and 2 replicate this experimental observation. The MnCat models studied here produce bond lengths in good agreement with the earlier BS-DFT results of Sinnecker et al.19 It can be seen that the location of the MnIII ion has a profound effect on other bond lengths of the active site models. This effect is perhaps best demonstrated by the bond lengths to the water group (O6) at the Mn1 site and to the O8 atom at the Mn2 site for the MnCat model systems. The bond to the water molecule is lengthened by 0.35 Å on going from model 1A to 1B, while the bond to O8 decreases by approximately 0.5 Å. This leads to a sixfold coordination geometry for both the manganese ions in 1B, whereas the bond from Mn2 to O8 is non-existent for all other models resulting in the Mn2 site being fivefold coordinated in models 1A, 1A(OH), 2A and 2A(OH). Table 1. Interatomic bond lengths (Å) of the MnCat cluster models compared to available experimental data.

Bond

1A

1A(OH)

1B

2A

2A(OH)

EXAFS17

Mn1 − Mn2 Mn1 − O1 Mn1 – O2 Mn2 – O1 Mn2 – O2 Mn1 – O3 Mn1 – O5 Mn1 – O6 Mn2 – O4 Mn2 – O7 Mn2 – O8

2.71 1.82 1.79 1.86 1.82 1.92 2.03 2.00 2.19 2.00 2.49

2.70 1.82 1.81 1.85 1.81 2.04 2.02 1.84 2.22 2.04 2.45

2.70 1.87 1.85 1.80 1.77 2.19 1.98 2.35 1.94 2.09 2.01

2.68 1.79 1.77 1.86 1.82 1.97 2.09 2.00 2.16 1.98 2.75

2.67 1.82 1.78 1.83 1.81 2.05 2.06 1.83 2.15 2.01 2.69

2.70* ~1.81 ~1.81 ~1.81 ~1.81 ~2.10 ~2.10 ~2.10 ~2.10 ~2.10 ~2.10


Cryst. Struct.a6,7 3.03/3.09 2.06/2.05 1.91/2.03 2.22/2.18 1.98/2.12 2.11/2.13 1.85/2.10 2.10/2.27 2.10/2.14 2.41/2.18 2.38/2.63

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Mn1 − N1 Mn2 – N2

2.10 2.10

2.13 2.12

2.08 2.13

2.14 2.12

2.15 2.12

~2.10 ~2.10

2.17/2.28 2.16/2.26

a

For the crystal structure data, the first column refers to Lactobacillus plantarum (1JKU) data and the second column corresponds with crystal structure data from Thermus thermophilus (2V8U). *A smaller value of 2.67 Å has also been reported by Waldo et al.47

Similarly for the azide inhibited MnCat models this behaviour is well illustrated by the bond lengths to the azide (N5) at the Mn1 site and the O7 atom at the Mn2 site. The Mn−azide bond increases by 0.15 Å on going from model 1C to 1D while the Mn−O7 bond decreases roughly by 0.5 Å. Similar coordination pattern behaviours can also be seen in 1C and 1D, with 1D displaying six-fold coordination at both Mn sites and 1C showing fivefold coordination at the Mn2 site. The observation of both mono- and bidentate binding patterns of the terminal Glu residue coordinated to the Mn2 site leading to the A and B (similarly C and D) assignments has been reported previously from molecular dynamics simulations.48 In all of the studied models the Jahn-Teller axis of the MnIII ion was found to be aligned perpendicular to the µ-oxo bridges, a finding that is in good agreement with earlier studies of MnCat and many synthetic mixed valence MnIIIMnIV dimer complexes.19,46 For the azide models this is in disagreement with the experimental interpretation of Coates et al.,14 where the azide nitrogen was assigned as a ligand to MnIII in an equatorial position based on its EPR parameters. Table 2. Interatomic bond lengths (Å) of the azide inhibited MnCat cluster models compared to available experimental data.

Bond Mn1 − Mn2 Mn1 − O1 Mn1 – O2 Mn2 – O1 Mn2 – O2 Mn1 – O3 Mn1 – O5 Mn2 – O4 Mn2 – O6 Mn2 – O7 Mn1 − N1 Mn2 – N2 Mn1 – N5

1C 2.72 1.81 1.82 1.85 1.81 1.99 1.99 2.22 2.03 2.43 2.14 2.14 1.98

1D 2.74 1.87 1.87 1.80 1.77 2.37 1.98 1.94 2.12 2.01 2.19 2.18 2.13

EXAFS17 2.73 ~1.81 ~1.81 ~1.81 ~1.81 ~2.04 ~2.04 ~2.04 ~2.04 ~2.04 ~2.04 ~2.04 ~2.04


Cryst. Struct.6 3.17 2.15 2.00 2.11 2.11 2.13 1.88 2.11 2.32 2.36 2.26 2.23 2.16


In energy terms, the sixfold coordinated structure of 1B was found to be marginally preferred by 3.9 kcal mol−1 compared to model 1A (cf. 3.5 kcal mol−1 found by Sinnecker et al.). A type B minimum structure could not be found for the 2V8U starting coordinates. For the azide inhibited models, 1D was found to be favoured over 1C by 7.9 kcal mol−1.

Heisenberg Exchange Coupling Constants The Heisenberg exchange coupling constants, J were calculated for all the models studied. The largest value of −93 cm-1 was found for model 1B with model 1A producing a similar exchange coupling value of −85 cm-1. The Heisenberg exchange coupling constant for model 1A(OH) was found to be slightly smaller than these with a J value of −71 cm-1. The 2A model was found to have a J value of −91 cm-1 and 2A(OH) produced a J value of −79 cm-1. For the azide inhibited MnCat, 1C produced a J value of −84 cm-1 with 1D being found to have a J value of −86 cm-1. The Heisenberg exchange coupling constants calculated in this work were found to be in good agreement with the earlier findings of Sinnecker et al.19 An upper limit to the Heisenberg exchange coupling constant for the superoxidised state of MnCat has been estimated to be no greater than −175 cm-1, on the basis of temperature dependent magnetisation measurements of the two pH dependent MnIIIMnIII states.49 However it is widely believed in the literature that the actual J value is significantly smaller than this, due to many studies on MnIIIMnIV inorganic complexes such as [(dtne)Mn2(µ-O)2(µ-OAc)(BPh4)2] and [(tacn)Mn2(µ- O)2(µ-OAc)(BPh4)2] (J = −110 cm-1 for both complexes (where dtne = 1,2-bis(4,7-dimethyl-1,4,7-triazacyclonon-1yl)ethane and tacn = 1,4,7-triazacyclononane )) which both possess the same core structure seen in MnCat.50–52


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Effective g-Tensor In stereotypical di-µ-oxo bridged MnIIIMnIV complexes the orientation of the effective gtensor with respect to the active site structure is shown in Figure 5. The orientation of the z-component is typically assumed to be parallel to the MnIII ion Jahn-Teller axis, which is perpendicular to the Mn2O2 core structure. The x- and y- component orientations are subsequently assumed to lie on the Mn2O2 plane. The components x and y might only be resolved in single-crystal experiments. The components of both metal hyperfine tensors are assumed to display the same characteristic orientation behaviour.53

Figure 5. Simplified structure of the MnCat µ-oxo core illustrating the experimentally assumed orientation of the g-tensor components with respect to the structure of the core complex.

Calculated g-tensors for all MnCat cluster models are presented in Table 3. On a qualitative level, all models show a similar pattern, where g11, the smallest component, corresponds to the unique z-component of the standard assignment seen in experiments (see Figure 5). The remaining two components are approximately equal.



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Table 3. Calculated Spin Projected g-tensors for the MnCat cluster models compared to available experimental data.

giso g11 g22 g33

1A 1.9968 1.9824 2.0030 2.0048

1A(OH) 1.9985 1.9872 2.0032 2.0050

1B 1.9962 1.9815 2.0030 2.0042

2A 1.9973 1.9823 2.0039 2.0056

2A(OH) 1.9993 1.9878 2.0043 2.0059

Exp.12 1.9988 1.9876 (z) 2.0040 (y) 2.0048 (x)

The calculated g-tensors for the azide inhibited MnCat model systems are given in Table 4. The g-tensors for the models 1C and 1D display a similar pattern to the uninhibited manganese catalase model systems. The smallest component g11 correlates to the unique zcomponent and the remaining components being found to be almost equivalent resulting in an approximately axial g-tensor. Table 4. Calculated Spin Projected g-tensors for the azide inhibited MnCat cluster models compared to available experimental data

giso g11 g22 g33

1C 1.9996 1.9862 2.0026 2.0053

1D 1.9967 1.9768 2.0016 2.0043

Exp.17 − 1.994(∥) 2.008(⊥) 2.008(⊥)

Figure 6 shows the calculated orientations of the effective g-tensor for all MnCat cluster models studied in this work. It can be seen that the orientation of the effective g-tensor varies only slightly with the model system. All of the model systems studied provide a good agreement with the experimental assumption (Figure 6) with the g11 component being parallel with the MnIII Jahn-Teller axis and the two nearly degenerate perpendicular components of the tensor being found to lie in the Mn2O2 plane, perpendicular to g11.


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Figure 6. The orientation of the calculated g-tensors relative to the core structure for all MnCat and azide inhibited MnCat cluster models studied in this chapter. Colour coding: manganese (purple), oxygen (red), nitrogen (blue). 55

Mn Hyperfine Couplings

The 55Mn hyperfine coupling constants (HFCs) for the MnCat model systems are shown in Table 5. In general good agreement of the MnIV HFC with experimental data is observed for all models with the isotropic HFC slightly lower than the experimental value in all models. Anisotropic HFCs match the experimental data set well although are again found to be lower than the reported experimental values. The calculated MnIII HFCs for all models match the experimental data very well, although the isotropic HFC is found to be slightly lower than the experimental result for all models apart from model 1B where it is higher than the experimental value. The anisotropic MnIII HFCs match the experimental 15 ACS Paragon Plus Environment


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data set very well. All components of the MnIII tensor are calculated to be larger than the experimental values, with all models showing the overall tensor being close to axial. Table 5. Calculated Spin Projected experimental data.

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Mn hyperfine couplings (in MHz) for MnCat models compared to available

MnIII 1A 1A(OH) 1B 2A 2A(OH) Exp.(LP)16 Exp.(TT)13

Aiso −353 −340 −404 −327 −308 −387 −382

T1 −56 −55 −58 −55 −54 −37 −52

T2 −49 −49 −50 −49 −49 −37 −30

T3 105 105 108 103 103 75 82

Aiso 227 229 222 227 226 235 237

MnIV T1 T2 −7 1 −8 −4 −4 −1 −8 3 −8 −6 −8 −8 −13 −5

T3 6 13 6 5 14 15 18

For the azide inhibited MnCat model systems, the calculated and experimental 55Mn HFC are shown in Table 6. From this table, reasonable agreement between the calculated and experimental MnIV HFCs can be seen for both models 1C and 1D with the isotropic and anisotropic HFCs being slightly better for model 1C when compared to model 1D. For the MnIII centre, the isotropic HFC for 1C is calculated to be lower than the experimental value conversely the isotropic HFC of 1D is higher than experiment. Similar to the uninhibited models the anisotropic HFCs are slightly larger than experiment for both models. Table 6. Calculated Spin Projected available experimental data.

55

Mn hyperfine couplings (in MHz) for azide inhibited MnCat models compared to

MnIII 1C 1D Exp.(LP)17

Aiso −347 −465 −375

T1 −58 −65 −35

T2 −45 −38 −35

T3 104 103 71

Aiso 229 221 230

MnIV T1 T2 −8 −4 −2 −1 −7 −7

T3 12 3 14

The experimental values are reported in most circumstances solely for MnCat samples from Thermus thermophilus. Experimental values for samples of Lactobacillus plantarum are only reported by Haddy et al.,16,17 and involve a simulation of the EPR spectra that assumes an ideal axial tensor (Table 5 and Table 6). As a result of this the experimental results for Lactobacillus plantarum are likely to be less accurate than the results obtained


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using modern EPR techniques, Teutloff et al.13 Agreement between calculated values and experimental determinations is reasonable in all cases but it is not possible to distinguish between the different Mn oxidation state models based on the 55Mn HFCs analysis alone. 14

N Hyperfine and Nuclear Quadrupole Couplings

Additional insight can be gained by analysing the

14

N HFC which arises from histidine

nitrogen atoms coordinating directly to the manganese spin centres, Figures 3 and 4. ESEEM studies performed on both of the MnCat enzymes from both Lactobacillus plantarum and Thermus thermophilus have reported HFCs and NQCs for the two histidine nitrogen atoms directly coordinated to the MnIII and MnIV ions in the uninhibited MnCat.20 A comparison of these experimental and calculated nitrogen EPR parameters can be seen in Table 7. For the nitrogen atom bound to MnIV, general good agreement is observed for all the calculated isotropic couplings. The model 2A(OH) provides a value which is lower than experimentally observed although does produce anisotropic and nuclear quadrupole couplings in good agreement with the experimental values. The overall agreement between the experimental and calculated values for the MnIV coordinated nitrogen is satisfying. Considering the MnIII coordinated nitrogen, the calculated isotropic couplings are found to be lower than the experimental values. Good agreement is found for the anisotropic values however. An underestimation of the calculated isotropic 14N HFC has been reported for the histidine ligand coordinated to manganese in the OEC previously.54,55 Table 7. Calculated Spin Projected 14N hyperfine couplings and nuclear quadrupole couplings (in MHz) for MnCat models compared to available experimental results. 14

1A 1A(OH) 1B 2A 2A(OH)

Aiso −4.59 −4.11 −4.29 −4.31 −4.3

T1 −0.64 −0.73 −0.73 −0.66 −0.71

N-MnIII T2 T3 e2Qq/h −0.50 1.15 −1.86 −0.54 1.27 −2.11 −0.53 1.25 −1.90 −0.49 1.14 −1.91 0.59 0.96 −2.13

14

η 0.90 0.70 0.85 0.82 0.64


Aiso 3.02 2.67 2.65 2.53 1.91

T1 −0.35 −0.45 −0.38 −0.40 −0.52

N-MnIV T2 T3 e2Qq/h 0.16 0.19 −1.72 0.17 0.27 −2.08 0.15 0.23 −1.78 0.15 0.25 −1.93 0.20 0.32 −2.17

η 0.95 0.64 1.00 0.78 0.59


Exp.(LP)20 −5.75 −0.60 −0.20 0.80 Exp.(TT)20 −5.20 −0.70 −0.30 1.00

2.01 2.25

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0.79 2.67 −0.57 0.16 0.41 0.65 2.28 −0.70 0.28 0.42

2.25 2.29

Similar experimental values have been reported by Coates et al.14

Comparing the calculated and experimental

14

N EPR parameters for the azide inhibited

MnCat models 1C and 1D as seen in Table 8, allows us to make a clear distinction between the oxidation state assignments of Mn1 and Mn2 respectively. By comparing the calculated HFC data for the models 1C and 1D, it can be seen that 1C gives a unique agreement with the experimental HFC data for the azide nitrogen. In model 1D where the azide ion binds to the Mn1III, the 14N isotropic HFC of 14.7 MHz far exceeds the experimentally observed value of 2.5 MHz for the azide nitrogen. In contrast 1C produces a HFC value in much better agreement with the experimental HFC. Thus a Mn oxidation state assignment Mn1(IV)Mn2(III) is strongly indicated. It is possible that the large magnitude HFC value seen in 1D would preclude efficient nuclear state mixing needed for HYSCORE and may not be detectable. In this situation the observed experimental value may then correspond to the smaller isotropic HFC of the azide N6 or N7 atoms. However the calculated nuclear quadrupolar values (K2(3+ η2)) for both of these nitrogens are significantly removed from that observed experimentally and would not support this proposal. As seen in the uninhibited MnCat systems the histidine nitrogen isotropic HFCs were found to be lower than the experimental values. This is particularly the case for 1D, which produces calculated isotropic HFCs in poor agreement with experiment, providing another reason to reject the oxidation state assignment. Table 8. Calculated Spin Projected 14N hyperfine couplings and nuclear quadrupole coupling (in MHz) for azide inhibited MnCat models compared to available experimental results.

1C

1D

Label N1 N2 N5 N6 N7 N1

Aiso 2.96 −3.79 1.27 −0.55 −0.08 −0.21

T1 −0.35 −0.37 −0.36 −0.62 −1.67 −0.80

T2 0.14 −0.04 0.14 0.29 −0.06 −0.65


T3 0.21 0.42 0.22 0.33 1.72 1.45

K2(3+ η2)a 0.90 1.00 1.7 0.1 0.5 1.0

0.58 0.50

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Exp.14 a

N2 N5 N6 N7 His His Azide

2.0 14.7 1.2 1.4 3.50 6.40 2.50

−0.25 −1.30 −0.81 −2.17 − − −

0.05 −0.70 0.16 −0.18 − − −

0.20 2.00 0.64 2.35 − − −

1.0 1.3 0.1 0.3 1.00 0.90 1.60

K2(3+ η2) is a combination of the nuclear quadrupolar coupling constant (e2Qq/4ℏ) and the asymmetry parameter η.

The large magnitude of the calculated azide nitrogen HFC in 1D can be attributed to the Jahn-Teller axis which lies along the MnIII−N azide bond. This results in a large hyperfine interaction with the half occupied 3dz2 orbital. BS-DFT studies of mixed valence MnIIIMnIV dimers have observed similar behaviour for nitrogen nuclei lying along the Jahn-Teller axis of the MnIII ion.24 Additionally ENDOR studies of compounds containing such a coordination feature have shown a 14N HFC in the magnitude range of 9−13 MHz.56 These calculated HFCs provide a clear distinction between the models 1C and 1D and strongly indicate that the azide coordinates to MnIV rather than MnIII in disagreement with the experimental assignment.14 17

O EPR hyperfine Couplings

The MnCat active site possesses several oxygen atoms coordinating directly to the manganese spin centres. Only the bridged oxygens and the water or hydroxo ligand to Mn1 are exchangeable. Exploiting this, the HFCs of these exchangeable nuclei have been experimentally determined using 17O ENDOR experiments. These reported two classes of HFC, assigned to a bridging µ-oxo group and a substrate water on the basis of their respective exchange times and their measured HFC.21 Recently a series of oxygen bridged bimetallic manganese complexes (both biological and synthetic) were studied with multifrequency EPR techniques providing significantly different HFCs for the µ-oxo bridged oxygen compared to the earlier 17O exchange experiments.23



Page 20 of 28

A comparison between calculated and experimental 17O HFCs is shown in Table 9. While Table 9 also provides computed

17

O anisotropies, these have only been experimentally

determined for the bridging µ-oxo unit in the multifrequency studies of Rapatskiy et al.23 The bridging oxygen nuclei highlights a shortcoming in the contemporary spin projection methodology. Usually the ligand nuclei calculated raw EPR values are spin projected using the coefficients of the metal centre that they are coordinated to, however for bridging atoms this treatment is insufficient. At the present time, a number of solutions have been proposed. The first is to simply average the two projected hyperfine couplings,57,58 while an alternative approach is to sum the spin projections to arrive at the correct hyperfine interaction.23 Experience from studying several µ-oxo bridged manganese complexes (see Table S2 and S3 in Supporting Information) and the results of Rapatskiy et al. conclude that the second spin projection technique produces results in better agreement with experiment.23 The resulting calculated tensors should be considered with some caution as the spin projection methodology adopted needs further testing. Table 9. Calculated Spin Projected experimental data.

1A

1A(OH)

1B

1B(OH)

2A

Exp.

17

Label O1 O2 O6 O1 O2 O6 O1 O2 O6 O1 O2 O6 O1 O2 O6

O hyperfine couplings (in MHz) for MnCat models compared to available

Type bridge bridge MnIV bridge bridge MnIV bridge bridge MnIII bridge bridge MnIV bridge bridge MnIV bridge23 Water21

Aiso 3.5 5.6 2.4 −1.1 0.3 4.5 4.3 7.8 −18.1 6.9 7.6 2.9 0.2 1.8 3.2 5.2† 3.8

T1 −33.0 −38.3 −2.2 −30.0 −31.2 −10.3 −36.3 −44.6 −9.2 −42.2 −40.1 −1.9 −33.3 −33.9 −10.8 −10 −

T2 10.8 11.5 0.4 1.9 −0.7 −0.2 10.3 20.9 4.1 17.9 13.2 0.3 −1.7 2.7 0.2 7.5 −

T3 22.2 26.8 1.8 28.1 32.0 10.5 26.1 23.7 5.1 24.4 26.9 1.7 35.0 31.2 10.6 18.1 −

†An earlier ENDOR study by McConnell et al. reported an isotropic HFC of 13.0 MHz (bridge), see text for details.21


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The bridging µ-oxo nuclei display calculated isotropic HFCs in the range of 1−8 MHz, in disagreement with the larger measured coupling of 13 MHz by McConnell et al. but in better agreement with the results of Rapatskiy et al.21,23 The assignment made by McConnell et al. was supported by HFCs observed for dinuclear MnIIIMnIV complexes,59– 61

which featured only the µ-oxo bridging oxygens. Rapatskiy et al. have offered the

explanation that the 17O ENDOR profile measured in the earlier studies did not accurately represent the true isotopic coupling but instead represented the largest component of the hyperfine tensor with the other hyperfine tensor components being masked in the experiment due to line broadening effects.23 Most notably in terms of Mn oxidation state assignment, Model 1B finds a large magnitude HFC for the water molecule (O6) when it is coordinated to MnIII. In the A case where the water or hydroxo is ligated to the MnIV centre, the calculated HFC is found to be in substantially better agreement with the experimental result. This finding combined with the azide 14N HFC of the previous section is strong evidence supporting a Mn oxidation state assignment of Mn1(IV)Mn2(III). Comparing models for water (1A and 2A) and hydroxide [1A(OH) and 2A(OH)] ligation in Table 9, would indicate better agreement with the bridged HFC magnitude for the water ligated model. The magnitude of this coupling for the hydroxo forms is significantly lower than the experimental value with much better agreement being shown for the water ligand model. Our analysis therefore would indicate that active site is composed of a Mn1(IV)Mn2(III) Mn oxidation state with a water ligand to Mn1 in disagreement with previous assignments.14,19,21

Conclusions BS-DFT calculations performed on cluster models of the superoxidised MnIIIMnIV active site of manganese catalase in its native and azide inhibited form give rise to g-tensor and 21 ACS Paragon Plus Environment


hyperfine couplings in good agreement with experimental determinations. While a clear distinction between different models is not forthcoming from g-tensor and 55Mn HFCs both the azide 14N and 17O HFCs can clearly differentiate between the oxidation state of the two Mn ions of the active site. Comparison between calculated and experimental values shows that the oxidation state assignment is Mn1(IV)Mn2(III) in disagreement with previous experimental estimates. On oxidation of III/III to form the III/IV complex the 6-coordinate Mn1 site favours Mn(IV) whereas the extreme Jahn - Teller distorted five coordinate Mn2 site more readily accommodates the Mn(III) state. ACKNOWLEDGEMENTS NJB and TAC acknowledge support from the UK BBSRC Doctoral Training Partnership (DTP) program. ASSOCIATED CONTENT Supporting Information Data used to determine

55

Mn isotropic HFC scaling factor. Comparison of averaged and

summed spin projection methods for bridging 17O HFCs for model complexes. Available free of charge at http://pubs.acs.org

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TOC Graphic

Mn(IV)

Mn(III)


Comparison of Experimental and Broken Symmetry Density Functional

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