Metalloporphyrin–Nitroxyl Interactions: The Low ... - ACS Publications

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Metalloporphyrin−Nitroxyl Interactions: The Low-Energy States of Reduced Manganese, Iron, and Cobalt Porphyrin Nitrosyls Jeanet Conradie†,‡ and Abhik Ghosh*,† †

Department of Chemistry and Center for Theoretical and Computational Chemistry, UiT − The Arctic University of Norway, 9037 Tromsø, Norway ‡ Department of Chemistry, University of the Free State, 9300 Bloemfontein, Republic of South Africa S Supporting Information *

ABSTRACT: DFT calculations employing the OLYP and B3LYP functionals have been used to map out the low energy states of the metalloporphyrin−nitroxyl adducts “M(Por) + NO−” and “M(Por) + HNO”, where M = Fe, Co, and Mn and Por2− is the dianion of unsubstituted porphyrin. For [Fe(Por)(NO)]−, the calculations yield two low-energy solutions, with MS = 0 and 1. The MS = 0 solution is thought to represent the experimentally observed diamagnetic ground states of {FeNO}8 porphyrins, and both functionals yield FeNO geometrical parameters in excellent agreement with a recent crystal structure. For [Co(Por)(NO)]−, the lowest-energy solution for both OLYP and B3LYP is a true {CoNO}9 state that appears to be best described as a high-spin Co(II) center with a dxy2dxz1dyz1dz22dx2−y21 configuration antiferromagnetically coupled to a NO− diradical. Such an electronic configuration is expected to lead to diagnostic structural features, including long equatorial Co−N distances (∼2.1 Å), a strong displacement (∼0.4 Å) of the metal from the mean plane of the equatorial nitrogens, and a relatively short Co−N(O) distance (1.8 Å), which should all be experimentally observable. The dx2−y21 electronic configuration should also lead to characteristic EPR hyperfine parameters. The calculations also indicate a number of other low-energy states for [Co(Por)(NO)]−, including multiple {CoNO}8 porphyrin anion radical states. For [Mn(Por)(NO)]−, both functionals indicate a rather complex electronic state landscape, including multiple {MnNO}6 porphyrin anion radical states as well as a high-spin S = 3/2 {MnNO}7 state. Both functionals clearly indicate a low-spin Fe(II) state for [Fe(Por)(HNO)]. On the other hand, two comparably low-energy states are predicted for both [Co(Por)(HNO)] and [Mn(Por)(HNO)]. For [Co(Por)(HNO)], the two states are a low-spin Co(II) state with a dxy2dxz2dyz2dz21 configuration and a low-spin Co(III)(HNO)•− state. For [Mn(Por)(HNO)], the two states may be described as low- (S = 1/2) and intermediatespin (S = 3/2) Mn(II). The latter state has a relatively long Mn−N(O) distance of about 2.07 Å, which may be indicative of facile HNO dissociation.

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INTRODUCTION

The calculations reported herein focus on the model complexes [M(Por)(NO)]0,− and [M(Por)(HNO)], where M = Mn, Fe, and Co and Por is unsubstituted porphine. The results obtained provide the first, extensive overview of the structures, spin density profiles, and low-energy states of these species. Tables 1 and 2 present calculated OLYP30,31 and B3LYP32 data (both obtained with all-electron STO-Tz2P basis sets), respectively, on the various species studied. Figures 1−4 present selected spin density plots. The complex codes used in Figures 1−4 (A−X) are given in Tables 1 and 2.

The interactions of hemes with the diatomic ligands CO, NO, and O2 underlie a host of critically important metabolic and signaling processes.1 In recent years, two other small moleculesHNO2−4 and H2S5have also been recognized for their signaling roles. A handful of heme−HNO species have been spectroscopically characterized6−11 but none as yet has lent itself to X-ray structural characterization. The {FeNO}8, i.e., Fe(II) + NO−, state also occurs in key intermediates of heme enzymes such as cytochrome c nitrite reductase (ccNIR),12,13 fungal cytochrome P450 nitric oxide reductase (P450nor),14,15 and hydroxylamine oxidoreductase16 as well as in model complexes.2,3,17−20 In a key recent development, a relatively stable {FeNO}8 complex of an electron-deficient porphyrin has been isolated and crystallographically characterized.21 By contrast, much less is known about the interactions of NO− and HNO with nonheme metalloporphyrins such as Mn(II) and Co(II) porphyrins.22−24 The present exploratory DFT25−29 study was motivated by a desire to shed light on these less-known interactions and potentially to identify new, reduced metalloporphyrin−NO species. © XXXX American Chemical Society

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METHODS All calculations were carried out with the ADF 2014 program system.33 Two different functionalsOLYP and B3LYP (20% Hartree−Fock exchange)were employed, in conjunction with Grimme’s D334 dispersion corrections. A Cs symmetry constraint was generally used. A suitably fine grid for numerical integration of matrix elements and tight convergence criteria for both SCF and geometry iterations were employed throughout. Received: May 20, 2016

A

DOI: 10.1021/acs.jpcb.6b04983 J. Phys. Chem. B XXXX, XXX, XXX−XXX

B

a

0 −1 −1 −1 0 0 −1 −1 −1 −1 0 0 −1 −1 −1 −1 0 0 0 0 0 0 0 0 0

q

S

1/2 0 1 1 0 1 1/2 1/2 1/2 3/2 0 1 1/2 1/2 3/2 3/2 0 1 2 1/2 1/2 3/2 1/2 3/2 5/2 P Q R

V W

K N L O M S T

F I H G J

A B C

complex code 0.00 −1.43 −1.17 −1.17 0.00 0.55 −1.12 −1.16 −1.24 −0.75 0.00 0.11 −1.22 −1.20 −1.14 −1.30 0.00 0.58 0.53 0.00 0.15 0.55 0.00 0.07 0.35

Erel (eV) A′ 59|58 59|59 59|58 60|58 59|59 59|58 60|59 59|59 61|60 59|58 58|58 59|57 59|58 58|58 60|57 59|57 59|59 60|58 60|57 60|59 59|59 60|59 59|58 60|57 60|57

A″ 42|42 42|42 43|42 42|42 42|42 43|42 42|42 43|42 41|41 44|42 42|42 42|42 42|42 43|42 42|42 43|42 42|42 42|42 43|42 42|42 43|42 43|41 42|42 42|42 43|41

1.698 1.762 1.687 1.690 1.812 1.698 1.791 1.810 1.765 1.717 1.601 1.771 1.820 1.596 1.768 1.767 1.730 1.993 1.965 1.938 1.877 1.935 1.789 2.071 2.221

M−N(O) 1.172 1.195 1.181 1.180 1.168 1.160 1.177 1.180 1.190 1.180 1.178 1.181 1.196 1.187 1.191 1.209 1.224 1.234 1.238 1.220 1.246 1.226 1.234 1.245 1.240

N−O 2.009 1.999 2.024 2.025 1.992 2.080 2.009 2.004 2.053 2.102 2.032 2.036 2.039 2.047 2.052 2.206 2.000 2.015 2.105 2.003 1.992 2.063 2.012 2.038 2.065

M−Neq,cis 2.042 2.050 2.059 2.059 2.018 2.110 2.038 2.034 2.131 2.127 2.034 2.057 2.068 2.050 2.076 2.210 2.014 2.029 2.113 2.016 1.996 2.107 2.034 2.046 2.134

M−Neq,trans

geometry (Å, deg) 147.5 129.6 147.9 147.5 123.3 156.5 123.8 123.4 131.9 161.7 179.8 148.1 137.3 179.9 148.0 180.0 132.4 132.4 131.7 133.8 127.2 132.2 130.7 132.6 128.3

M−N−O

M 0.731 0.806 1.099 1.134 0.000 0.691 0.050 −0.127 1.844 2.147 0.000 2.792 1.021 −0.040 2.784 4.087 0.000 2.273 3.920 1.012 −0.095 2.638 1.875 3.625 4.450

0.171 −0.157 −0.031 −0.054 0.000 0.195 −0.018 0.140 −0.453 −0.035 0.000 −0.354 0.029 0.027 −0.417 −0.701 0.000 −0.098 −0.135 0.031 0.562 −0.047 −0.251 −0.176 0.247

N(O)

Por 0.306 −0.532 0.993 0.995 0.000 1.268 0.981 0.910 −0.066 1.009 0.000 −0.165 0.232 0.996 0.942 0.021 0.000 −0.012 0.435 0.002 0.032 0.537 −0.319 −0.230 0.079

O −0.208 −0.117 −0.061 −0.075 0.000 −0.154 −0.013 0.077 −0.325 −0.121 0.000 −0.273 −0.282 0.017 −0.309 −0.407 0.000 −0.163 −0.220 −0.045 0.501 −0.128 −0.305 −0.219 0.224

Mulliken spin populations

All energies are quoted relative to the ground state of the neutral species. The symbols M−Neq,cis and M−Neq,trans refer to equatorial M−N vectors that are cis and trans relative to the NO ligand.

[Mn(Por)(HNO)]

[Co(Por)(HNO)]

[Fe(Por)(HNO)]

[Mn(Por)(NO)]

[Co(Por)(NO)]

[Fe(Por)(NO)]

all-electron occupation (α|β)

Table 1. Selected OLYP/STO-Tz2P Calculated Results for Metalloporphyrin−XO Adductsa

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DOI: 10.1021/acs.jpcb.6b04983 J. Phys. Chem. B XXXX, XXX, XXX−XXX

C

a

0 −1 −1 −1 0 0 −1 −1 −1 −1 0 0 −1 −1 −1 −1 0 0 −1 0 0 0 0 0 0 0 0 0

q

S

1/2 0 1 1 0 1 1/2 1/2 1/2 3/2 0 1 1/2 1/2 3/2 3/2 0 1 1/2 0 1 2 1/2 1/2 3/2 1/2 3/2 5/2 K′ L S T U V W X P Q R

O

K N

G H J

E F

A B D

complex code 0.00 −1.45 −1.63 −1.29 0.00 0.52 −1.18 −1.50 −1.06 −1.10 0.00 −0.22 −1.56 −1.25 −1.60 −1.59 0.00 0.39 −1.11 0.00 0.23 0.73 0.00 0.22 0.54 0.06 0.00 0.37

Erel (eV) A′ 59|58 59|59 59|58 60|58 59|59 59|58 60|59 61|60 59|59 59|58 58|58 59|57 59|58 58|58 60|57 59|57 76|76 77|75 76|76 59|59 60|58 60|58 60|59 59|59 60|59 59|58 60|57 60|57

A″ 42|42 42|42 43|42 42|42 42|42 43|42 42|42 41|41 43|42 44|42 42|42 42|42 42|42 43|42 42|42 43|42 45|45 45|45 46|45 42|42 42|42 43|41 42|42 43|42 43|41 42|42 42|42 43|41

1.798 1.867 1.798 1.811 1.959 1.912 1.919 1.858 1.815 1.854 1.604 1.850 1.859 1.601 1.870 1.862 1.623 1.778 1.663 1.760 1.999 2.108 2.037 1.910 2.215 1.820 2.032 2.189

M−N(O) 1.164 1.181 1.201 1.174 1.151 1.148 1.158 1.199 1.164 1.192 1.162 1.177 1.199 1.172 1.188 1.188 1.158 1.174 1.174 1.228 1.229 1.269 1.202 1.244 1.193 1.249 1.255 1.231

N−O

1.996 2.098 2.025 2.033 2.057 2.040 2.042 2.046 2.032 2.015 2.045 1.997 2.007 2.006 1.995 1.984 2.045 2.008 2.027 2.107

2.009 2.004 2.168 2.018 1.988 2.069 2.000

M−Neq,cis 2.026 2.027 2.171 2.039 2.000 2.056 2.015 2.098 (mean) 2.017 2.101 2.027 2.042 2.035 2.038 2.056 2.057 2.033 2.038 2.045 2.100 2.017 2.008 2.004 1.992 2.064 2.034 2.034 2.058

M−Neq,trans

geometry (Å, deg)

2.181 2.243 2.185

M−Lax 140.8 129.3 180.0 139.7 121.5 131.5 122.1 132.6 119.9 180.0 180.0 148.2 138.3 179.8 144.5 148.0 179.8 137.8 180.0 129.2 129.3 118.0 131.7 124.6 134.9 126.1 125.6 122.1

M−N−O

M 1.951 1.945 3.321 2.071 −0.798 2.554 0.796 2.305 0.000 2.360 0.000 3.269 3.289 0.207 3.371 3.375 0.000 3.076 0.940 0.554 2.310 2.516 1.009 0.466 2.680 1.088 3.603 4.452

O −0.405 −0.451 −0.550 −0.441 0.283 −0.360 −0.281 −0.547 0.000 0.114 0.000 −0.493 −0.505 −0.086 −0.512 −0.513 0.000 1.912 −0.360 −0.316 −0.299 0.666 −0.032 −0.664 0.009 −0.364 −0.335 0.212

N(O) −0.506 −0.650 −0.913 −0.593 0.470 −0.511 −0.468 −0.849 0.006 0.441 0.000 −0.676 −0.748 −0.120 −0.760 −0.765 0.000 1.845 −0.557 −0.193 −0.064 0.740 0.046 −0.685 0.027 −0.032 −0.171 0.194

Mulliken spin populations Por −0.040 −0.844 0.142 0.963 0.045 0.317 0.953 0.091 0.994 0.085 0.000 −0.100 −1.036 0.999 0.901 0.903 0.000 −4.833 0.977 −0.045 0.053 0.078 −0.023 1.883 0.284 0.308 −0.097 0.142

All energies are quoted relative to the ground state of the neutral species. The symbols M−Neq,cis and M−-Neq,trans refer to equatorial M−N vectors that are cis and trans relative to the NO ligand.

Mn(Por)(HNO)

Co(Por)(HNO)

Fe(Por)(HNO)

Mn(Por)(NO)(Py)

[Mn(Por)(NO)]

[Co(Por)(NO)]

[Fe(Por)(NO)]

occupation (α|β)

Table 2. Selected B3LYP-D3/STO-Tz2P Calculated Data for Metalloporphyrin−XO Adductsa

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B3LYP, it is MS = 1 (D, Figure 1), essentially a high-spin Fe(II) ion with a dxy2dxz1dyz1dz21dx2−y21 configuration antiferromagnetically coupled to a NO− diradical. That said, B3LYP does indicate a low energy for state B so the calculations, taken together, do suggest an S = 0 ground state, which is consistent with the experimentally observed diamagnetism of reduced nitrosylhemes. Both OLYP and B3LYP yield similar, broken-symmetry spin density profiles for [Fe(Por)(NO)]− , which is rather interesting, considering that OLYP does not yield a brokensymmetry spin density for the apparently isoelectronic species [Co(Por)(NO)]. Although to a first approximation, the broken-symmetry spin density of [Fe(Por)(NO)]− may be thought of as indicative of reflecting antiferromagnetic coupling between a low-spin Fe(I) center and NO•, both functionals also place a significant amount of spin density on the porphyrin. The “eighth” Enemark−Feltham electron thus appears to be more delocalized in the {FeNO}8 case than in the {CoNO}8 case. That said, we are not aware of any experimental evidence in favor of partial ring-centered reduction of an iron porphyrin nitrosyl complex. Thus, in their spectroscopic study, Ryan and co-workers found similar frequencies for the oxidation-state marker band ν2 for [Fe(TPP)(NO)] (1564 cm−1) and [Fe(TPP)(NO)]− (1561 cm−1).45,46 Also, a B3LYP geometry optimization of [Fe(Br8TFPPP)(NO)]− did not yield a brokensymmetry solution for MS = 0. Importantly for this anion, the optimized metrical parameters, including the Fe−N(O) distance and the FeNO angle, are in near-perfect agreement with experiment (Figure 2).21 Thus, the exact nature of the {FeNO}8 state may well be somewhat sensitive to environmental influences such as subtituent effects and solvation. b. Reduced Cobalt Nitrosyl States. For [Co(Por)(NO)], the lowest-energy solutions for both OLYP and B3LYP correspond to MS = 0 (E, Figure 3), consistent with the experimentally observed diamagnetism of CoNO porphyrins.47,48 For both functionals, the lowest-energy triplet (F, Figure 3) is found some 0.5 eV above the ground state. Other results obtained with the two functionals do evince key differences, however. Thus, whereas B3LYP yields a brokensymmetry spin density profile and a rather long Co−N(O) distance of 1.959 Å, OLYP yields a fully spin-paired electron density and a shorter, more realistic Co−N(O) distance of 1.812 Å.49 These differences are illustrative, once again, of the tendency of B3LYP to underestimate the spin coupling among electrons.

Figure 1. Spin density plots for the ground state of [Fe(Por)(NO)] and key low-energy states of [Fe(Por)(NO)]−. The contour value chosen is 0.006 e/Å3.

The choice of the two functionals is based on earlier studies, both on transition metal compounds in general and nitrosyl complexes in particular.35−43 The broad conclusion from these studies is that, whereas classic pure functionals such as PW91 and BP86 exhibit an undue preference for “spin-coupled states”, hybrid functionals such as B3LYP unduly prefer states with higher degrees of spin decoupling. In a number of cases, including a study of iron nitrosyls, pure functionals based on the OPTX exchange functionals yielded distinctly better electronic state energetics than B3LYP.37,38,40,41 Confoundingly, in other cases, OLYP yielded comparatively poor energetics.43 We shall see that, in the present study, OLYP and B3LYP provide relatively similar descriptions of the various species and electronic states studied.44

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RESULTS AND DISCUSSION a. Reduced Iron Nitrosyl States. For nitrosylheme, [Fe(Por)(NO)] (A, Figure 1), it has already been recognized for some time that pure and hybrid functionals yield somewhat different spin density profiles.38,40 Thus, whereas the OLYP spin density is readily described in terms of a singly occupied Fe(dz2)-based MO with a small amount of NO(π*) character, B3LYP results in a much more pronounced separation of majority and minority spin densities so the overall spin density profile may be approximately described as an intermediate-spin Fe(III) center (S = 3/2) antiferromagnetically coupled to a NO− diradical (S = 1). For the [Fe(Por)(NO)]− anion, the two functionals also yield somewhat different results. For OLYP, the lowest-energy solution corresponds to MS = 0 (B, Figure 1); for

Figure 2. Comparison of B3LYP and experimental geometry parameters for the [Fe(Br8TFPPP)(NO)]− anion. D

DOI: 10.1021/acs.jpcb.6b04983 J. Phys. Chem. B XXXX, XXX, XXX−XXX

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Figure 3. Spin density plots for the ground state of [Co(Por)(NO)] and key low-energy states of [Co(Por)(NO)]−. The contour value chosen is 0.009 e/Å3.

For [Co(Por)(NO)]−, the lowest-energy state for both functionals corresponds to an MS = 1/2 solution with a spin density profile (G, Figure 3) indicitive of a singly occupied dx2−y2 orbital. Careful examination of the occupied and unoccupied MOs indicates a high-spin Co(II) center with a d xy 2 d xz1 d yz 1 d z2 2 d x2−y2 1 configuration antiferromagnetically coupled to a NO− diradical. Such an electronic description is also qualitatively consistent with key features of the optimized geometries, in particular, the long equatorial Co−N distances (∼2.1 Å), a strong displacement (∼0.4 Å) of the metal from the mean plane of the equatorial nitrogens, and a relatively short Co−N(O) distance (1.8 Å). Both the dx2−y21 electronic configuration and the key structural features of [Co(Por)(NO)]− provide “handles” that could lead to the eventual experimental identification of such a state.50 For the anion, the calculations also identify two low-energy {CoNO}8 porphyrin anion radical states (H and I, Figure 3). B3LYP also yielded a rather unusual MS = 3/2 solution some 0.4 eV above the ground state that appears best described as a high-spin Co(III) center with a dxy2dxz1dyz1dz21dx2−y21 configuration antiferromagnetically coupled to a NO•2− radicaldianion (J, Figure 3). c. Reduced Manganese Nitrosyl States. Both OLYP and B3LYP predict a low singlet−triplet gap for five-coordinate, neutral [Mn(Por)(NO)] of only a couple of tenths of an electronvolt. However, whereas OLYP predicts a singlet ground state, B3LYP favors the triplet as the ground state. These results are in accord with a recent spectroscopic and ab initio study indicative of the reversible interconversion of the singlet and triplet states of five-coordinate [Mn(TPP)(NO)].51 For sixcoordinate [Mn(Por)(NO)(py)] (py = pyridine), B3LYP also favors a singlet ground state.52 The electronic configuration of the singlet state may be described as classic low-spin {MNO}6; the triplet state (K, Figure 4) is best described as a high-spin Mn(III) center with a dxy1dxz1dyz1dz21 configuration antiferromagnetically coupled to a NO− diradical. For [Mn(Por)(NO)]−, there are several contenders for the ground state (Figure 4), which may be variously described as L (MS = 1/2): a low-spin {MnNO}6 porphyrin anion radical;

Figure 4. Spin density plots for the ground state of [Mn(Por)(NO)] and [Mn(Por)(NO)(py)], as well as the key low-energy states of [Mn(Por)(NO)]− and [Mn(Por)(NO)(py)]−. The contour value chosen is 0.006 e/Å3.

M (MS = 3/2): a high-spin Mn(II) center antiferromagnetically coupled to a NO− diradical; N (MS = 1/2): a high-spin Mn(III) center with a dxy1dxz1dyz1dz21 configuration antiferromagnetically coupled to a NO− diradical and to a porphyrin anion radical; O (MS = 3/2): a high-spin Mn(III) center with a dxy1dxz1dyz1dz21 configuration antiferromagnetically coupled to a NO− diradical and ferromagnetically coupled to a porphyrin anion radical. Somewhat surprisingly, OLYP calculations largely failed for [Mn(Por)(NO)(py)]− (owing to dissociation of the pyridine in the course of the optimizations). B3LYP calculations indicate a low-spin {MnNO}6 porphyrin anion radical as a plausible contender for the ground state. Attempts to optimize alternative states led to the pyridine falling off; these solutions are not shown in Figure 4. E

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density largely in the HNO π* orbital, which is consistent with the expected π-acceptor behavior of HNO.

Compared with FeNO porphyrins, MnNO porphyrins have been far less studied and little is known about MnNO porphyrin anions.53 The considerable variations in the MnNO angle among states L−O (Tables 1 and 2) may provide an experimental handle for the electronic−structural characterization of a MnNO porphyrin anion, in the event it proves possible to generate such a species. d. HNO Complexes. Both OLYP and B3LYP indicate an S = 0 ground state for [Fe(Por)(HNO)];6−11 unlike OLYP, however, B3LYP yields a broken-symmetry spin density for this state (S, Figure 5). This, however, is only a superficial

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CONCLUSIONS Combined use of the OLYP and B3LYP functionals, large STO-Tz2P basis sets, and judicious use of group theory have allowed us to map out in considerable detail the low-energy electronic states of metalloporphyrin−nitroxyl adducts involving Fe, Co, and Mn. Our key conclusions may be summarized as follows. 1. Both functionals indicate two low-energy solutions, with MS = 0 and 1, for [Fe(Por)(NO)]−. For OLYP, the MS = 0 solution is lower in energy, consistent with the observed diamagnetism of {FeNO}8 porphyrins. B3LYP, on the other hand, appears to incorrectly place the MS = 1 solution at a lower energy than the MS = 0 solution. On a positive note, both functionals do a good job of reproducing the geometrical parameters of the FeNO unit, relative to a recent X-ray structure. 2. For [Co(Por)(NO)]−, the calculations predict several low-energy states, including a true {CoNO}9 state and multiple {CoNO}8 porphyrin anion radicals. The {CoNO}9 state appears to be best described as a highspin Co(II) with a dxy2dxz1dyz1dz22dx2−y21 configuration antiferromagnetically coupled to a NO− diradical. The dx2−y21 configuration should provide several experimental “handles” including long equatorial Co−N distances (∼2.1 Å) and a strong displacement (∼0.4 Å) of the metal from the porphyrin N4 plane, as well as characteristic EPR hyperfine parameters. 3. The calculations also predict several contenders for the ground state of [Mn(Por)(NO)]−, including a high-spin S = 3/2 {MnNO}7 state and multiple {MnNO} 6 porphyrin anion radical states. 4. As far as charge-neutral HNO complexes are concerned, our calculations indicate a low-spin Fe(II) formulation for [Fe(Por)(HNO)]. For each of [Co(Por)(HNO)] and [Mn(Por)(HNO)] on the other hand, our calculations indicate two states with comparably low energies as potential ground states. 5. On the whole, the OLYP and B3LYP functionals appear to have performed comparably in this study. Although B3LYP at times has tended to favor states with higher spin multiplicity or greater α/β spin decoupling, we have succeeded in locating the majority of low-energy states with both functionals. Combined use of a couple of wellchosen functionals, including a pure functional and a hybrid one, thus appears to be an effective strategy for mapping out the electronic state landscape of transition metal complexes.

Figure 5. Spin density plots for the ground state and key low-energy states of [M(Por)(HNO)], M = Mn, Fe, or Co. The contour value chosen is 0.006 e/Å3.

difference, in our opinion; an examination of the MOs clearly indicates a low-spin t2g6 configuration for both functionals. The energy of the lowest triplet state (T, Figure 5), relative to the ground state, is about 0.6 eV with OLYP and 0.2 eV with B3LYP. Unfortunately, there are no pertinent X-ray structures with which the calculated metrical parameters of S can be directly compared. EXAFS measurements on myoglobin−HNO have yielded a Fe−NHNO distance of 1.82 Å,54 which is significantly longer than both the corresponding OLYP (1.73 Å) and B3LYP (1.76 Å) values for S. Geometry optimization of [Fe(Por)(HNO)(py)], a six-coordinate model of myoglobin− NO, did result in longer Fe−NHNO distances of −1.75 Å for OLYP and 1.80 Å for B3LYP. The latter is essentially in agreement with the EXAFS value within experimental error. For [Co(Por)(HNO)], the calculations yield two low-energy solutions, both with MS = 1/2V and W in Figure 5. V is clearly a low-spin Co(II) complex with a dxy2dxz2dyz2dz21 configuration. W, on the other hand, may be described as a low-spin Co(III)(HNO)•− complex. Experimentally, the very different spin density distributions of the two states should translate to distinct EPR hyperfine parameters. For [Mn(Por)(HNO)] too, the calculations predict two lowenergy solutions, P with MS = 1/2 and Q with MS = 3/2 (Figure 5). P may be described as a low-spin Mn(II) state with a dxy1dxz2dyz2 electronic configuration and Q as an intermediatespin Mn(II) state with a dxy1dxz1dyz2dz21 configuration. The spin density profiles of both states exhibit significant separation of majority and minority spin densities, with the minority spin

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.6b04983. Optimized Cartesian coordinates (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: +47 45476145. F

DOI: 10.1021/acs.jpcb.6b04983 J. Phys. Chem. B XXXX, XXX, XXX−XXX

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The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by FRINATEK project 231086 of the Research Council of Norway and by the National Research Foundation of the Republic of South Africa.

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DOI: 10.1021/acs.jpcb.6b04983 J. Phys. Chem. B XXXX, XXX, XXX−XXX