Effects of Solvents, Ligand Aromaticity, and Coordination Sphere on

ARTICLE pubs.acs.org/JPCB

Effects of Solvents, Ligand Aromaticity, and Coordination Sphere on the g Tensor of Anionic o-Semiquinone Radicals Complexed by Mg2þ Ions: DFT Studies Maciej Witwicki* and Julia Jezierska Faculty of Chemistry, Wroclaw University, 14 F. Joliot-Curie St., Wroclaw 50-283, Poland

bS Supporting Information ABSTRACT: Density functional theory (DFT) was employed to study the impact of Mg2þ ions on the o-semiquinone radical anions of different aromaticity in protic and aprotic solvents. After the geometry optimization of ligands and complexes, their g tensors were computed at the UBP86/TZVP and UB3LYP/TZVP theory levels. The suitability of various model systems, assuming continuum dielectric approaches, different Mg2þ coordination spheres (completed by solvent molecules), and inclusion of additional solvent molecules H-bonded to the ligands, was tested in terms of correlation between the experimental and calculated gshifts. The effects of complexation, ligands aromaticity, and solvents on the electron spin density for o-semiquinones are discussed. To recognize clearly the changes in the nature of the g tensor components, the contributions from particular excited states were analyzed. A structural characterization of the tested complexes is expected to be helpful in investigations on the complicated biosystems in which the similar paramagnetic units are present.

1. INTRODUCTION Quinones, along with their singly reduced semiquinone and doubly reduced hydroquinone forms, are known to possess biological significance. They are present in all life forms as they act as electron-transfer agents in the mitochondrial respiratory chain or in the reaction centers of bacterial and plant photosynthesis.1 The electron transfer2 can be activated through noncovalent interactions3 (e.g., hydrogen bonding) as well as by metal ions acting as Lewis acids.4 Hence, the redox quinoenzymes frequently occur in conjugation with metal cations.5 The binding mode of the metal ion directly determines the redox potentials which together with the electron transfer reorganization energy are the main factors influencing the rate of electron transfer.6 What is more, the quinones and their reduced forms, semiquinones and hydroquinones, are the structural units of humic acids,7 being the most widespread component of nonliving organic matter. Humic acids are also involved in a great number of chemical and biological processes in natural ecosystems determining the development of plants and microorganisms; e. g., they are responsible for the metal accumulation in soils as well as degradation and redox transformation of matter. Electron paramagnetic resonance (EPR) spectroscopy and especially high-field high-frequency EPR (HF EPR) allowing for better resolution of the g tensor components are the fundamental tools for studying semiquinone radicals in their biological and natural surroundings as well as in the laboratory systems.8-11 The studies on the metal ions complexes with semiqinone r 2011 American Chemical Society

radicals brought to light many interesting aspects induced by the metal-radical interaction, such as a redistribution of spin density strongly affecting the EPR properties of the complexes in comparison to those observed for free radicals.12-15 An important feature of the Mg2þ ions coordination by the semiquinone radical ligands in natural systems is a substantial excess of the Mg2þ ions over the ligands as this metal concentration, similarly to Ca2þ and Zn2þ, is of many orders of magnitude greater than trace metal ions16 stimulating the formation of mainly the 1:1 (metal-to-ligand) complexes. In recent years the intensity of theoretical studies on the chemical and biochemical systems has been constantly growing as such studies are frequently employed to support or verify the conclusions reached by the analysis of experimental data.17 Moreover, the current theoretical chemistry achieved a stage where the more realistic models can be investigated by including the environment and dynamics effects. An important role in this aspect is played by the quantum chemical methods based on density functional theory (DFT) with their excellent ratio of the computational cost to the performance permitting for their application to nearly real chemical systems. The semiquinone radical anions have been also theoretically studied in detail.10k,18,19 The results are particularly important as the g and A tensors of

Received: November 3, 2010 Revised: February 7, 2011 Published: March 09, 2011 3172

dx.doi.org/10.1021/jp110515j | J. Phys. Chem. B 2011, 115, 3172–3184

The Journal of Physical Chemistry B

ARTICLE

Figure 1. Anionic semiquinone radical ligands derived from o-quinone (sq), 9,10-phenanthrenequinone (psq), and 1,10-phenanthroline-5,6dione (ptsq).

these bioradicals are sensitive to the intermolecular interactions and therefore are useful sensors of the molecular environment. The aim of this work is to characterize theoretically, using DFT, the effects of Mg2þ coordination on the molecular and electronic structure of the o-semiquinone radical anions in correlation with the corresponding g tensor components calculated with Neese’s coupled-perturbed Kohn-Sham (CPKS) method20 at the UB3LYP/TZVP and UBP86/TZVP theory levels. The semiquione radicals with different aromaticity, derived from o-quinone (sq), 9,10-phenanthrenequinone (psq), and 1,10-phenanthroline-5,6-dione (ptsq) (see Figure 1), were chosen as ligands (L) coordinating the Mg2þ ions. To estimate the environment effects, two different solvents, acetonitrile (aprotic) and water (protic), were taken into consideration in two ways: (i) by including the solvents molecules as the additional ligands for the Mg2þ coordination and (ii) by including the solvent dielectric constants (PCM/COSMO approach). Furthermore, the effect of water molecules H-bonded to the radicals after the Mg2þ complexation was tested.

2. COMPUTATIONAL DETAILS 2þ

2a. Geometry Optimization. Optimizations of the Mg complexes and uncomplexed ligands geometries were carried out with the Gaussian 09 suite of programs21 utilizing the popular UB3LYP hybrid functional22 and TZVP basis set.23 Since the X-ray crystal structures for the investigated species are unknown, the initial geometries for optimizations were prepared using the structures derived from those revealed for more or less similar diamagnetic Mg2þ complexes. Predominantly, they were found to be octahedral;24 however, pentagonal bipyramidal were reported as well.25 Attempts to optimize both these coordination geometries and additionally the square planar and tetrahedral ones were carried out assuming Mg:L = 1:1 complexes with five, four, or two solvent molecules, respectively. The geometries of the simple models without the coordinated solvent molecules were also investigated (the coordination number = 2 for Mg2þ). Moreover, to complete the effect of solvation on geometry, the species were surrounded with a solvent cavity of appropriate dielectric constant (ε), in accordance with the integral equation formalism variant (IEFPCM) of Tomasi’s PCM method.26 No symmetry constraints were set in the optimization procedures. The geometries of species taken under discussion did not reveal imaginary frequencies that are the characteristic of saddle points on the energy surfaces. 2b. g Tensors and Population Analysis. To calculate the g tensors and to perform the L€owdin population analysis, the ORCA electronic structure system27 was used. The L€owdin population analysis is a variation of the method proposed by Mulliken, wherein atomic populations are calculated in the L€owdin orthogonalized atomic orbitals basis.42 The UB3LYP22

Figure 2. Optimized structures of the Mg2þ complexes with sq together with names and atoms numbering.

hybrid and UBP8628 general gradient approximation functionals together with the TZVP23 basis set were employed. To cover the effects of solvent cavity in these calculations, the conductor-like screening model (COSMO) implemented in the ORCA program was utilized.29 The g tensors were calculated using Neese’s CPKS method20a combined with an accurate spin-orbit coupling operator [RI-SOMF(1X)].20b The calculated components are given as g-shifts (Δgij) in parts per million (ppm): Δgij = (gij - ge) 106, where ij = xx, yy, zz, and ge = 2.002 319 is the free electron g value. The presented calculations of the g tensor did not employ gauge including atomic orbitals (GIAO), and the results are therefore dependent on the choice of origin. However, if moderate or large basis sets are used and the choice of origin is reasonable (either at the center of the electronic charge as in this work or at the center of nuclear charge or at the center of mass), this effect is in range of a few ppm and does not pose a problem.20,30

3. RESULTS AND DISCUSSION 3a. Molecular Structure and Spin Distribution. The initial pentagonal bipyramidal geometries (assuming five solvent molecules) during the optimization procedure were converged to the octahedral with one solvent molecule outside the Mg2þ coordination sphere. This result was independent of semiquinone ligand (sq, psq, and ptsq) or employed solvent (water, acetonitrile). It is understandable as in the similar systems (ref 25) mentioned in section 2a the pentagonal bipyramidal geometries were forced by the ligands' structures. For every complex 3173

dx.doi.org/10.1021/jp110515j |J. Phys. Chem. B 2011, 115, 3172–3184

The Journal of Physical Chemistry B with two coordinated solvent molecules, the square planar geometry revealed an imaginary frequency and reoptimization of these structures along their imaginary modes led to the tetrahedral geometries. In this work, the following rules for the structure naming are used: (a) short names of o-semiquinones given in Figure 1 point to the radical molecule; (b) an arabic number following the short name of o-semiquinone is used to differentiate the Mg2þ complexes: 1 is used for the simple models without any additional solvent molecules in the coordination sphere, and 2 indicates the tetrahedral geometries and 3 the octahedral ones; (c) the letter A or W after the number indicates that acetonitrile or water molecules, respectively, complete the coordination sphere; and (d) the letter A or W in superscript (for acetonitrile and water, respectively) indicates that the solvent cavity was included in the calculation. For example, ptsq3WW denotes the octahedral complex of Mg2þ with semiquinone derived from 1,10-phenanthroline-5,6-dione with coordination sphere completed with water molecules and solvent cavity covered utilizing the PCM/ COSMO method for water (ε = 78.36). The naming is additionally illustrated in Figure 2 for the optimized geometries of the Mg2þ complexes with sq. Analogical figures for psq and ptsq are given in the Supporting Information (Figure S.1). The relations between the structural parameters, spin density distributions, and g tensors for p- and o-semiquinones have been discussed previously in detail (see for example refs 10k, 18, 19, 31, and 32). It is known that the gxx and gyy components of semiquinones are dominated by the second-order spin-orbit/ orbital Zeeman term, which is related to the distribution of spin density between the hydroxyl oxygens (O1 and O2) and the ipso carbons (C1 and C2). Since the spin density depends on the RC-O bonds lengths and is significantly affected by solvent effects,10k,18a-18c,19,31 the changes of these distances as the result of Mg2þ complexation ought to be monitored as well (see Table 1). To obtain an accurate spin density distribution for the uncomplexed semiquinones, it is obligatory to include solvent effects into calculations. For the aprotic solvents (like acetonitrile), the PCM or COSMO correction fulfills this requirement. However, the explicit molecules hydrogen bonded to the radical anion need to be taken into consideration for the protic solvents (like water) in addition to the PCM or COSMO. Hence, every spin population, bond length or g tensor obtained for the Mg2þ complexes in acetonitrile ought to be compared to those predicted in terms of dielectric continuum approach for uncomplexed radicals (sqA, psqA, ptsqA). On the other hand, these values for the Mg2þ complexes in water should be compared to those predicted for the radicals involved in the hydrogen bonding with water molecules (sq(H2O)3W, psq(H2O)3W, and ptsq(H2O)3W). The optimized structures of the radicals with the H-bonded water molecules are shown in the Supporting Information (Figure S.2). Independently of the coordination sphere, the RC-O distances are significantly greater for semiquinone radicals bonding to Mg2þ than those obtained for the uncomplexed radicals. In the case of the uncomplexed radicals, larger RC-O were predicted for sq than for psq, also after the PCM and hydrogen-bonding inclusion, whereas for sq coordinated to Mg2þ they were revealed to be smaller than for psq. This shows that the impact of ligand aromaticity on RC-O is opposite after the complexation. Importantly, the RMg-O distances decrease on the increasing ligand aromacity.

ARTICLE

Table 1. Lengths (in Å) of the C-O and Mg-O Bonds for Mg2þ Complexes with Anionic Semiquinone Radicals Together with the Lengths of the C-O Bond for the Uncomplexed Anionic Semiquinone Radicalsa RC1-O1

RC2-O2 2þ

Mg

RO1-Mg

RO2-Mg

Complexes

sq1

1.305

1.305

1.909

1.909

sq1A

1.283

1.283

2.048

2.048

sq1W

1.282

1.282

2.056

2.057

psq1

1.316

1.316

1.895

1.895

psq1A

1.284

1.284

2.042

2.042

psq1W

1.285

1.285

2.022

2.022

ptsq1 ptsq1A

1.312 1.280

1.312 1.280

1.901 2.054

1.901 2.054

ptsq1W

1.279

1.279

2.058

2.058

sq2A

1.291

1.291

1.968

1.968

sq2AA

1.288

1.288

2.002

2.002

sq2W

1.296

1.296

1.954

1.954

sq2WW

1.284

1.284

2.047

2.048

psq2A

1.296

1.296

1.958

1.958

psq2AA psq2W

1.289 1.302

1.289 1.302

1.995 1.942

1.995 1.942

psq2WW

1.285

1.285

2.037

2.037

ptsq2A

1.294

1.294

1.964

1.964

ptsq2AA

1.285

1.285

2.003

2.003

ptsq2W

1.300

1.300

1.948

1.948

ptsq2WW

1.280

1.280

2.046

2.046

sq3A

1.280

1.280

2.053

2.053

sq3AA sq3W

1.280 1.288

1.280 1.288

2.080 2.037

2.078 2.037

sq3WW

1.280

1.280

2.092

2.092

psq3A

1.283

1.283

2.045

2.045

psq3AA

1.280

1.280

2.074

2.074

psq3W

1.293

1.293

2.025

2.025

psq3WW

1.281

1.281

2.079

2.081

ptsq3A

1.281

1.281

2.053

2.053

ptsq3AA ptsq3W

1.276 1.290

1.276 1.290

2.086 2.031

2.086 2.031

ptsq3WW

1.277

1.277

2.087

2.088

o-Semiquinones

a

3174

sq

1.252

1.252

sqA

1.265

1.265

sqW

1.266

1.266

sq(H2O)3

1.265

1.265

sq(H2O)3W

1.273

1.274

psq

1.249

1.249

psqA psqW

1.263 1.263

1.263 1.263

psq(H2O)3

1.263

1.257

psq(H2O)3W

1.273

1.266

ptsq

1.249

1.249

ptsqA

1.259

1.259

ptsqW

1.260

1.260

ptsq(H2O)3

1.262

1.256

ptsq(H2O)3W

1.270

1.261

All predicted at the UB3LYP/TZVP theory level. dx.doi.org/10.1021/jp110515j |J. Phys. Chem. B 2011, 115, 3172–3184

The Journal of Physical Chemistry B The increase of RC-O under the Mg2þ coordination is clearly exemplified by comparison of these parameters for sq1, psq1, and ptsq1 with those for the parent radicals, also after including of the PCM formalism. Although the RC-O values for the Mg2þ complexes with partly and fully completed coordination spheres are quite similar, the RMg-O distances are significantly different, as is seen, e.g., for sq1A (2.048 Å) and sq2AA (2.002 Å) or sq3AA (2.078 Å). Hence, the complexes with partly completed coordination sphere seem to be a rough approximation to the real systems properties. The inclusion of the PCM correction for uncomplexed radicals, also when they are H-bonded to water molecules, leads to the increase of RC-O, whereas for all Mg2þ-complexed radicals to the decrease. At the same time, the calculations corrected by the PCM result in a significant increase of the RMg-O distances. The RC-O and RMg-O distances were found to be dependent on the type of coordination sphere (with the same solvent included). For tetrahedral geometries, the RC-O values are greater than for octahedral, whereas for RMg-O this tendency is inversed. The impact of solvent on the RC-O and RMg-O bonds requires an additional comment. Without the PCM inclusion, the RC-O values are notably greater for the Mg2þ complexes formed in water than for those in acetonitrile (Table 1). However, when the PCM is taken into account, this tendency for the tetrahedral complexes is reversed, whereas for the octahedral complexes the RC-O values become almost solvent independent. The RMg-O distances obtained from the optimizations without the PCM formalisms are greater for acetonitrile, whereas the PCM inclusion results in opposite tendency. From the EPR point of view, it is important to investigate how the spin distribution in o-semiquinones is affected by the Mg2þ complexation. The Mg2þ binding results in a significant spin density redistribution exposed by the L€owdin spin populations (see Table 2), emphasized in greater accumulation of the spin density on the ipso carbons comparing to that for the free radicals. Quite the contrary, the population on the hydroxyl oxygen atoms is diminished. Therefore, the Mg2þ complexation generates the spin density redistribution similar to this caused by the bulk dielectric effects and by the hydrogen bonds formation. Such changes in the spin distribution ought to give a significant decrease of the perpendicular g tensor components, as the decrease of spin population on the hydroxyl oxygen atoms was shown to lead to the reduced g tensor components.10k,18a,18c,19,31-33 However, the redistribution induced by the Mg2þ binding is of far greater magnitude, and so the decrease of the g tensor components is expected to be more significant as well. The spin populations on the hydroxyl oxygen and ipso carbon atoms for the uncomplexed radicals in vacuum and those interacting with solvent are compared with those for the octahedral and tetrahedral Mg2þ complexes formed in acetonitrile and water in Figure 3, A and B, respectively. Significantly, a spin accumulation on the Mg atom was found to be very small (see Table 2). Although it has been shown that for similar chemical systems containing other diamagnetic metals and o-semiquinones the hyperfine coupling constants can be observed,10j,12i,13 their small magnitudes strongly suggest a very small accumulation of the spin density on the metal cations. This indicates that the spin populations predicted in this work accurately mimic the spin density of real systems. The effect of ligand aromaticity is also distinctly seen in the spin distribution. For the semiquinones with condensed aromatic

ARTICLE

Table 2. L€ owdin Spin Populations (G) Predicted at the UB3LYP/TZVP Theory Level FC1

FC2

FO1

FO2

FMg

Mg2þ Complexes sq1

0.213

0.213

0.158

0.158

0.014

sq1A sq1W

0.169 0.167

0.169 0.167

0.198 0.199

0.198 0.199

0.005 0.005

psq1

0.220

0.220

0.114

0.114

0.011

psq1A

0.201

0.201

0.175

0.175

0.005

psq1W

0.201

0.201

0.175

0.175

0.005

ptsq1

0.227

0.227

0.124

0.124

0.012

ptsq1A

0.198

0.198

0.187

0.187

0.005

ptsq1W

0.197

0.187

0.189

0.189

0.004

sq2A sq2AA

0.182 0.174

0.182 0.175

0.188 0.194

0.188 0.194

0.005 0.003

sq2W

0.193

0.193

0.178

0.178

0.007

sq2WW

0.166

0.165

0.201

0.201

0.005

psq2A

0.211

0.210

0.156

0.156

0.005

psq2AA

0.204

0.204

0.170

0.170

0.003

psq2W

0.215

0.215

0.142

0.142

0.006

psq2WW

0.198

0.198

0.179

0.179

0.004

ptsq2A ptsq2AA

0.213 0.203

0.213 0.203

0.164 0.182

0.164 0.182

0.004 0.003

ptsq2W

0.219

0.219

0.151

0.151

0.006

ptsq2WW

0.195

0.195

0.190

0.190

0.004

sq3A

0.152

0.152

0.214

0.214

0.000

sq3AA

0.151

0.150

0.215

0.215

-0.001

sq3W

0.175

0.175

0.196

0.196

0.001

sq3WW

0.154

0.154

0.212

0.212

-0.001

psq3A psq3AA

0.190 0.186

0.190 0.187

0.190 0.195

0.190 0.195

0.000 -0.001

psq3W

0.207

0.207

0.165

0.165

0.001

psq3WW

0.189

0.189

0.192

0.193

-0.001

ptsq3A

0.190

0.190

0.197

0.197

0.000

ptsq3AA

0.182

0.182

0.205

0.206

-0.001

ptsq3W

0.208

0.208

0.173

0.173

0.001

ptsq3WW

0.185

0.185

0.203

0.203

-0.001

sq sqA

0.060 0.104

0.060 0.104

0.253 0.243

0.252 0.243

sqW

0.106

0.106

0.242

0.242

sq(H2O)3

0.103

0.104

0.247

0.247

sq(H2O)3W

0.131

0.132

0.236

0.234

psq

0.096

0.096

0.244

0.244

psqA

0.146

0.146

0.230

0.230

psqW

0.148

0.148

0.230

0.230

psq(H2O)3 psq(H2O)3W

0.150 0.179

0.126 0.156

0.225 0.210

0.232 0.215

ptsq

0.097

0.097

0.248

0.248

ptsqA

0.140

0.140

0.237

0.237

ptsqW

0.141

0.141

0.236

0.237

ptsq(H2O)3

0.150

0.125

0.230

0.237

ptsq(H2O)3W

0.178

0.146

0.219

0.227

o-Semiquinones

rings, the spin populations on the ipso carbon atoms are significantly greater and on the hydroxyl oxygen atoms 3175



ARTICLE

3b. g Tensors for o-Semiquinones Complexes with the Mg2þ Ions. The calculated Δg tensor components are listed in

Figure 3. Comparison of the L€owdin spin populations (F) on the ipso carbon (C1) and hydroxyl oxygen (O1) predicted at the UB3LYP/ TZVP level: for sq and its Mg2þ complexes in water (A) and in acetonitrile (B); for two radical anions of different aromaticity and their Mg2þ complexes (C).

significantly smaller as compared to the populations for the radical derived from o-quinone. Neither solvent effects nor metal complexation does not change this tendency (see Table 2 and Figure 3C). Therefore, the effect of ligand aromaticity should be observed in the EPR spectral parameters of free and metalcomplexed o-semiquinones. Interestingly, the tetrahedral coordination geometry causes greater accumulation of spin density on the ipso carbon atoms and smaller on the hydroxyl oxygens. Hence, the type of coordination sphere is expected to affect the values of the g tensor components.

Table 3. As the Δgzz values were found to be insensitive to the complexation or solvent effects, therefore only the perpendicular components (Δgxx and Δgyy) will be further discussed. Generally, the decrease of the perpendicular components due to the Mg2þ complexation is an after effect of spin density redistribution away from the oxygen atoms (see point section 3a). This stays in agreement with Stone’s qualitative model.33 The comparison of the UBP86 and UB3LYP results shows that both density functionals gave similar outcomes. Only for the uncomplexed radicals in aprotic solvent the UB3LYP appeared to work significantly better. The report on our detailed investigation concerning the solvent effects on the sq, psq, and ptsq radicals can be found in ref 31. To investigate the impact of geometrical parameters on the Δg tensor, the components were rigidly scanned along the RC-O bonds for the sq radical and its sq3W complex. From Figure 4A it is easily seen that Δgxx and Δgyy significantly increase with the RC-O distances expanding. A similar effect was observed previously for p-semiquinone radical anion.32 The perpendicular components are predicted to be greater for sq than for psq and ptsq in parallel to the same RC-O change, indicating again the same tendency as shown in Figure 4A for sq. Interestingly, the sqA geometry (optimized with the solvent cavity inclusion) results in the perpendicular components smaller than those for sq (gas phase), although the RC-O change in opposite way (e.g., Δgxx = 4789 for sqA and 5179 for sq, whereas RC-O = 1.265 and 1.252 Å, respectively). For the radicals with H-bonded water molecules and for the Mg2þ complexes, it is even more strongly pronounced. However, the environmental effects can influence the Δg tensor in two different ways:19 (i) directly, by polarizing the electron density at a given structure and (ii) indirectly, by changing the structure. Hence, when the lowering of the perpendicular components with the increase of the RC-O distances is observed due to the solvation or Mg2þ complexation, it distinctly indicates that the indirect (increase of RC-O) and direct (electron density polarization) environment effects, due to solvation, hydrogen bonding, or Mg2þ complexation, have to bring opposite contributions to the Δg tensor. The indirect effect accompanying the RC-O changes is illustrated in Figure 4A. To include only the direct effect, the perpendicular Δg tensor components were calculated for the structure optimized in the gas phase with a stepwise increase of dielectric constant (ε). In accordance with the expectations,19,31 the Δgxx and Δgyy components were found to decrease on ε enhancement (Figure 5). In addition to RC-O, the RMg-O distances effects were also monitored. The Δgyy component appeared to be insignificantly dependent on RMg-O (see Figure 4B), especially for the Mg-O bond lengths from 1.90 to 2.10 Å, typical of fully optimized complexes structures (Table 1). Quite the contrary, Δgxx increase with RMg-O values growing, as is exemplified by the scan performed for the sq3W complex. The changes of the perpendicular components due to increasing values of ε (see Figure 5) observed for the sq3W complex are relatively small, but the tendency is opposite to that for sq. The small magnitude of these changes reveals that the effect of Mg2þ ion on the electron density of semiquinone radical is more significant than the effect of solvent cavity. Independently of the coordination sphere, the Mg2þ complexes with sq reveal a significant decrease of Δgxx and Δgyy 3176



ARTICLE

Table 3. Δg Tensors (in ppm) Calculated at the UB3LYP/TZVP and UBP86/TZVP Theory Levels UB3LYP/TZVP Δgxx

sq1 2587 sq1A 3570 sq1W 3599 psq1 1969 psq1A 2980 psq1W 2978 ptsq1 1949 ptsq1A 3076 ptsq1W 3109 sq2A 3418 A sq2A 3475 sq2W 3189 sq2WW 3669 psq2A 2682 psq2AA 2900 psq2W 2485 psq2WW 3086 ptsq2A 2714 ptsq2AA 2997 ptsq2W 2492 ptsq2WW 3170 sq3A 4123 sq3AA 4045 sq3W 3621 sq3WW 3966 psq3A 3360 psq3AA 3404 psq3W 2845 psq3WW 3365 ptsq3A 3372 ptsq3AA 3480 ptsq3W 2884 ptsq3WW 3418 exptl for sq and Mg2þ complex in watera exptl for psq and Mg2þ complex in acetonitrileb exptl for ptsq and Mg2þ complex in acetonitrileb sq sqA sqW sq(H2O)3 sq(H2O)3W psq psqA psqW psq(H2O)3 psq(H2O)3W ptsq ptsqA ptsqW ptsq(H2O)3 ptsq(H2O)3W exptl for sq in watera exptl for psq in acetonitrileb exptl for ptsq in acetonitrileb a

5179 4789 4773 4260 3957 4571 4295 4281 4281 3797 4584 4328 4322 4283 3947

UBP86/TZVP

Δgyy

Δgzz

1831 2445 2464 788 2402 2427 1304 2474 2499 2359 2463 2253 2507 2161 2313 2072 2396 2216 2389 2152 2466 2734 2806 2579 2772 2534 2610 2397 2690 2547 2670 2445 2743

Mg2þ Complexes -117 -119 -119 -93 -96 -100 -103 -110 -111 -70 -70 -123 -102 -100 -103 -126 -117 -114 -119 -136 -130 -57 -46 -115 -115 -110 -102 -136 -144 -121 -116 -151 -157

4406 3988 3973 3939 3679 4163 3841 3830 3503 3383 4302 3965 3956 3576 3470

o-Semiquinones -110 -125 -125 -112 -124 -89 -94 -94 -122 -165 -95 -99 -100 -134 -119

Δgiso

Δgxx

Δgyy

Δgzz

Δgiso

1434 1965 1981 888 1762 1768 1050 1813 1832 1902 1956 1773 2025 1581 1703 1477 1788 1606 1756 1503 1835 2267 2268 2028 2208 1928 1971 1702 1970 1933 2011 1726 2002 1881 1981 1281

2634 3653 3676 1931 2938 2936 2024 3073 3100 3428 3534 3243 3730 2586 2833 2433 3020 2680 2971 2509 3141 4056 4034 3647 3977 3188 3262 2752 3238 3250 3372 2855 3328

1728 2260 2278 900 2195 2217 1473 2282 2302 2165 2281 2070 2315 1953 2107 1877 2177 2041 2196 1997 2260 2498 2591 2369 2554 2265 2362 2162 2436 2305 2430 2241 2500

-117 -115 -115 -91 -90 -94 -109 -104 -104 -73 -70 -122 -99 -102 -97 -119 -108 -113 -112 -129 -122 -76 -54 -120 -121 -125 -102 -133 -141 -134 -116 -148 -156

1415 1932 1946 913 1681 1686 1130 1750 1766 1840 1915 1730 1982 1479 1614 1397 1696 1536 1685 1459 1760 2159 2190 1965 2137 1776 1840 1593 1844 1807 1895 1649 1891 1881 1981 1281

3158 2884 2874 2696 2504 2882 2681 2672 2554 2339 2930 2731 2726 2575 2432 2281 2481 2681

4903 4696 4687 4029 3836 4140 4041 4031 3972 3590 4192 4103 4103 4012 3778

4216 3794 3780 3675 3465 3781 3513 3506 3182 3108 3947 3658 3650 3274 3210

-105 -118 -118 -102 -118 -79 -84 -83 -99 -151 -87 -90 -90 -111 -97

3005 2791 2783 2534 2394 2614 2490 2485 2351 2182 2684 2557 2555 2392 2297 2281 2481 2681

Taken from ref 14. b Taken from ref 13.

compared to those for the free sq radical in aprotic solvent. However, when the hydrogen bonds between o-semiquinone radical and water molecules are replaced by the Mg2þ ion, only the Δgyy component is distinctly reduced in magnitude. The decrease of Δgxx in such case is less important (e.g., for sq(H2O)3W and sq3WW than for sqA and sq3AA), leading consequently to

smaller decrease in their Δgiso. The different change of Δg tensor components due to Mg2þ coordination in aprotic and protic solvents may be applied for characterization of more complicated biological or natural systems. The small change of Δgxx (or even Δgiso) on the Mg2þ coordination can be an indication that the free semiquinones were initially engaged in hydrogen bonding. 3177



ARTICLE

Figure 5. Calculated g-shifts (in ppm) for the sq and sq3W gas-phaseoptimized structures as a function of 1/ε at the UB3LYP/TZVP level. ε is the dielectric constant in the range from 1 to 100. The insignificant Δgzz are not displayed.

Figure 4. Rigidly scanned Δgxx and Δgyy components for sq and sq3W along the RC-O (A) and RMg-O (B) bonds at the UB3LYP/TZVP theory level.

The impact of coordination sphere of metal ion on the radical Δg tensor is another interesting aspect. Both perpendicular components (and in consequence the Δgiso values) were found to be greater for the octahedral coordination sphere than for the tetrahedral, independent of the solvent or the continuum dielectric model inclusion. This effect may be explained by greater L€owdin spin populations on the oxygen atoms predicted for the octahedral coordination. Furthermore, as was shown above (Figure 4), the opposite change in the C-O and O-Mg distances (smaller RC-O and greater RMg-O) for the octahedral complexes give opposite contributions to the perpendicular components. Hence, the increased perpendicular components for the octahedral coordination strongly suggest that the effect of changes in RMg-O overcomes that caused by the changes in RC-O. Therefore, the EPR properties of the semiquinones complexes with Mg2þ seem to be strongly affected by the RMg-O bonds changes. These observations suggest also that the coordination sphere or its change may be effectively monitored via EPR spectroscopy. The Δgxx and Δgyy components of the investigated complexes are also dependent on aromaticity of the semiquinone ligand.

The Mg2þ complexes with psq tend to have smaller perpendicular components than their counterparts with sq. The solvent effects on the Δg tensor for o-semiquinone complexes with Mg2þ ions are also associated with the coordination sphere. For the tetrahedral complex there are important differences between the Δgxx components obtained for the complexes with acetonitrile and water, while the Δgyy values differ in smaller degree. The inclusion of the continuum dielectric approaches (PCM/COSMO) increases the Δgxx and Δgyy values. This effect for water is especially significant and leads to Δgxx greater than that for acetonitrile. For the octahedral coordination in acetonitrile, the perpendicular components are again greater than those obtained when water is coordinated; however, after the use of the dielectric approaches the components become almost indistinguishable. The effect of the solvent cavity on the Δg tensors of the discussed Mg2þ complexes should be interpreted in terms of the spin density redistribution induced by the changes in RC-O and RMg-O. For example, the comparison of the values of perpendicular components for sq2W and sq2WW reveals an enhancement in the spin populations on the hydroxyl oxygen atoms correlated with the RC-O decrease and RMg-O increase, respectively. The changes in RC-O and RMg-O bring opposite impact, and so the growth of the perpendicular components again indicates that the changes in RMg-O bring more significant effect than those in RC-O. 3c. Analysis of the g Tensor Contributions. The individual contributions to the Δg tensor were calculated employing an alternative one-component method proposed by Schreckenbach and Ziegler34 as implemented in the ADF 2008.01 package.35 In these relativistic spin-unrestricted DFT calculations based on the scalar Pauli Hamiltonian the local density approximation of Vosko, Wilk, and Nusair36 was combined with the BP8628 functional. Standard all-electron Slater-type TZP basis set was used for all atoms. 3178



ARTICLE

Table 4. Individual Contributions (in ppm) to the Δg Tensor Calculated at the UVWNBP86/TZP Theory Level for Anionic oSemiquinone Radical and Its Octahedral Mg2þ Complex sq Δgxx

Δgyy

sq(H2O)3 Δgzz

Δgxx

Δgyy

sq3W Δgzz

Δgxx

Δgyy

Δgzz

Δgtot

6032

5116

-212

4898

4519

-138

4170

3005

-264

Δgrel

-216

-216

-216

-219

-219

-219

-208

-208

-208

82 258

67 584

41 -17

69 318

41 625

82 -2

79 318

64 547

38 -1

Δgd Δgp(occ-occ) Δgp(occ-vir)

5908

4681

-20

4730

4071

1

3982

2602

-93

Σ(DfV)

-178

37

-20

-158

-83

46

-296

-108

-65

Σ(SfV)

-108

174

0

-187

226

-38

-113

195

5

Σ(DfS)

6194

4469

0

5076

3929

-7

4391

2514

-33

0

2016

0

0

1458

0

0

209

0

4980

0

0

3763

0

0

3798

0

0

total

HfS H-2fS

In this one-component method Δg tensor is given by three contributions34 p

Δgijtot ¼ Δgijrel þ Δgijd þ Δgij

d where Δgrel ij combines scalar relativistic corrections, the Δgij term p corresponds to the diamagnetic correction, and Δg ij is the paramagnetic term dominating the deviation from the free electron ge value (except for the very small total deviations from ge). Δg pij contains contributions due to the coupling between ) as well as between occupied and occupied orbitals (Δg p,occ-occ ij ). The ADF program was used because virtual ones (Δg p,occ-vir ij in the implementation included in it allows to analyze Δgp,occ-vir ij terms of single excitations. The calculated contributions to the Δg tensor for sq, sq(H2O)3, and sq3W are listed in Table 4 and the isosurfaces of the suitable orbitals are shown in Figure 6. The Δgrel ij values predicted for all three model systems are negative and minor. Moreover, this term is insensitive to the hydrogen bonds formation or Mg2þ complexation. Δgdij is slightly positive for all three systems; however, its magnitude in comparison to Δgtot ij is far too small to be is discussed meaningfully. For the Δgzz component Δgp,occ-occ ij slightly negative for sq and very close to the zero value for contribution is positive for sq(H2O)3 and sq3W. The Δgp,occ-occ ij all perpendicular components, insignificantly sensitive to the hydrogen bond formation or Mg2þ complexation; however, for Δgyy it is always almost twice as large as for Δgxx. contribution is usually the most important The Δgp,occ-vir ij one37 and it dominates Δg shifts predicted for the perpendicular components. Δgzz is very small in magnitude because of the insignificant coupling between occupied and virtual orbitals. To meaningfully discuss these couplings for the perpendicular components, the electronic excitations were classified into three groups (according to Kaupp et al.19): (i) from doubly occupied orbitals to SOMO (D f S); (ii) from SOMO to virtual ones (S f V); and (iii) and from doubly occupied to virtual orbitals (DfV) which are expected to bring small contributions to the Δg tensor of organic radicals as they arise from the spin values determined by each of these polarization. The Δgp,occ-vir ij three groups of excitations are listed in Table 4. The sq perpendicular components are dominated by the D f S excitations, in accordance with the report for p-semiquinone.19 This group of excitations is the leading one also after the hydrogen bonds formation or the Mg2þ complexation. For the o-semiquinone radical anion in the gas phase (sq), the largest Δgxx

Figure 6. Frontier molecular orbitals giving the most important paramagnetic contribution to the Δg tensor components for o-semiquinone radical and its Mg2þ complex. The labels of the orbitals are given according to the results for sq.

component is mainly prevailed by the HOMO-2 f SOMO excitation, not by HOMO f SOMO as was stated for psemiquinone.19 HOMO-2 is an in-plane molecular orbital with a large contribution from the O1 px and O2 py atomic orbitals and b2 symmetry. The HOMO f SOMO excitation brings a significant contribution to the Δgyy component. HOMO is also an in-plane molecular orbital with an important contribution from O1 px and O2 py but of a1 symmetry. The formation of hydrogen bonds (sq(H2O)3) between water molecules and o-semiquinone radical results in a significant reduction of the Δgxx and Δgyy components as the contributions from the HOMO-2 f SOMO and HOMOfSOMO excited states are clearly decreased. The Mg2þ complexation results in a similar contribution of the HOMO-2 f SOMO excitation to Δgxx as that predicted for sq(H2O)3. Nevertheless, Δgxx is further reduced for about 700 ppm due to decrease of the remaining D f S excitations. The value of the Δgyy component is in greater degree reduced on Mg2þ complexation as compared 3179


The Journal of Physical Chemistry B to the hydrogen bonds formation, mainly because of an important lowering of the contribution from the HOMO f SOMO excitation. 3d. Impact of the Hydrogen Bonding and Binding Site. Hydrogen bonding can be considered as the most important noncovalent interaction between the molecules. Its structure and function tend to be essential for many systems of chemical and biological importance.38 Quinones are a great example of biologically active systems in which hydrogen bonding plays a vital role.39 Therefore, the impact of hydrogen bonds on the EPR properties of semiquinone radicals has been intensively investigated also via theoretical approach.10k,18,19,31 In case of osemiquinones the Mg2þ complexation does not have to prevent the formation of two hydrogen bonds between protic solvent molecules and the paramagnetic ligand (one per each hydroxyl oxygen). To investigate the hydrogen bonding effect on the Δg tensor, the tetrahedral and octahedral complexes were optimized with two water molecules H-bonded to the radical ligand. The resulting structures for sq are shown in Figure 7A and for psq and ptsq in the Supporting Information (Figure S.3). The components of the Δg tensors predicted for these structures are listed in Table 5. The Δgxx is the only component that apparently decreases when hydrogen bonding is additionally involved. This effect is not so crucial as in the case of uncomplexed semiquinone radicals; however, the Δgxx shifts smaller than 400 ppm may be important for a proper interpretation of the high-field EPR spectra of the complicated natural systems. Thus, when very accurate theoretical values are required, the hydrogen bonding in metal complexes with o-semiquinone radicals has to be taken into account. In section 3b of this paper it was mentioned that the changes in the perpendicular components on the metal ion coordination to the semiquinone radical can be used as an important indication of hydrogen bonding formed with these radicals before the metal coordination. Even if the hydrogen bonding between the protic solvent and the radical ligand is included, the Δgyy shift is still of far greater magnitude than for the newly corrected Δgxx and the previous conclusion is still valid. The semiquinone radical derived from 1,10-phenanthroline5,6-dione (ptsq) is an ambidentate ligand and the alternative binding of metal ions via the nitrogen atoms is possible, although the experimental results suggest the coordination through the oxygen donors as most likely.13 To investigate the impact of the other coordination site on the Δg tensor, the octahedral Mg2þ complexes with N,N-chelating ptsq were optimized. Additionally, for such complexes in water the hydrogen bonding between the hydroxyl oxygens and water molecules were taken into account. The resulting structures are shown in Figure 7B and the calculated Δg tensors are listed in Table 6. The influence of the employed functional on the Δg tensor predicted for the alternative Mg2þ complex with the N,Nchelating ptsq radical was somewhat greater than that for the complex with O,O-chelating ptsq. Nonetheless, the UB3LYP and UBP86 functionals give comparable results. The values of Δg tensor components in acetonitrile for free radical (ptsqA) and those for its Mg2þ alternative complex (ptsq4AA) are in general comparable. Only Δgyy is predicted to be a bit greater for ptsq4AA and consequently Δgiso is slightly greater as well. By comparison of the Δg parameters for ptsq4W(H2O)3W with those for ptsq4WW, it is easily seen that the hydrogen bonding has a prominent effect, similar to that for the uncomplexed radical.

ARTICLE

Figure 7. Optimized structures together with corresponding names: for the Mg2þ complexes with sq and water molecules (A); for the complexes with Mg2þ coordinated to ptsq via the nitrogen atoms (B). The water molecules H-bonded to the ligands oxygen atoms are highlighted.

Summarizing, the lack of a significant impact of the Mg2þ coordination through two N donors of ptsq on the Δg tensor is somewhat unexpected, and it may prevent discriminating between the N-chelating coordination mode and free ptsq by EPR monitoring of the Δg tensor components. However, as has been shown by us previously,10j the coordination of heavier metal ions, such as Pb2þ, via an alternative binding site can have a significant effect on the EPR properties of semiquinone radicals, and so this problem should be further investigated. 3e. Comparison with the Experiment. Unfortunately, a direct comparison of the Δg tensor components with their experimental counterparts is limited, as a very few high-field experiments have been performed as yet. Therefore, the Δgiso parameter has to be put in the center of interest. 3180



ARTICLE

Table 5. Δg Tensors (in ppm) Calculated at the UB3LYP/ TZVP and UBP86/TZVP Theory Levels for the Structures with the H-Bonded Water Molecules UB3LYP/TZVP

UBP86/TZVP

Δgxx

Δgyy

Δgzz Δgiso Δgxx Δgyy Δgzz Δgiso

sq2W(H2O)2

3020

2349

-110 1753 3064 2174 -109 1710

sq2W(H2O)2W

3286

2501

-91 1898 3337 2326 -87 1859

sq3W(H2O)2

3139

2603

-94 1883 3150 2417 -96 1824

sq3W(H2O)2W

3532

2740

-96 2059 3545 2552 -98 2000

1881 1881 exptl for sq and Mg2þcomplex in watera 2332 2119 -143 1436 2279 1931 -138 1357 psq2W(H2O)2

a

psq2W(H2O)2W

2748

2344

-114 1660 2684 2145 -101 1576

psq3W(H2O)2

2593

2404

-202 1598 2494 2190 -145 1513

psq3W(H2O)2W

2918

2574

-154 1779 2804 2353 -148 1670

ptsq2W(H2O)2

2343

2192

-148 1462 2361 2042 -140 1421

ptsq2W(H2O)2W

2846

2430

-117 1720 2819 2243 -101 1654

ptsq3W(H2O)2

2600

2448

-161 1629 2564 2263 -156 1557

ptsq3W(H2O)2W

3058

2673

-167 1855 2976 2458 -163 1757

Taken from ref 17.

Table 6. Δg Tensors (in ppm) Calculated at the UB3LYP/ TZVP and UBP86/TZVP Theory Levels for Structures of ptsq with Mg2þ Coordinated via Nitrogen Atoms UB3LYP/TZVP Δgxx

Δgyy Δgzz Δgiso Δgxx

UBP86/TZVP Δgyy Δgzz Δgiso

ptsq4A

4438 4353

5 2932 4014 3962

14 2663

ptsq4AA

4355 4351

-2 2901 4092 3970

24 2695

ptsq4W

4069 3926 -54 2647 3671 3562 -46 2396

ptsq4WW

4341 4174 -46 2823 4082 3810 -25 2622

ptsq4W(H2O)3

4369 4021 -61 2776 4028 3659 -31 2552

ptsq4W(H2O)3W 4053 3629 -97 2528 3766 3369 -81 2351

The predicted Δgiso values for the tetrahedral coordination sphere tend to be less deviated from the experimental value for the Mg2þ complex with sq in water solution. Even after the inclusion of hydrogen bonding to the hydroxyl oxygens of the radical ligand, Δgiso for the octahedral coordination is inferior as compared to that for the tetrahedral one. However, the difference of about 200 ppm between Δgiso for different coordination spheres is in this case too small to reveal definitely which sphere seems to be preferred in a real system. Inclusion of the hydrogen bonding between the radical ligand and protic solvent molecules is important for all systems under investigation. For the Mg2þ complexes it results in a significant decrease of only Δgxx component, but this effect is of lower magnitude than that observed for the uncomplexed o-semiquinones. Nevertheless, the hydrogen bonding inclusion leads to better accordance between the experimental and theoretical Δgiso values for sq complexes, independently on the coordination sphere. The Δgiso values calculated for the octahedral psq complexes with Mg2þ in acetonitrile reveals better agreement with the experimental value, but the difference between Δgiso for various coordination spheres again seems to be too small to determine the favorable coordination. However, after inclusion of the

hydrogen bonding with water, the differences between the particular perpendicular components of sq2W(H2O)3W and sq3W(H2O)3W are less significant (below 250 ppm for Δgxx and Δgyy) than in the case of psq2AA and psq3AA (about 500 ppm for Δgxx and about 300 ppm for Δgyy). Hence, first the octahedral coordination sphere in acetonitrile seems to be more probable, as still the small Δgiso difference is a result of the more significant difference between the perpendicular components. Second, this fact strongly suggests that for the aprotic solvents, or in general when the hydrogen bonds are absent, the Δg tensor of o-semiquinone radical complexes appeared to be more dependent on the diamagnetic metal coordination sphere. Δgiso calculated for the ptsq complexes with Mg2þ ions are significantly overestimated as compared to the experimental value found in acetonitrile.13 However, the observed magnitudes of calculated Δg tensors for the ptsq complexes are consistent with those obtained for the sq and psq complexes. This suggests that in the case of ptsq other chemical interactions not included into the calculations can take place and influences the spin density and in consequence the Δg tensor. The coordination via the nitrogen atoms can be excluded as the Δg tensor components calculated for the corresponding ptsq4AA complex are too close to those for the free radical (ptsqA), while the experimental values are more significantly reduced. This experimental result stimulates interest also for a different reason. The comparison of the experimental Δgiso and hydrogen isotropic hyperfine coupling constants (IHCC) for the Mg2þ and Ca2þ complexes with psq reveals slight differences.13 Smaller Δgiso for the Ca2þ complex suggests a somewhat more significant redistribution of the spin density away from the hydroxyl oxygens. Although for the ptsq and its Mg2þ complex the experimental Δgiso were significantly lower than that for the Ca2þ complex, the IHCC are comparable. Therefore, these Δgiso values suggest a significant spin density redistribution as compared to the Ca2þ complex but IHCC do not. At this point the situation is unclear for us and requires further investigation. Since the direct comparison with the experiment is limited to the Δgiso values, it would be advisable to check the equivalence between the theoretical values obtained by us and the experimentally resolved g tensor components for a similar system. Pyrroloquinoline quinone (2,7,9-tricarboxypyrroloquinoline, PQQ) seems to be the best choice. This quinone cofactor, which belongs to a class of dehydrogenases known as quinonoproteins, is bonded to Ca2þ ion and exhibits EPR spectrum with the Δgxx = 3531, Δgyy = 2861, and Δgzz = -199 components.11 The magnitude of the Δg-shifts predicted by us for the o-semiquinone complexes is similar, in spite of the chemical differences, which in combination with the good agreement for Δgiso strongly indicates a high accuracy for our calculations. It is important to note that the formation of semiquinone radical complexes can be essential for EPR properties of humic acids, in which two types of radicals are recognized:7b,8c (a) stable protonated (native) and (b) short-living deprotonated (transient). The EPR studies showed that for transient radicals the Δgiso value is significantly greater. Recently, owing to HF EPR studies, the Δg tensor components were determined for both type of these humic acid radicals10i as well as for Mg2þ complex with the transient radical:10m for the transient radical gxx = 3381, Δgyy = 3181, and Δgzz = -19 and for its Mg2þ complex Δgxx = 3081, Δgyy = 2881, and Δgzz = -19. Hence, for the transient radical the decrease of perpendicular components is somewhat smaller than that predicted for the small o-semiqunones. 3181


The Journal of Physical Chemistry B It suggests that in humic acid after Mg2þ complexation a number of hydroxyl oxygens remains as the uncomplexed spin density acceptors and the total spin density amount on the hydroxyl oxygens is not significantly reduced. The increase of free radical concentration in humic acids under interaction with ions such as Mg2þ, Ca2þ, Zn2þ, or Cd2þ is a common fact.40 It was demonstrated that interaction of metal ions with o-hydroquinone forms (widely spread among humic acids) stimulates their oxidation.15 The resulting radical species, in spite of their most likely transient nature, do not reveal expectedly higher Δgiso. Our theoretical results show that the changes in Δgiso induced by the Mg2þ complexation are of a close magnitude to the difference between the deprotonated and protonated free semiquinone radicals observed in the natural solid humic acid systems, which may be the reason for mutual masking of both effects in the EPR spectra. Therefore, in the X-band EPR experiment, two signals, one from the native radicals and other form the transient radical complexes, should stay unresolved, and so the only change that can be monitored is the increase of free radical concentration. Additionally, the transformation of native forms into metal complexes of transient radicals via mechanism proposed by us previously41 cannot be excluded.

4. CONCLUSIONS Our systematic DFT study on a set of Mg2þ complexes with osemiquinone radical anions confirmed that the use of modern DFT methods, combined with an accurate approximation to the spin-orbit operator,20 allows quantitative prediction of the g tensors of diamagnetic metal ions complexes with the radical ligands. A good agreement between the theoretical and experimental Δgiso values proves that other predicted properties (spin distribution, RC-O, RMg-O) properly characterize the molecular and electronic structure of the real systems. The effects of increased aromaticity and various coordination spheres were shown to have a significant influence on the EPR properties of o-semiquinone radicals complexes with Mg2þ. Thus, the perpendicular Δg tensor components were found to be smaller due to the increasing ligand aromaticity and greater for the octahedral than for the tetrahedral coordination spheres. Therefore, the metal coordination sphere or the ligand aromaticity may be monitored via EPR spectroscopy. Different changes in the g tensor caused by metal complexation were predicted for the protic and aprotic solvents. A significant decrease of both perpendicular components was observed only in the aprotic solvent. On the other hand, when the hydrogen bonds between o-semiquinone radical and water molecules were replaced by the Mg2þ ion (protic solvent), the Δgxx component was less significantly decreased. This effect was also clearly pronounced after inclusion of the additional water molecules H-bonded to the hydroxyl oxygens in the Mg2þ complex. This tendency may be applied for the characterization of more complex biological or natural systems as smaller changes in Δgxx may be treated as a general indication that the hydrogen bonding to the radical center was present before the complexation took place. The changes in the g tensor components of the Mg2þ complexes were correlated with the spin density redistribution from the ligand hydroxyl oxygen atoms onto the ipso carbons; however, this effect is of far greater magnitude than that induced by the hydrogen bonding. It appeared that the EPR properties of

ARTICLE

the o-semiquinone complexes with the Mg2þ ions are not only affected by the C-O distances but also by O-Mg. Additionally, the contributions from the particular excited states were analyzed. The apparent reduction of Δgxx and Δgyy observed as a result of the o-semiquinone radicals complexation by the Mg2þ ions was attributed to the decrease of the HOMO-2 f SOMO and HOMO f SOMO excitation contributions, respectively. This work provided a complementary insight into the basic aspects of the interactions between radical and metal ion in correlation with EPR properties. Moreover, the species studied herein are good models and should allow to understand more complex similar systems. Our theoretical investigations provided a reasonable guess of EPR parameters and can be helpful in analysis of the EPR spectra of similar radicals and their complexes.

’ ASSOCIATED CONTENT

bS

Supporting Information. Optimized structures not shown in the text, a schematic visualization of the HOMO-2 f SOMO and HOMO f SOMO excitation contributions to the g tensor for sq, and information about principal axes of the g tensors for the structures discussed in the text. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected].

’ ACKNOWLEDGMENT This work was supported by the Polish Ministry of Science and Higher Education (MNiSW), project no. N N204 124038. The computations were performed using computers of the Wroczaw Center for Networking and Supercomputing (Grant No. 47). ’ REFERENCES (1) (a) Patai, S. Chemistry of Quinoid Compounds; Interscience: New York, 1974. (b) Trumpower, B. L. Functions of Quinones in Energy Conserving Systems; Academic Press: New York, 1982. (c) Brunmark, A.; Cadenas, E. Free Radical Biol. Med. 1987, 7, 435. (2) (a) Ferguson-Miller, S.; Babcock, G. T. Chem. Rev. 1996, 96, 2889. (b) Levanon, V.; M€obius, K. Annu. Rev. Biophys. Biomol. Struct. 1997, 26, 495. (3) Rotello, V. M. In Electron Transfer in Chemistry; Balzani, V., Ed.; Wiley-VCH: Weinheim, Germany, 2001; Vol. 4. (b) Lewis, F. D. In Electron Transfer in Chemistry; Balzani, V., Ed.; Wiley-VCH: Weinheim, Germany, 2001; Vol. 3. (4) Fukuzumi, S. In Electron Transfer in Chemistry; Balzani, V., Ed.; Wiley-VCH: Weinheim, Germany, 2001; Vol. 4. (5) (a) Duin, J. A.; Jongejan, J. A. Annu. Rev. Biochem. 1989, 58, 403. (b) Klinman, J. P.; Mu, D. Annu. Rev. Biochem. 1994, 63, 299. (c) Anthony, C. Arch. Biochem. Biophys. 2004, 428, 2. (6) Marcus, R. A. Angew. Chem., Int. Ed. 1993, 32, 1111. (7) (a) Stevenson, F. J. Humus Chemistry. Genesis, Composition, Reactions, 2nd ed.; John Wiley and Sons: New York, 1994. (b) Senesi, N., Loffredo, E. in: Sparks, E. D. Soil Physical Chemistry, 2nd ed.; CRC Press: Boca Raton, FL, 1999. (8) (a) Rex, R. W. Nature 1960, 188, 1185. (b) Steelink, C.; Tollin, G. Biochim. Biophys. Acta 1962, 59, 2534. (c) Senesi, N. Adv. Soil Sci. 1990, 14, 77.(d) Steelink, C.; Tollin, G. in: McLaren, A. D.; Peterson, G. M. Soil Biochemistry; Dekker: New York, 1967. 3182


The Journal of Physical Chemistry B (9) (a) Carrington, A.; Smith, I. C. P. Mol. Phys. 1964, 8, 101. (b) Hales, B. J. J. Am. Chem. Soc. 1975, 97, 5993. (c) O’Malley, P. J.; Babcock, G. T. J. Am. Chem. Soc. 1986, 108, 3995. (d) Lubitz, W.; Abresch, E. C.; Debus, R. J.; Isaacson, R. A.; Okamura, M. Y.; Feher, G. Biochim. Biophys. Acta 1985, 808, 464. (e) O’Malley, P. J.; Babcock, G. T. J. Chem. Phys. 1984, 80, 3912. (f) Niethammer, D.; Kirste, B.; Kurreck, H. J. Chem. Soc., Faraday Trans. 1990, 86, 3191. (g) Samoilova, R. I.; van Liemt, W.; Steggerda, W. F.; Lugtenburg, J.; Hoff, A. J.; Spoyalov, A. P.; Tyryshkin, A. M.; Gritzan, N. P.; Tsvetkov, Y. D. J. Chem. Soc., Perkin Trans. 2 1994, 609. (h) Samoilova, R. I.; Gritsan, N. P.; Hoff, A. J.; van Liemt, W.; Lugtenburg, J.; Spoyalov, A. P.; Tsvetkov, Y. D. J. Chem. Soc., Perkin Trans. 2 1995, 2063. (i) van der Brink, J. S.; Spoyalov, A. P.; Gast, P.; van Liemt, W.; Raap, J.; Lugtenberg, J.; Hoff, A. J. FEBS Lett. 1994, 353, 273. (10) (a) Calvo, R.; Abresch, E. C.; Bittl, R.; Feher, G.; Hofbauer, W.; Isaacson, R. A.; Lubitz, W.; Okamura, M. Y.; Paddock, M. L. J. Am. Chem. Soc. 2000, 122, 7327. (b) Link, G.; Berthold, T.; Bechtold, M.; Weidner, J.-U.; Ohmes, E.; Tang, J.; Poluektov, O.; Utschig, L.; Schlesselman, S. L.; Thurnauer, M. C.; Kothe, G. J. Am. Chem. Soc. 2001, 123, 4211. (c) van der Est, A.; Prisner, T.; Bittl, R.; Fromme, P.; Lubitz, W.; M€obius, K.; Stehlik, D. J. Phys. Chem. B 1997, 101, 1437. (d) Rohrer, M.; MacMillan, F.; Prisner, T.; Gardiner, A. T.; M€obius, K.; Lubitz, W. J. Phys. Chem. B 1998, 102, 4648. (e) Kamlowski, A.; Zech, S. G.; Fromme, P.; Bittl, R.; Lubitz, W.; Witt, H. T.; Stehlik, D. J. Phys. Chem. B 1998, 102, 8266. (f) Yang, F.; Shen, G.; Schluchter, W. M.; Zybailov, B. L.; Ganago, A. O.; Vassiliev, I. R.; Bryant, D. A.; Golbeck, J. H. J. Phys. Chem. B 1998, 102, 8288. (g) Zech, S. G.; Hofbauer, W.; Kamlowski, A.; Fromme, P.; Stehlik, D.; Lubitz, W.; Bittl, R. J. Phys. Chem. B 2000, 104, 9728. (h) Calvo, R.; Isaacson, R. A.; Paddock, M. L.; Abresch, E. C.; Okamura, M. Y.; Maniero, A.-L.; Brunel, L.-C.; Feher, G. J. Phys. Chem. B 2001, 105, 4053. (i) Christoforidis, K. C.; Un, S.; Deligiannakis, Y. J. Phys. Chem. A 2007, 111, 11860. (j) Witwicki, M.; Jerzykiewicz, M.; Jaszewski, A. R.; Jezierska, J.; Ozarowski, A. J. Phys. Chem. A 2009, 113, 14115. (k) Witwicki, M.; Jezierska, J.; Ozarowski, A. Chem. Phys. Lett. 2009, 473, 160. (l) Epel, B.; Niklas, J.; Sinnecker, S.; Zimmermann, H.; Lubitz, W. J. Phys. Chem. B 2006, 110, 11549. (m) Christoforidis, K. C.; Un, S.; Deligiannakis, Y. Environ. Sci. Technol. 2010, 44, 7011. (11) (a) Kay, C. W. M.; Mennenga, B.; G€orisch, H.; Bittl, R. J. Am. Chem. Soc. 2005, 127, 7974. (b) Kay, C. W. M.; Mennenga, B.; G€ orisch, H.; Bittl, R. FEBS Lett. 2004, 564, 69. (12) (a) Sato, A.; Takagi, K.; Kano, K.; Kato, N.; Duine, J. A.; Ikeda, T. Biochem. J. 2001, 357, 893. (b) Soedjak, H. S.; Cano, R. E.; Tran, L.; Bales, B. L.; Hajdu, J. Biochim. Biophys. Acta 1997, 1335, 305. (c) Yuasa, J.; Suenobu, T.; Fukuzumi, S. J. Phys. Chem. A 2005, 109, 9356. (d) Okamoto, K.; Imahori, H.; Fukuzumi, S. J. Am. Chem. Soc. 2003, 125, 7014. (e) Roy, S.; Sarkar, B.; Bubrin, D.; Niemeyer, M.; Zalis, Lahiri, G. K.; Kaim, W. J. Am. Chem. Soc. 2008, 130, 15231. (f) Itoh, S.; Taniguchi, M.; Tadaka, N.; Nagatomo, S.; Kitagawa, T.; Fukuzumi, S. J. Am. Chem. Soc. 2000, 122, 12087. (g) Kalyanaraman, B.; Felix, C. C.; Sealy, R. C. Environ. Health Perspect. 1985, 64, 185. (h) Eaton, D. R. Inorg. Chem. 1964, 3, 1268. (i) Felix, C. C.; Hyde, J. S.; Sarna, T.; Sealy, R. C. J. Am. Chem. Soc. 1978, 100, 3922. (j) Cox, N.; Jin, L.; Jaszewski, A.; Smith, P. J.; Krausz, E.; Rutherford, A. W.; Pace, R. Biophys. J. 2009, 97, 2024. (k) Debus, R. J.; Feher, G.; Okamura, M. Y. Biochemistry 1986, 25, 2276. (k) Alegría, A. E.; Sanchez-Cruz, P.; Rivas, L. Free Radical Biol. Med. 2004, 27, 1631. (13) Yuasa, J.; Suenobu, T.; Fukuzumi, S. ChemPhysChem 2006, 7, 942. (14) Felix, C. C.; Sealy, R. C. J. Am. Chem. Soc. 1981, 103, 2831. (15) Lebedev, A.; Ivanova, M. V.; Timoshin, A. A.; Ruuge, E. K. ChemPhysChem 2007, 8, 1863. (16) Mandal, R.; Salam, M. S. .A.; Murimboh, J.; Hassan, N. M.; Hakrabarti, Ch. C.; Back, M. Environ. Sci. Technol. 2000, 34, 2201. (17) Kirchner, B.; Wennmohs, F.; Ye, S.; Neese, F. Curr. Opin. Chem. Biol. 2007, 11, 134. (18) (a) Mattar, S. M. J. Phys. Chem. B 2004, 108, 9449. (b) Sinnecker, S.; Reijerse, E.; Neese, F.; Lubitz, W. J. Am. Chem. Soc. 2004, 126, 3280. (c) Kaupp, M.; Remenyi, C.; Vaara, J.; Malkina, O.;

ARTICLE

Malkin, V. G. J. Am. Chem. Soc. 2002, 124, 2709. (d) Kaupp, M. Biochemistry 2002, 41, 2895. (e) Kacprzak, S.; Kaupp, M.; MacMillan, F. J. Am. Chem. Soc. 2006, 128, 5659. (f) Kacprzak, S.; Kaupp, M. J. Phys. Chem. B 2004, 108, 2464. (g) Kacprzak, S.; Kaupp, M. J. Phys. Chem. B 2006, 110, 8158. (h) O’Malley, P. J. J. Chem. Phys. A 1997, 101, 6334. (i) O’Malley, P. J.; Collins, S. Chem. Phys. Lett. 1996, 259, 296. (j) Asher, J. R.; Doltsinis, N. L.; Kaupp, M. J. Am. Chem. Soc. 2004, 126, 9854. (k) Asher, J. R.; Kaupp, M. ChemPhysChem 2007, 8, 69. (19) Ciofini, I.; Reviakine, R.; Arbuznikov, A.; Kaupp, M. Theor. Chem. Acc. 2004, 111, 132. (20) (a) Neese, F. J. Chem. Phys. 2001, 115, 11080. (b) Neese, F. J. Chem. Phys. 2005, 122, 34107. (21) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, Jr.; J. A.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R. E. Stratmann, O. Yazyev, A. J. Austin, R. Cammi, C. Pomelli, J. W. Ochterski, R. Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, O.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, Revision A.2; Gaussian, Inc.: Wallingford. CT, 2009 (www. gaussian.com). (22) (a) Lee, C. T.; Yang, W. T.; Parr, R. G. Phys. Rev. B 1988, 37, 785. (b) Becke, A. D. J. Chem. Phys. 1993, 98, 5648. (c) Stephens, P. J.; Devlin, F. J.; Chabalowski, C. F.; Frisch, M. J. J. Phys. Chem. 1994, 98, 11623. (23) Schaefer, A.; Horn, H.; Ahlrichs, R. J. Chem. Phys. 1992, 97, 2571. (24) (a) Sobota, P.; Utko, J.; Sztajnowska, K.; Ejfler, J.; Jerzykiewicz, L. B. Inorg. Chem. 2000, 39, 235. (b) Piskunov, A. V.; Lado, A. V.; Abakumov, G. A.; Cherkasov, V. K.; Kuznetsova, O. V.; Fukin, G. K.; Baranov, E. V. Russ. Chem. Bull. 2007, 56, 97. (25) (a) Owen, J. D. J. Chem. Soc., Dalton Trans. 1978, 1418. (b) Smith, G.; O’Reilly, E. J.; Kennard, C. H. L. Polyhedron 1987, 6, 871. (c) Kennard, C. H. L.; Smith, G.; O’Reilly, E. J.; Reynolds, B. J.; Mak, T. C. W. J. Chem. Soc., Dalton Trans. 1988, 2357. (26) (a) Cances, E.; Mennucci, B.; Tomasi, J. J. Chem. Phys. 1997, 107, 3032. (b) Tomasi, J.; Mennucci, B.; Cances, E. J. Mol. Struct. (Theochem) 1999, 464, 211. (c) Tomasi, J.; Mennucci, B.; Cammi, R. Chem. Rev. 2005, 105, 2999. (27) Neese, F. ORCA—An Ab initio, DFT, and Semiempirical Electronic Structure Package, Version 2.6.35; University of Bonn: Bonn, Germany, 2007 (www.thch.uni-bonn.de/tc/orca/). (28) (a) Becke., A. D. Phys. Rev. A 1988, 38, 3098. (b) Perdew, J. P. Phys. Rev. B 1986, 33, 8822. Erratum:Perdew, J. P. Phys. Rev. B 1986, 34, 7406. (29) (a) Klamt, A.; Sch€u€urmann, G. J. Chem. Soc., Perkin. Trans. 1993, 799. (b) Sinnecker, S.; Rajendran, A.; Klamt, A.; Diedenhofen, M.; Neese, F. J. Phys. Chem. A 2006, 110, 2235. (30) Mattar, S. M. J. Phys. Chem. A 2007, 111, 251. (31) Witwicki, M.; Jezierska, J. Chem. Phys. Lett. 2010, 493, 364. (32) Kn€upling, M.; T€ orring, J. T.; Un, S. Chem. Phys. 1997, 219, 291. (33) (a) Stone, A. J. Mol. Phys. 1963, 6, 509. (b) Stone, A. J. Mol. Phys. 1964, 7, 311. (34) Schreckenbach, G.; Ziegler, T. J. Phys. Chem. A 1997, 101, 3388. (35) Amsterdam Density Functional (ADF) 2008.01; SCM, Theoretical Chemistry, Vrije Universiteit: Amsterdam, The Netherlands (http://www.scm.com). (36) Vosko, S. H.; Wilk, L.; Nusair, M. Can. J. Phys. 1980, 1200. (37) Schreckenbach, G.; Ziegler, T. Theor. Chem. Acc. 1998, 99, 71. (38) (a) Jeffrey, G. A. An Introduction to Hydrogen Bonding; Oxford University Press: New York, 1997. (b) Jeffrey, G. A.; Saenger, W. 3183



ARTICLE

Hydrogen Bonding in Biological Structures; Springer-Verlag: New York, 1991. (39) Aguilar-Martínez, M.; Macías-Ruvalcaba, N. A.; Bautista-Martínez, J. A.; Gomez, M.; Gonzalez, F. J.; Gonzalez, I. Curr. Org. Chem. 2004, 8, 1721. (40) (a) Jezierski, A.; Czechowski, F.; Jerzykiewicz, M.; Chen, Y.; Drozd, J. Spectrochim. Acta A 2000, 56, 379. (b) Jezierski, A.; Czechowski, F.; Jerzykiewicz, M.; Golonka, I.; Drozd, J.; Bylinska, E.; Chen, Y.; Seaward, M. R. D. Spectrochim. Acta A 2002, 58, 1293. (c) Jerzykiewicz, M.; Drozd, J.; Jezierski, A. Chemosphere 1999, 92, 253. (d) Jerzykiewicz, M.; Jezierski, A.; Czechowski, F.; Drozd J. Org. Geochem. 2002, 33, 265. (41) Witwicki, M.; Jaszewski, A. R.; Jezerska, J.; Jerzykiewicz, M.; Jezierski, A. Chem. Phys. Lett. 2008, 462, 300. (42) The detailed theoretical description of the L€owdin population analysis can be found in: (a) Jensen, F. Introduction to Computational Chemistry, 2nd ed.; Wiley: West Sussex, UK, 2007. (b) Szabo, A.; Ostlund, N. S. Modern Quantum Chemistry. Introduction to Advance Electronic Structure Theory; Dover: New York, 1989. (c) Neese, F., et al. ORCA Manual 2.8; available free of charge at www.thch.uni-bonn.de/tc/ orca/.

3184


Effects of Solvents, Ligand Aromaticity, and Coordination Sphere on

Recommend Documents