Electronic Structure of Biotin Conformers Studied ... - ACS Publications

Jan 31, 2018 - tetrahydrothiophene rings which are labeled A and B in Figure 1.2 ..... lone pairs and the πC O orbital of the ureido group of ring A...
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Cite This: J. Phys. Chem. A 2018, 122, 2079−2085

Electronic Structure of Biotin Conformers Studied with SAC-CI and OVGF Methods F. Abyar*,† and I. Novak‡ †

Chemical Engineering Department, Faculty of Engineering, Ardakan University, Ardakan, Iran 89518-95491 Charles Sturt University, POB 883, Orange, NSW 2008, Australia

‡

S Supporting Information *

ABSTRACT: In this work, the study was performed with 37 gasphase conformers of biotin and two biologically active conformers of biotin in the ligand−receptor complexes with astavidin and streptavidin. The ionization energies and photoelectron spectra of conformers were calculated by two methods: the general-R symmetry-adapted cluster-configuration interaction (general-RSAC-CI) method and the outer-valence Green’s function (OVGF) method. The photoelectron spectrum of each conformer was calculated using basis set D95 (df,pd) for both methods. The simulated photoelectron spectra of free molecules and bioactive conformers calculated by the two methods were compared. Natural bonding orbital (NBO) calculations were also performed for the assignment of ionization bands of each conformer. NBO calculation indicated that the first to five ionization bands correspond to ionizations from orbitals localized in the two rings. The most important point about the ionization of all conformers is that the removal of an electron from the σ-bonding orbital (C−S) takes place above 10.0 eV. bonds are stable in the gas phase.7 To the best of the authors’ knowledge, there is no comprehensive study of conformers of biotin. In this work, 37 gas-phase conformers of biotin were investigated by density functional theory (DFT) together with two conformers which were found to be biologically active (in the ligand−receptor complex). A knowledge of the electronic structure of vitamins (especially their valence ionization energies) is important for understanding their biological activity. The photoelectron spectroscopy (UPS) is one of the best methods for studying the electronic structure of molecules.8−10 The most challenging part of gas-phase photoelectron spectroscopy of biomolecules is the possible decomposition and degradation of the sample during measurement. This is why there are no reported UV photoelectron spectra (and ionization energies) for many biologically important molecules in the gas phase. Accurate computational methods can be used to simulate UPS and obtain valence ionization energies. The high-level quantum chemical calculations based on the general R-symmetry-adapted cluster configuration (general-RSAC-CI) and outer-valence Green’s function (OVGF) methods provide a good description of valence ionization processes. Despite many investigations on the chemical and structural properties of biotin, there are no literature data on its ionization energies or photoelectron spectra. As a continuation of our

1. INTRODUCTION The B7 vitamin, known as biotin, has eight different forms, but only one of them is biologically active. For example, D-biotin is biologically active while its L form is not.1 Biotin plays an important role in cell growth, and when bound to proteins, it acts as a coenzyme for carboxylase enzymes which are involved in fatty acid synthesis, gluconeogenesis, and other biochemical processes. Also, biotin acts as an coenzyme with acetyl-CoA carboxylase to catalyze carbon dioxide fixation reactions. The structure of biotin consists of a carboxyl-group-containing side chain, and two rings consist of imidazolidine-2-one and tetrahydrothiophene rings which are labeled A and B in Figure 1.2 The molecular structure and conformation of biotin have been determined experimentally in the solid state by X-ray diffraction3 as well as in bioactive conformations when bonded to protein receptors.4,5 The biotin−protein complex has the strongest known ligand-protein binding constant in molecular biology, which makes the investigation of its electronic structure especially interesting. Vitamins have many isomers which include conformers and tautomers with different biological properties. Therefore, the conformational analysis of vitamins is very important. Fraschetti et al. investigated the structure and conformation of protonated D-(+)-biotin by combined computational and Infrared Multi photon dissociation (IMD) methods in the gas phase. They found that this compound has folded structures, with one structure predominating.6 In other work, Strzelczyk et al. have shown that only folded conformers which formed intermolecular hydrogen © 2018 American Chemical Society

Received: December 22, 2017 Revised: January 30, 2018 Published: January 31, 2018 2079

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Figure 1. Optimized structures of the populated conformers of biotin. The percentages of the population of conformers have been obtained in the gas phase.

earlier work,11−14 the ionization energies were calculated and the photoelectron spectrum was simulated for conformers of biotin by using general-R-SAC-CI and OVGF methods.

energies are included in Table 1. It appears that the SAC-CI method generally underestimates the valence ionization energies of biotin. The natural bonding orbital (NBO) calculations were also performed at the DFT level of theory using the D95 (df, pd) basis set to determine the contributions of different natural bonding orbitals in the canonical molecular orbitals involved in the ionization processes which is required for spectral band assignment. The NBO calculations were performed using NBO (version 6).28

2. COMPUTATIONAL METHODS In this work, the quantum chemical calculations were performed using the Gaussian 09 Quantum Chemistry Package.15 According to the data on the PubChem Web site, biotin has 37 conformers in the gas phase.16 The geometries of these conformers were optimized in the gas phase using density functional theory (DFT) at the B3LYP/6-31+G(d) level (see Figure S1). In order to obtain their Boltzmann population ratios (BPRs), standard Gibbs free energies of conformers of biotin were also calculated at the same level of theory. It was found that seven conformers are populated in the gas phase (see Figure 1). The ionization energies of the selected conformers were calculated with general-R-SACCI17−23 and OVGF24 methods. The calculations were performed with the same basis set as the D95 (df,pd) basis set used in both methods. The intensities of ionization bands were estimated by the monopole approximation in the general-R-SAC-CI method,25 which allows the correct evaluation of relative intensities of ionization bands in molecules. The use of the OVGF method is well established in UV photoelectron spectroscopy and provides the ionization energies which agree with experimental results to better than ±0.5 eV. The accuracy of simulated PE spectra of biotin can be gauged by comparison with the experimental spectra of its composite parts (i.e., by employing an orbital interaction model such as the composite molecule method, CMM). The experimental ionization energies give an indication of how accurate our calculated ionization energies of biotin may be. Biotin contains two moieties: tetrahydrothiophene and imidazolidine-2-one, whose photoelectron spectra were recorded,26,27 and the relevant ionization

3. RESULT AND DISCUSSION 3.1. Selection of the Basis Set. There are no reported experimental photoelectron spectra of biotin, to the best of our knowledge. Therefore, the suitability of the selected basis set (D95 (df,pd)) was investigated by two computational methods. The NBO calculations show that first ionization takes place from the lone pairs of the S atom located in the tetrahydrothiophene ring (ring B in Figure 1). The values of ionization energies calculated for tetrahydrothiophene by SAC-CI were about 8.18 and 8.29 eV by the OVGF method. Tetrahydrothiophene has an ionization energy of about 8.41 eV that has been reported by Kuhn et al.27 The lowest valence ionization energies of tetrahydrothiophene as calculated by the two methods are in good agreement with the measured ionization energy of tetrahydrothiophene (see Table 1). This suggests that our theoretical methods are suitable for predicting ionization energies and simulating the UV photoelectron spectrum of biotin. 3.2. Ionization Energy and Simulated Photoelectron Spectroscopy of Biotin. As mentioned before, thermochemistry calculations performed in this work showed that only seven conformers are stable in the gas phase. The calculated photoelectron spectrum of conformers of biotin by SAC-CI and OVGF methods is shown in Figure 2. ((a) SAC-CI are indicated with 2080

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Table 1. Ionization energies (IE) of conformers of biotin and fragment molecules such as tetrahydrothiophene and imidazolidine2-one calculated by SAC-CI and OVGF with the same basis set. The experimental values of ionization energies of relevant components of biotin (tetrahydrothiophene and imidazolidine-2-one) taken from references 26, 27 are also given. conformer I II III IV V VI VII Bio-conformer avidin Bio-conformer streptavidin Tetrahydrothiophene

imidazoline-2-one

I1(eV) a

b

8.19 (0.81) 8.67c(0.905)d 8.03(0.81) 8.6 8.16(0.81) 8.66 8.16(0.81) 8.67 8.249(0.81) 8.81 8.06(0.81) 8.61 8.08(0.81) 8.61 7.97a 8.60c 7.99a 8.83c 8.18a 8.37c 8.41e (nS) 9.48a 9.5c (π-) 9.6e

I2

I3

I4

I5

I6

I7

8.38 (0.80) 9.53 (0.902) 8.24(0.80) 9.47 8.32(0.81) 9.52 8.36(0.80) 9.53 8.61(0.80) 9.77 8.27(0.80) 9.48 8.31(0.80) 9.49 8.40 9.59 8.13 9.32 10.65a 10.61c 9.50a 9.75c ( π+) 9.89e

8.77(0.79) 9.99(0.896) 8.68(0.803) 9.92 8.76(0.81) 9.97 8.79(0.80) 9.97 8.84(0.80) 9.95 8.70(0.80) 9.93 8.72(0.79) 9.95 8.62 9.64 8.33 9.74 11.588a 11.82c 11.38e (σ) 9.93a 10.38c (nO) 10.33e

9.19 (0.78) 10.85 (0.899) 9.10 (0.79) 10.79 9.15(0.78) 10.83 9.17(0.78) 10.84 9.28(0.78) 10.94 9.13(0.78) 10.8 9.14(0.78) 10.81 8.91 10.57 8.63 10.00 11.869 12.00c

10.11(0.80) 11.2(0.897) 10.23(0.81) 11.17 10.32(0.81) 11.21 10.41(0.81) 11.24 10.41(0.80) 11.32 10.28(0.81) 11.19 10.19(0.81) 11.16 10.30 11.26 10.47 11.38 12.067 12.18

10.44(0.79) 11.5(0.90) 10.64(0.81) 11.41 11.05(0.81) 11.42 10.94(0.80) 11.4 10.97(0.80) 11.36 10.80(0.81) 11.44 10.78(0.81) 11.53 10.46 11.58 10.99 11.61 12.312 12.42

11.29 (0.81) 11.86(0.901) 10.77 (0.81) 11.78 11.97(0.80) 11.98 11.81(0.81) 12.03 11.38(0.81) 12.12 11.81(0.81) 11.77 11.22(0.81) 11.66 11.40 11.71 11.67 11.92 13.665 13.84

13.50a 13.38c 13.4e

13.79 13.96

14.11 14.25

14.37 14.66

a Calculated IEs at the SAC-CI/D95(df,pd) method. bIntensity of ionization with SAC-CI theory. cCalculated IEs with OVGF with the same basis set. dPole strength of the intensities is between 0.91−0.92 so were not included in the table. eThe experimental values of ionization energies of relevant fragment molecules: tetrahydrothiophene and imidazolidine-2-one taken from refs. 26, 27.

Figure 2. Calculated photoelectron spectra of all conformers of biotin: (a) SAC-CI (solid lines) and (b) OVGF (dashed lines). Vertical lines show the energy positions of the calculated ionization bands.

calculated spectrum, the SAC-CI spectrum was shifted toward higher ionization energies with energy shifts varying between 0.35 and 0.5 eV. To simulate the photoelectron spectrum of biotin, the Boltzmann-weighted photoelectron (BWP) values of conformers were summed, as shown for two methods in Figure 3b. The seven ionization energies and the corresponding band intensities obtained with two methods are given in Table. 1. Also, pole strengths are presented, and it can be seen that all are between 0.9 and 0.92, which is consistent with a one-electron

solid lines and (b) OVGF are shown with dashed lines.) Vertical lines show the energy positions of the calculated ionization bands obtained by the two methods. The comparison between two calculated photoelectron spectra for all conformers is shown in Figure 3a. Energy deference between SAC-CI and OVGF calculated ionization with experimental values shows that the OVGF calculation is in better agreement with experiment (see Table. 1). Therefore, to adjust the position of the first peak of the OVGF calculated spectrum vs the first peak of the SAC-CI 2081

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Figure 3. (a) Comparison between the SAC-CI calculated photoelectron spectra of conformers (solid lines) with their simulated photoelectron spectra obtained with the OVGF method (dashed lines) (arrangement of conformers is the same as in Figure 2). (b) Calculated Boltzmann-weighted photoelectron (BWP) spectrum of conformers labeled with SAC-CI and OVGF.

depiction of ionization.29−31 The main electronic configuration (MEC) and assignment spectra for five ionization bands are summarized in Tables S1−S7. Also, Figures S2−S8 present the shapes of canonical molecular orbitals involved in the first five ionization bands of the conformers. 3.2.1. Photoelectron Spectra of Conformers. 3.2.1.1. Conformer I. The ionization energies and corresponding band intensities are shown in Table 1. The lowest-energy band in the calculated OVGF spectrum comprises only one ionization. As shown in Figure 3a, the SAC-CI spectrum has been shifted to higher binding energy by 0.35 eV to match the OVGF simulated spectrum. After the energy shift, the first ionization energies of conformer I calculated by the two methods are very similar. The OVGF calculation gives seven ionization bands in the simulated photoelectron spectra but only five features in the SAC-CI simulation. As shown in Figure 2a, the first feature of SAC-CI comprises two ionizations related to removing electrons from the highest occupied molecular orbital (HOMO) (no. 65 orbital) and HOMO-1, respectively. The first ionization band of conformer I is related to the ionization from the HOMO orbital. Table S1 also shows that ionization occurs from the lone pairs on sulfur in the five-membered ring (ring B). The shape of this orbital is shown in Figure S2. The second ionization band occurs from HOMO-1, which has nonbonding character, and corresponds to the linear combination of nitrogen lone pairs in ring A. The second ionization energy is higher in the OVGF calculation. The third ionization band is from HOMO-2, which is a linear combination of nitrogen lone pairs and the πCO orbital of the ureido group of ring A. The fourth ionization originates from HOMO-3 related to the oxygen lone pair in the carbonyl group of ring A. The MO corresponding to the fifth ionization band is a linear combination of two single ionized HF determinants related to HOMO-4 (major contribution) and HOMO-5. HOMO-4 is mostly related to the lone electron pairs of sulfur and the σ (S1−C9) bond, while HOMO-5 is mainly from the oxygen lone pair on CO of the COOH group and σ bonds of S1−C10 and C15−C16. The shapes of some canonical molecular orbitals of conformer I confirm that the most probable ionization occurs from these. Koopmans’ approximation states that the ionization energy approximately equals the negative value of the HF molecular orbital energy.32 The approximation does not include effects of electron

correlation or electron reorganization, which are important in determining the final value of the ionization energy. SAC-CI and OVGF consider electron correlation; therefore, it may break down the implied Koopmans’ theorem in the ionization process. It is notable that the fifth ionization energy exhibits non-Koopmans’ behavior while the Koopmans’ approximation is valid for the first four ionization bands. 3.2.1.2. Conformer II. The calculated SAC-CI spectrum of this conformer consists of five features, while its OVGF spectrum gives six features (see Figure 2a,b). The second and fifth peaks in the SAC-CI spectrum of conformer II comprise two ionizations, while the OVGF spectrum predicts a single ionization relevant to the fourth peak. As shown in Figure 2b, the OVGF simulated spectrum of conformer II has one feature less than conformer I. The first vertical ionization band of this conformer is shifted toward lower ionization energy in comparison to the SAC-CI spectrum of conformer I, while an OVGF spectrum predicts nearly the same ionization energy for the two conformers. The energy separation between the first and second ionization bands in conformer II is higher than in conformer I according to the OVGF calculations (see Figure 2b). The calculated spectrum of SAC-CI has been shifted toward higher binding energy (by about +0.48 eV) to match the position of the first calculated ionization band in the calculated OVGF spectrum. There appears to be good agreement between the shifted ionization energies obtained by OVGF with the calculated SAC-CI spectrum. The first ionization band is due to the ionization from the HOMO orbital (Table S2). The HOMO orbital originates from the S atom in the five-membered ring, similar to the assignment of conformer I. The MEC of the second ionization takes place from HOMO-1, related to lone pairs of nitrogen atoms. The third band corresponds to ionization from an orbital which can be described as a linear combination of two single ionic HF determinants of HOMO-2 and HOMO-4 with different contributions (Table S2). This ionization takes place from different sites in conformer II, while in conformer I, it happens from the HOMO-3 orbital that is mostly localized on ring A. The fourth ionization band is related to the ionization of the electron from HOMO-3 (oxygen lone electron pairs of the COOH group). Therefore, the assignment of the fourth ionization band is similar to that of conformer I (see Table S2). Similar to conformer I, the fifth ionization band is related to the linear combination of HOMO-2 and HOMO-4 2082

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As seen in Figure 2, there are six and five distinguishable peaks in the calculated photoelectron spectrum according to the SAC-CI and OVGF methods, respectively. The comparison between previous OVGF spectra with the OVGF spectrum of conformer V shows that the spectrum of conformer V is shifted to higher ionization energies. On the other hand, the SAC-CI calculation predicts a peak position similar to that of conformer I. Also, the energy gap between the second and third ionization bands of conformer V is smaller than in others. The SAC-CI spectrum was shifted to higher binding energy (by +0.5 eV) to achieve the best agreement with the OVGF spectrum. Similar to the spectra of previously described conformers, the first ionization band of conformer V corresponds to ionization from the HOMO which has sulfur lone pair character (see Table S5 and Figure S6). As mentioned earlier, the first ionization energy of this conformer is higher than others, which means that its HOMO has lower energy than other conformers. It is notable that the second ionization band originates mostly from HOMO-1, whose assignment is different from that of other conformers. HOMO-1 has nonbonding character and lone pair character localized at N5 unlike in other conformers, where electrons were removed from orbitals which were linear combinations of N5 and N6 lone pairs (see Tables S1−S5). The third ionization in conformer V should take place from HOMO-2 according to Koopmans’ theorem, but it actually corresponds to ionization from an orbital which can be described as a linear combination of three HF canonical (single-determinant) orbitals HOMO-1, HOMO-2, and HOMO-3 when electron correlation is included. It is opposite to the MEC of pervious conformers. The main electronic configuration relevant to the fourth ionization band is a linear combination of three HF single-determinant HOMO-2, HOMO-3, and HOMO-4 wave functions, unlike in other conformers. HOMO-2 predominates in the wave function of the fourth ionic state of other conformers. This implies that the extent of electron correlation in the fourth ionic state of conformer V is larger than in other conformers. Ionization in the fourth band takes place mostly from ring A and B localized orbitals. Similar to other conformers, the fifth ionization band pertains to a linear combination of HF single-determinant wave functions related to HOMO-4 and HOMO-2 (with HOMO-4 being the major contribution). It is possible that ring A ruptures in the course of this ionization because it corresponds to the electron removed from the predominantly σ-bonding orbital (S1−C9) with some sulfur lone pair character. It is evident from Table S5 that Koopmans’ theorem breaks down for the third, fourth, and fifth ionization bands in this conformer. The role of electronic correlation/reorganization is very important in these ionic states. 3.2.1.6. Conformer VI. The simulated photoelectron spectrum of conformer VI is different from the spectrum of conformer V and has some similarities to the spectra of other conformers (see Figures 2 and 3). This spectrum contains six features with an intensity ratio of 2:1:1:1:1:1: according to the SAC-CI method. The OVGF simulated spectrum also consists of six features with only the fifth feature having double intensity. As shown in Figure 3a, the SAC-CI spectrum was shifted by +0.41 eV to higher ionization energies to match the OVGF spectrum. The first ionization takes place from the HOMO with sulfur lone pair character. It is seen that the assignment of the first ionization band is thus the same as for other conformers. The MEC of the second ionization band is HOMO-1, which has nonbonding character related to nitrogen atoms of ring A. The wave function of the third ionic state is a linear combination of HOMO-4 and HOMO-2 (the latter making a major

orbitals with the nonbonding character due to lone pairs on N and O atoms. It is interesting to notice that the third and fifth ionization bands correspond to the ionization of orbitals composed of the same linear combination with different contributions. The seventh ionization band is shifted to lower energy in the two methods, but more so in OVGF than in the SAC-CI method. Koopmans’ approximation is valid for the first, second, and fourth ionization bands but not for third and fifth ionization bands. The comparison between Tables S1 and S2 confirms that the extent of electron correlation/relaxation is more significant in conformer II than in conformer I because of the failure of Koopmans’ theorem for conformer II. 3.2.1.3. Conformer III. The comparison the spectra of conformer III with conformers I and II shows that the simulated spectra are shifted to higher binding energies as predicted by the two computational methods. The calculated SAC-CI spectrum has been shifted by +0.43 eV to match the OVGF spectrum (see Figure 3). It can be seen from Figure 2 that the density of ionic states (DOS) of conformer III is lower than for conformers I and II, so the gap in energy between the ionic states of conformer III is larger than for conformers I and II. The simulated spectra of conformer III consists of six features as predicted by both the OVGF and SAC-CI methods (unlike the prediction for conformer II). In the SAC-CI spectrum, the first peak is due to the two ionizations, while the remaining peaks correspond to single ionizations. The fifth feature in the OVGF spectrum consists of two ionizations. The MECs of the ionic states of conformer III are the same as those of conformer II and are not discussed further. Figure 3 shows that the seventh ionization band of this conformer is shifted to higher binding energy as predicted by both methods. Also, the breakdown of Koopmans’ approximation for the third and fifth ionization is similar to that of conformer II. The canonical molecular orbitals of conformer III corresponding to the first five ionizations are shown in Figure S4. 3.2.1.4. Conformer IV. The simulated photoelectron spectrum of this conformer is shown in Figure 2. As seen in Figure 2, the shape of the calculated photoelectron spectrum of conformer IV is very similar to that of conformer III with a negligible difference in ionization energies. The difference between conformers III and IV is related to the rotation around the C15−C16 bond. Similar to conformer III, the first ionization band of conformer IV corresponds to the ionization from HOMO, which is a nonbonding molecular orbital (Table S4). Figure S5 shows that HOMO is mostly localized on the sulfur atom in ring B. The main electronic configuration of the second ionic state of this conformer is similar to that of conformer III with little difference in the contributing orbitals (see Table S5). The third ionization band is a linear combination of HOMO-2 and HOMO-4, with HOMO-2 making the major contribution. The MEC of the fourth ionic state occurs from the oxygen atom of ring A, which is related to the ionization from the HOMO-3 orbital. The MEC of the fifth ionic state is a linear combination of two HF determinants related to the ionization from HOMO-2 and HOMO-4 ,with the main contribution in the linear combination being provided by HOMO-4. It can be seen from Table S4 that the percentages of molecular orbitals in linear combinations are unlike that of conformer III. The shapes of the molecular orbitals of conformer IV have been shown in Figure S5. Similar to conformers III and I, the Koopmans’ approximation breaks down for the third and fifth ionization bands. 3.2.1.5. Conformer V. The calculated photoelectron spectra of this conformer are different from those of other conformers. 2083

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localized on the rings. The most important point about the photoelectron spectra of all of the conformers is that the removal of the electron from the σ-bonding bond orbital (C−S) does not take place below 10.0 eV. The relationship between the calculated electronic structure and known biological activity can be described in only in qualitative terms but is nonetheless instructive. As the 2D diagrams (Figures 4 and 5) show, the most

contribution). HOMO-2 is mostly composed of the lone electron pair at the N5 atom and the CO carbonyl group in ring A. The wave function of the fourth ionic state of conformer VI corresponds to HOMO-3. HOMO-3 has nonbonding character due to oxygen lone pairs of COOH (the oxygen atom of the carboxyl bond on ring A). Finally, the fifth ionization band is similar to the third ionization band with the contribution of the determinants related to HOMO-2 and HOMO-4, but now with HOMO-4 making the major contribution. The effect of reversal in orbital contributions is due to electron correlation. Therefore, its assignment is similar to the third ionization band and is not discussed further. Figure S7 shows the canonical molecular orbitals of conformer VI. 3.2.1.7. Conformer VII. The SAC-CI calculated spectrum of conformer VII is similar to those of all other conformers, with conformer V being an exception. The spectrum of conformer VII was shifted to lower ionization energies and consists of six features with an intensity ratio of 2:1:1:1:1:1. As can be seen from Figure 2a, the first feature comprises the two lowest-energy ionization bands. The SAC-CI simulated spectrum of this conformer has been shifted by +0.35 to higher binding energy in order to match the calculated OVGF spectrum. In addition, the shape of the OVGF photoelectron spectrum for this conformer is very different from that of other conformers. The energy separation among the fifth, sixth, and seventh ionization bands is small, which convolutes them into a single feature in this spectrum. First, ionization takes place from the HOMO which has sulfur lone pair character (see Table S7). Similar to a previous assignment, the second ionization is due to HOMO-1, which is largely from oxygen lone pairs of the CO bond of ring A. The wave function of the third ionic states of conformer VII (related to the third ionization band) is a linear combination of two ionic state HF determinants related to the ionization from HOMO-2 and HOMO-4 (with HOMO-2 making the major contribution). NBO calculations show that HOMO-2 mostly has nitrogen lone pair character localized in ring A with some admixture of the π orbital of the carbonyl group in ring A. For this ionization, Koopmans’ approximation breaks down because of the electron correlation/reorganization effects. The fourth ionization band originates from HOMO-3, where HOMO-3 has nonbonding character due to lone pairs of CO bond in ring A. Finally, removal of the electron related to the fifth ionization band is related to the orbital that is a linear combination of the HF single determinant related to HOMO-4 and HOMO-6 (with HOMO-4 making the major contribution). It is different from the assignment of the fifth ionization band in other conformers. HOMO-6 has mainly σ character related to σ(C−S) and (C11−C12) bonds. Koopmans’ approximation is not valid for the third and fifth ionization bands in this conformer. The shapes of the canonical molecular orbitals of conformer VII are shown in Figure S8.

Figure 4. View of ligand−protein interactions involving biotin and streptavidin.

Figure 5. View of ligand−protein interactions involving biotin and avidin.

important interactions between biotin and the receptor are based on the cooperative hydrogen bonding, which is unusually strong and involves the ureido moiety of the imidazolidine-2-one ring;33 it involves oxygen- and nitrogen-localized orbitals (Table 1). It is interesting that the π+ orbital (in-phase combination of nitrogen lone pairs) and no (oxygen lone pair) change their ionization energies significantly upon going from the gas-phase conformations to biologically active conformations (Table 1). This conformational readjustment leads to the lowering of ionization energies (increase in orbital energies) for π+ and no. This in turn improves the electron-donating ability of the ureido moiety which is necessary for very strong hydrogen bond formation and the tight biotin-receptor binding.

4. CONCLUSIONS The OVGF method predicts higher ionization energies for all conformers in comparison to the ionization energies obtained by the SAC-CI method. The energy deference between the SAC-CI and OVGF calculated ionization with experimental values shows that the OVGF calculation has more agreement with experiment (see Table 1 and Figure S9). In general, SAC-CI spectra have been shifted to higher binding energy to match with OVGF. On the basis of the calculations, third and fifth ionization bands are a linear combination of two HF determinants in all of the conformers expect for conformer V. NBO calculations indicate that the first five valence ionizations correspond to the orbitals 2084

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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.jpca.7b12631. Data tables and chemical structures (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected], [email protected]. Tel: 98353223240923. Fax: 983532248384. ORCID

F. Abyar: 0000-0003-0915-1529 I. Novak: 0000-0002-3413-2605 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors thank Ardakan University, Iran and Charles Sturt University, Australia for financial support.

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REFERENCES

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DOI: 10.1021/acs.jpca.7b12631 J. Phys. Chem. A 2018, 122, 2079−2085