NâHÂ·Â·Â·S Interaction Continues To Be an Enigma: Experimental and

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A: Spectroscopy, Photochemistry, and Excited States

N-H···S Interaction Continues to be an Enigma; Experimental and Computational Investigations of Hydrogen Bonded Complexes of Benzimidazole with Thioethers Sanjay J. Wategaonkar, and Aditi Bhattacherjee J. Phys. Chem. A, Just Accepted Manuscript • DOI: 10.1021/acs.jpca.8b01943 • Publication Date (Web): 11 Apr 2018 Downloaded from http://pubs.acs.org on April 12, 2018

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The Journal of Physical Chemistry

N-H···S Interaction Continues to be an Enigma; Experimental and

Computational

Investigations

of

Hydrogen

Bonded

Complexes of Benzimidazole with Thioethers

Aditi Bhattacherjee# and Sanjay Wategaonkar* Department of Chemical Sciences, Tata Institute of Fundamental Research, Homi Bhabha Road, Mumbai 400 005, India

Submitted to Journal of Physical Chemistry A

* Address for correspondence:

Sanjay Wategaonkar Telephone: 91-22-2278-2259, Fax: 91-22-2278-2106, E-mail: [email protected]

# Present address: School of Chemistry, University of Bristol, Bristol BS8 1TH, United Kingdom

1 ACS Paragon Plus Environment

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Abstract The N-H···S hydrogen bond, even though classified as an unconventional hydrogen bond, is found to bear important structural implications on protein structure and folding. In this article, we report a gas phase study of the N-H···S hydrogen bond between the model compounds of histidine (benzimidazole,

denoted

BIM)

and

methionine

(dimethylsulfide,

diethylsulfide,

and

tetrahydrothiophene, denoted Me2S, Et2S, and THT, respectively). A combination of laser spectroscopic methods such as laser induced fluorescence (LIF), 2-color resonant 2-photon ionization (2cR2PI), and fluorescence depletion by infrared spectroscopy (FDIR) is used in conjunction with DFT and ab initio calculations to characterize the nature of this prevalent H-bonding interaction in simple bimolecular complexes. A single conformer was found to exist for the BIM-Me2S complex, whereas the BIM-Et2S and BIM-THT complexes showed the presence of three and two conformers, respectively. These conformers were characterized on the basis of IR spectroscopic results and electronic structure calculations. Quantum theory of atoms in molecules (QTAIM), natural bond orbital (NBO) and energy decomposition (NEDA) analyses were performed to investigate the nature of the N-H···S H-bond. Comparison of the results with the N-H···O type of interactions in BIM and indole revealed that the strength of the N-H···S H-bond is similar to N-H···O in these binary gasphase complexes.


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1. Introduction High resolution spectroscopy in conjunction with advanced quantum chemical calculations continues to shed light on an increasingly large number of unconventional hydrogen bonds and their novel properties, both in the gas- and the condensed phase. These weak, non-covalent interactions are ubiquitous in proteins, crystals, and organometallic compounds and play a guiding role in several processes such as protein-folding, molecular self-assembly, intra- and intermolecular proton transfer, as well as stabilizing transition state structures.1-8 Although often assumed to be weak, these interactions, in some cases, are found to be surprisingly strong to the extent that they also compete with classical hydrogen bonds. This has been demonstrated in the gas phase spectroscopy of small intermolecular complexes involving S and π electrons as acceptor,9-13 or C-H as donor.14-15 The sulfur atom by virtue of its large size and lower electronegativity compared to oxygen has not quite been considered as a conventional hydrogen bond donor/acceptor. However, vacuumultraviolet-ionization detected IR predissociation spectroscopy of the H2S dimer showed it to be structurally similar to the H2O dimer; and furthermore, the SH···O H-bonding interaction was also shown to follow the acid-base formalism observed in the case of conventional H-bonds.16-18 It has also been implicated as an active hydrogen-bond acceptor in many proteins and crystals based on the bond distance/angle parameters.19-25 An infrared spectroscopic study of two methionine-containing dipeptides showed that the strength of N-H···S hydrogen bonds involving the NH groups of backbone or side-chain amides are comparable to classical intra-backbone N-H···O=C hydrogen bonds.9 These strong non-classical interactions enable the local folding of the methionine residue in the gas phase. The role of these unconventional hydrogen bonds to the structure and bioactivity of macromolecules is also notable in the examples of aliphatic C-H···S-Fe 3-center-4-electron interactions in rubredoxin and electron transfer activity in various metal-sulfur complexes.12, 26-27 Due to the omnipresence yet limited investigation of sulfur-containing hydrogen bonds, a systematic comparison of the nature, strength, and properties of sulfur with respect to oxygen as a hydrogen bond acceptor in the model compounds of tyrosine (phenols) and tryptophan (indole) was initiated and extensively characterized.28-30 The hydrogen-bonding ability of a number of solvent molecules containing oxygen or sulfur atoms as acceptor and varying in proton affinity has been reported.30 It is found that 3 ACS Paragon Plus Environment


hydrogen bonds involving sulfur possess a higher dispersion stabilization component towards the overall binding energy in comparison to oxygen which shows higher electrostatic contribution. Nevertheless, for both oxygen and sulfur, the shifts in the H-bonded O-H stretching frequency and computed binding energies of the complexes obey independent linear correlations with the proton affinity of the acceptor solvent molecule.30 These studies affirm that the O-H···S interactions confirm to several H-bonding criteria such as directionality, red-shift of the OH stretching frequencies, acidbase formalism, etc. although these are strongly dominated by dispersion interactions.30 Such detailed correlations which are useful in estimating H-bond properties from empirical observations are not available so far for N-H···O and N-H···S H-bonded imidazoles. Imidazole is the chromophore of the naturally-occurring amino acid histidine. The C-S-C covalent bridge in dimethyl sulfide (Me2S), diethyl sulfide (Et2S), and tetrahydrothiophene (THT) serves as a prototype for the sulfur acceptor in the amino acid, methionine9 as well as the vitamin, biotin.31-32 Therefore, study of the intermolecular complexes involving these two units might provide a molecular level understanding of the N-H···S interaction in proteins between methionine and the aromatic side-chain of histidine. In an earlier report, greater shift in the N-H stretching frequency in indole-Me2S compared to indole-H2O in a supersonic jet was presented as evidence that the N-H···S interaction is stronger than N-H···O.29 Using Fourier-transform infrared spectroscopy, the N-H···O and N-H···S H-bonds were found to be of similar strength in the gas-phase binary complexes of dimethylamine with dimethyl ether and dimethylsulfide at room temperature.33 Statistical survey of protein structures shows that there is widespread occurrence of the S atom in Met residues binding to the N-H of backbone amides.19-20, 34-35 The N-H···S interaction has also been reported to occur in the active site of proteins as well as in organic crystals and is classified as an unconventional hydrogen bond.27,

36-37

In this work, we study the hydrogen-bonded complexes of benzimidazole (BIM) with

three thioethers, Me2S, Et2S, and THT. BIM was chosen as a prototype because the nature of the NH···S interaction of fundamental gas-phase complexes therein (as a histidine analogue) is also expected to pave the way for a systematic understanding of similar unconventional H-bonds in indole and 3-methylindole (as a prototype for tryptophan).28-29 The objective of the present work is to


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characterize the N-H···S hydrogen bond in BIM and compare it with the spectroscopic and structural characteristics of previously reported N-H···O interactions.38 2. Methods The hydrogen bonded complexes were formed in a supersonic jet and investigated by means of UV and IR based spectroscopic techniques such as laser induced fluorescence (LIF), 2-color resonance enhanced two-photon ionization(2c-R2PI) and fluorescence depletion by infrared (FDIR) spectroscopy.39-40 In the cases where the ion signal of the complex was weak due to extensive photofragmentation, the action spectra were recorded by monitoring the fragment (monomer) mass channel. The details of the apparatus have been described earlier.41 BIM (Sigma Aldrich) was heated at 90°C in a stainless steel cell and the vapors were co-expanded with a buffer gas (Helium) through a pulsed-valve nozzle. The hydrogen bonded complexes were prepared by using a premix (0.25 to 0.5%) of solvents, namely, Me2S, Et2S, THT in Helium buffer gas. The excitation spectra of the jetcooled complexes were recorded either by monitoring the total fluorescence (LIF) or the massselected ion signal (R2PI) or the action spectrum. An Nd3+:YAG (Quantel YG781C FWHM ~ 6ns) pumped tunable dye laser (Quantel TDL 70) was used as the excitation laser. The wavelength calibration was carried out by recording the fringe spectrum of an etalon and the optogalvanic method. For recording the R2PI and action spectra, another Nd3+:YAG (Quantel Brilliant, 10 Hz, FWHM ~ 5ns) pumped dye laser (Pulsare, Fine adjustment) was used as the ionization source. The excitation and ionization laser pulses were co-propagated and focused onto the skimmed molecular beam by a 50 cm focal length quartz lens. The beams were spatially and temporally overlapped on the supersonic jet and the pulse energies were adjusted in order to make the ion signal two-color dependent. The IR spectra were recorded by counter-propagating the IR laser which preceded the UV pulse by ~50 ns. The IR spectra were recorded in between the 3600 to 2800 cm-1 spectral range and covered the fundamental NH and CH stretching regions. Typical IR pulse energies used in the experiment were < 1 mJ in the N-H region, and ~3 mJ in the C-H region. The infrared source was an Nd3+:YAG (Quantel Brilliant, 10 Hz, FWHM ~ 5ns) pumped IR-OPO operated with a LiNbO3 crystal and a bandwidth narrowing (~ 0.5 cm-1) etalon. The IR wavelength calibration was performed by



measuring and comparing the photoacoustic spectra of NH3 and CH4 gas with the reference lines provided in the HITRAN database.42 Electronic structure calculations were carried out at the DFT (using dispersion-corrected functionals) and MP2 levels to optimize the structures and calculate the binding energies and hydrogen-bonded stretching frequencies in the complexes. In addition to a strong N-H donor, BIM also possesses an activated C-H bond which may serve as a potential H bond donor. Additionally, computations were also performed to investigate the possibility of C-H···S hydrogen bond in these complexes. Atoms-in-molecules (AIM), natural bond orbital (NBO), and natural energy decomposition (NEDA) analyses were carried out to investigate the nature of the weak intermolecular interactions and corroborate the experimental findings. The Gaussian 09 suite of programs was used to compute the electronic structures of the hydrogen bonded complexes and their interaction energies.43 Geometry optimization and harmonic frequency calculation of the N-H···S and C-H···S bound complexes was carried out at different levels of DFT (B3LYP, ωB97X-D and LC-ωPBE) as well as the MP2 method using Dunning type basis sets with diffuse and polarization functions. Binding energies of the clusters were evaluated by correcting for the basis set superposition error and zero point energy. Topological parameters such as the electron density and its Laplacian at the bond critical point have been widely used to ascertain the existence and assess the strength of the hydrogen bond in intermolecular complexes and mapping out the natural bond orbitals involved in the interaction helps in estimating the bond order and the second-order interaction energy for a given complex.44-45 Therefore, the wavefunctions furnished by the quantum-chemical calculations were subjected to AIM and NBO analysis using the AIM2000 and NBO 6 programs.46-47 The interaction energy was partitioned into physically meaningful components by the energy decomposition analysis (NEDA) performed with the NBO 5.0 program linked to the GAMESS package.48-49


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3. Results (a) UV and FDIR spectroscopic results Figure 1 shows the excitation spectra of BIM with Me2S (I), Et2S (II), and THT (III). The trace (a) for each solvent shows the LIF spectra of the complexes whereas the trace (b) shows the mass-gated R2PI or the action spectra of the hydrogen-bonded clusters. The band origin (BO) transition of the BIM-Me2 S complex appeared at 35893 cm-1, red-shifted from that of BIM by 129 cm-1. This feature is confirmed to be due to the BIM-Me2S complex by recording a mass-gated 2cR2PI spectrum of the complex, shown in trace I(b). BIM-Et2S gave three major peaks in the LIF spectrum at 35892, 35856, and 35800 cm-1. The ion signal of the complex, however, was very weak and did not give a structured R2PI spectrum; hence the action spectrum of the complex was recorded by probing the fragment (monomer) mass channel under the experimental conditions (such as backing gas pressure, solvent concentration, time-delay between the laser pulse and gas pulse etc.) optimized for the excitation feature of the complex. It can be seen that the three features obtained in the LIF spectrum were reproduced in the action spectrum, confirming their origin from the hydrogen-bonded complex. The LIF spectrum of BIM-THT complex gave two new peaks at 35856 and 35816 cm-1, which were also observed in the action spectrum of the complex shown in trace III(b). It is interesting to note that the red-shifts in the BO transitions for these complexes are comparable with those found in BIM complexes with the analogous oxygen-containing solvents (Table 1), and in some cases they are even higher.38 A similar observation has also been reported for the NH···O/S bonded complexes of indole with Me2O/Me2S.29, 38 This is in contrast to the O-H···O and O-H···S bound complexes in phenol and p-cresol where the latter show smaller red-shifts in the electronic origin by 100 to 150 cm-1.30, 50 It therefore appears that sulfur-containing solvents are equally efficient as those containing oxygen in stabilizing the electronically excited-state of benzimidazole/indole via N-H···S H-bonding.



Figure 1: (Ia) LIF and (Ib) 2cR2PI spectra of BIM-Me2S, (IIa) LIF and (IIb) action spectra of BIMEt2S, and (IIIa) LIF and (IIIb) action spectra of BIM-THT complexes. The peak in the gray shaded region (36022 cm-1) is the band-origin of the monomer.

Figure 2: FDIR spectra of (a) BIM monomer, (b) BIM-Me2S, (c) BIM-Et2S, and (d) BIM-THT. For the latter two complexes, the position of the probe laser is indicated on the right.


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Figure 2(a) shows the FDIR spectrum of the BIM-Me2S complex obtained by probing its BO transition in the LIF spectrum. The N-H stretching frequency is found to be shifted from 3519 cm-1 in BIM monomer to 3317 cm-1 in the complex with a red-shift of 202 cm-1. In a previous report, the NH stretch in the BIM-Me2O complex had showed shifts in the range 150 to 250 cm-1 for its multiple conformers.38 In the C-H region of the spectrum (< 3150 cm-1) shown in Figure 2, the C-H stretches of BIM (3150-3050 cm-1) are found to be unaffected suggesting that these are not involved in complex formation. The aliphatic C-H stretches were identified below 3025 cm-1, which include the in-phase and out-of-phase asymmetric and symmetric modes of the solvent methyl groups. The FDIR spectra of the BIM-Et2S complex are shown in Figure 2(b). The three electronic transitions at 35800, 35856, and 35892 cm-1 gave different values for the ground state N-H stretching frequency at 3296, 3292, and 3302 cm-1, respectively. This suggests that these three spectral features represent distinctly different conformational isomers of the complex, all of which are held by an N-H···S H-bond. From Figure 2 it is apparent that the aromatic C-H stretches of the complex do not undergo any changes from that of the bare monomer, indicating that they remain unaffected by the intermolecular hydrogen bond. The aliphatic C-H stretches of the solvent Et2S (appearing below 3010 cm-1) show a few minor differences in the three conformers with respect to the number of peaks and their positions, suggesting that these conformations possibly arise due to different orientations of the ethyl chains, vide infra. Figure 2(c) shows the FDIR spectra of the BIM-THT complex obtained by probing the transitions at 35816 and 35856 cm-1, which gave N-H stretching frequencies at 3291 and 3294 cm-1, respectively. This similarly suggests that the two peaks correspond to two closely related conformers of the complex, both of which are bound by an N-H···S H-bond. Meanwhile, the alkyl C-H stretches of the solvent showed only minor structural differences between the two conformers (for example, peaks at 2983 and 2879 cm-1). The red shifts in the BO as well as the NH stretching frequency in the case of the BIM-Et2S and BIM-THT complexes were comparable. These values are summarized in Table 1.


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Table 1: A summary of the experimentally observed spectroscopic and computed geometrical/topological parameters of the BIM-Me2S/Me2O, BIM-Et2S/Et2O, and BIM-THT/THF complexes. The geometrical and topological parameters computed at the ωB97x-D/aug-cc-pVDZ level are presented for only those conformers that were experimentally observed (for other conformers see Table S1). N-H···S Spectroscopic Parameters ∆νel (cm-1) ∆νX-H (cm-1) Geometrical Parameters r(H···Y) (Å) R(X···Y) (Å) ∆ X-H (Å) ∠X-H-Y (°) D0 (kcal mol-1) Topological Parameters ρH-Y (au) ଶ ∇ ߩୌିଢ଼ (au)

N-H···O

BIM-Me2S

BIM-Et2S

BIM-THT

BIM-Me2O

BIM-Et2O

BIM-THF

129 202

130, 166, 222 217, 227, 223

166, 206 225, 228

102, 114, 122 184, 190, 221

160 183

192 252

BIM-Me2S (ph)

BIM-Et2S (ph, ph1,ph2)

BIM-THT (ph, im)

BIM-Me2O (ph, im, ⊥)

BIM-Et2O (lin)

BIM-THF (ph, im)

2.359 3.360 0.013 166.9 5.642

2.371, 2.368, 2.379 3.330, 3.386, 3.339 0.013, 0.013, 0.012 156.4, 176.3, 156.4 6.625, 6.444, 6.786

2.371, 2.372 3.349, 3.366 0.013, 0.013 160.3, 164.4 6.961, 5.776

1.881, 1.853, 1.961 2.862, 2.870, 2.896 0.012, 0.013, 0.010 160.4, 174.5, 151.5 6.356, 6.184, 5.246

1.925 2.942 0.011 176.5 4.919

1.849, 1.841 2.829, 2.839 0.015, 0.015 159.5, 164.1 8.169, 7.582

BIM-Me2S (ph)

BIM-Et2S (ph, ph1, ph2)

BIM-THT (ph, im)

BIM-Me2O (ph, im, ⊥)

BIM-Et2O (lin)

BIM-THF (ph, im)

0.0215 0.0471

0.0215, 0.0214, 0.0211 0.0465, 0.0459, 0.0458

0.0213, 0.0211 0.0461, 0.0460

0.0301, 0.0309, 0.0259 0.1007, 0.1077, 0.0880

0.0254 0.0892

0.0326, 0.0337 0.1099, 0.1116


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(b) Computational Results The multiple conformers considered for the BIM-Me2O complex in a previous report featured four types of conformers depending on the orientation of the C2 axis (or C-O-C angle bisector) of the solvent molecule with respect to the intermolecular H-bond.38 These included the ‘lin’ (C-O-C angle bisector collinear with the H-bond), ‘ph’ (tilted towards the phenyl group), ‘im’ (tilted towards the imidazole unit), and ‘⊥’ (perpendicular to the aromatic plane) conformers. These four types of structures were used as the initial structures for optimization of the BIM-Me2S, BIM-Et2S, and BIM-THT complexes at various levels of theory. The ‘lin’ structure was found to be universally unstable for the NH···S complexes and converged to the ‘ph’-type in most cases. Among the possible ph, im, and ⊥ conformers of the N-H···S complexes, the ⊥ conformer was found to be the most stable in most cases (Table 2) but showed the lowest NH stretching frequency red-shift. The inconsistency between various methods perhaps has to do with how the dispersion forces are handled in each method, especially when the net interaction energy of the H-bonded complexes are dominated by dispersion interaction, vide infra. It must be mentioned that both MP2 and ωB97x-D gave higher binding energy values for the various complexes as these methods account for the dispersion interaction. Although MP2 is known to overestimate the dispersion interaction, systematically larger binding energies were obtained using ωB97x-D. The binding energies obtained at LC-ωPBE were more comparable with B3LYP, although dispersion interaction is not accounted for within B3LYP. The ph and im conformers produced remarkably similar values for the H-bonded stretching frequencies as well as the binding energies, making categorical assignment to a particular conformer ambiguous. These representative structures optimized at the ωB97x-D/aug-cc-pVDZ level of theory are shown in Figures S1-S3 (see inset). At most levels of theory (including DFT and MP2), the Me2S solvent molecule was found to prefer an orientation where it is tilted towards the phenyl ring. A less probable, alternate structure of the complex is one that is bound by C-H···S interaction. Such a structure would reflect no change in the NH stretching frequency but instead show a frequency shift and concomitant increase in oscillator strength of the C-H bond, which



was not observed experimentally. The C-H···S bound structures were also found to be stable (Figure S4) implying that the sulfur atom may engage in stabilizing interactions via surrounding C-H bonds, as indeed found in protein active sites12 and supramolecular polymeric networks.7 It is sufficient to note that the computed binding energies of the C-H···S bound conformer were found to be only about 15 to 30% lower than those of the N-H···S complexes. Although the C-H···S bound structures were reasonably close in energy to the N-H···S conformers (Table 2), they were not observed in the experiment. The optimized structures of the different conformers which agree best with our experiment are discussed in Section 4.

Figure 3: Optimized structures of (a) BIM-Me2S (b) BIM-Et2S and (c) BIM-THT complexes obtained at the ωB97x-D/aug-cc-pVDZ level of theory. For all other conformers discussed in the text, see Figures S1S5.


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Table 2: Binding energies (kcal mol-1) of the N-H···S and C-H···S conformers of BIM-Me2S, BIM-Et2S, and BIM-THT computed at the various levels of theory. (Initial geometries that converged to a different conformer are indicated). Complex

BIM-Me2S

BIM-Et2S

BIM-THT

Level/Basis set B3LYP/aug-cc-pVDZ ωB97x-D/aug-cc-pVDZ LC-ωPBE/aug-cc-pVDZ MP2/aug-cc-pVDZ B3LYP/aug-cc-pVDZ ωB97x-D/aug-cc-pVDZ LC-ωPBE/aug-cc-pVDZ MP2/aug-cc-pVDZ B3LYP/aug-cc-pVDZ ωB97x-D/aug-cc-pVDZ LC-ωPBE/aug-cc-pVDZ MP2/aug-cc-pVDZ

N-H···S (ph) 3.120 5.452 3.333 5.210 3.425 6.625 3.727 ⊥ 3.395 6.961 3.681 ⊥

N-H···S (im) 3.054 5.016 3.335 ⊥ 3.408 ⊥ 3.699 ⊥ 3.395 5.776 3.613 ⊥

N-H···S (⊥) ph 5.952 ph 5.559 2.928 6.799 ph 6.433 ph 6.899 3.696 6.662

C-H···S 1.758 4.528 2.336 4.160 1.265 4.678 2.287 4.641 1.843 5.032 2.435 4.661

4. Discussion (a) Conformational assignment Figure 4 shows the comparison of the observed bound NH stretching transition with the computed frequencies (ωB97-xD/aug-cc-pVDZ) of the conformers that show the best agreement. All computed harmonic frequencies were scaled by a factor of 0.9494 to align the experimental and computed NH stretching frequencies of BIM monomer. The NH peak in the BIM-Me2S complex was found to agree well with the ph conformer (within 11 cm-1, Figure 4) whereas the im conformer at this level of theory was found to produce an imaginary frequency (torsion mode of the Me2S solvent), although the predicted NH shift for this structure agreed very well with the experiment (Figure S1). The NH stretching frequency of the ⊥ structure, which was also found to be a stationary point at this level of theory, deviated from the measured frequency by 16 cm-1. It must be emphasized that although it is difficult to unambiguously assign to a unique N-H···S bound conformer (ph, im, or ⊥), especially when the frequency shifts (Figure S1) and binding energies are quite comparable (Table 2), it is clear from the experimental results that the N-H···S interaction prevails over the weaker C-H···S interaction. 13 ACS Paragon Plus Environment


Figure 4: Comparison of the FDIR spectra of (a) BIM-Me2S, (b) BIM-Et2S, and (c) BIM-THT with the computed stick spectra (ωB97x-D/aug-cc-pVDZ) of the structures to which they were assigned.

Similarly, the ph conformer of the BIM-Et2S complex with different possible orientations of the ethyl groups (ph1 and ph 2) in the solvent molecule (Figure 3) were found to closely reproduce (within 10 cm-1) the trends in the observed frequency shifts (Figure 4). The im and ⊥ conformers deviated from the observed frequency shifts by ~ 15 to 35 cm-1 (Figure S2). Among the four possible orientations of the ethyl groups (Figure S5), conformer ph matches well with the observed NH stretching frequency corresponding to the strongest feature in the excitation spectrum at 35856 cm-1. It must be mentioned that the im conformer of the BIM-Et2S complex could not be optimized at the ωB97x-D/aug-cc-pVDZ level as it converged to the ⊥ structure. In case of the BIM-THT complex, the difference in the experimental NH stretching frequency of the two conformers (3 cm-1) was in good agreement with that calculated for the ph and im conformers at the ωB97x-D/aug-cc-pVDZ level, whereas the ⊥ conformer gave a frequency mismatch of > 80 cm-1 (Figure S3). The structures of the C-H···S bound conformer, which were not experimentally observed, are shown in Figure S4.


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(b) Comparison of N-H···S and N-H···O interactions Tables 1 and 3 list the observed spectroscopic as well as calculated geometric, topological, and NBO overlap characteristics of the N-H···O and N-H···S bound complexes in BIM for a direct comparison. Broadly speaking, the shifts in the electronic origin as well as the ground state bound NH stretching frequency are comparable for the two sets of complexes, which is also consistent with the comparable magnitudes of the relative elongation of the NH bond (10 to 13 mÅ) upon complex formation as well as the zero-point and BSSE-corrected binding energies (Table 2 and Ref. 38). However, there are subtle differences in both the cases. In the case of sulfur-containing solvents, BIM-Me2S shows a single conformer and BIM-Et2S/BIM-THT produce three/two conformers, whereas, for the oxygen-containing solvents, BIM-Me2O yields three conformers and BIM-Et2O/BIM-THF only show the presence of a single conformer. While in the case of BIM-Me2O, the three conformers were thought to arise from the different orientations of the C2 axis of Me2O with the hydrogen bond (i.e. lin, ph, im, and ⊥), the three conformers of BIM-Et2S are assigned to the different orientations of the ethyl group of the ph conformer (i.e ph, ph1, and ph2). Similar observations with respect to the number of conformations are also made in the H-bonded complexes of Indole-Me2S (1 conformer), 3-methylindole-Me2S (1 conformer) and IndoleMe2O (3 conformers).29 A single conformer was observed for the Indole-Et2O complex whereas the Indole-Et2S complex has not yet been reported. The question that remains is why a single conformer is observed for BIM-Me2S and multiple conformers for BIM-Me2O and why the situation is reversed for Et2O/Et2S. A possible explanation for the former is that the longer H···S H-bond distance in BIM-Me2S compared to the H···O bond distance in Me2O (~0.5 Å, Table 1) allows large-amplitude motions of the Me2S molecule, thereby reducing the barriers for the interconversion. The observation of the single/multiple conformers of the BIM-Et2O/Et2S and BIM-THF/THT complexes remains unexplained, however. It might involve the role of the solvent orientation with respect to the intermolecular H-bond and possible secondary interactions such as C-H···π, but requires further computational investigation.



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Figure 5: Correlation between the red-shifts of the bonded NH vibrational frequencies and proton affinity (Ref. 51) of the acceptor molecules. All of the conformers of BIM-Me2O (3), BIM-Et2S (3), and BIMTHT (2) are plotted. For the oxygen-containing solvents, a correlation of 0.845 was obtained (without considering the BIM-Et2O complex which is an outlier from destabilization of the H-bond due to steric factors). Similarly, BIM-Et2S is found to be an outlier and is not included in the fit. The correlation coefficient for N-H···S is not meaningful due to under-sampling, however, the linear scaling is shown to guide the eye. In Figure 5, the observed vibrational frequency shifts for the N-H···O and N-H···S complexes of BIM have been plotted against the proton affinity of the solvents.51 The data for the other oxygen containing solvents such as water, methanol, and ethanol are taken from previous reports.15,

41

The

correlation of the shifts with the proton affinity appears to be consistent in both cases, although the NH···S interaction in BIM lacks sufficient number of data points and needs more studies to derive a meaningful correlation. QTAIM analysis (Table 1, Figure S6) reflect slightly lower values for the electron density at the bond critical point for N-H···S H-bonds compared to the N-H···O (by 0.05 to 0.1 au). Natural bond orbital analysis shows overlap of both non-bonding (n) orbitals of the acceptor (O, S) atom with the antibonding (σ*) orbital of the donor NH bond in the H-bonding interaction. The combined second-order perturbation energies for the two n→σ* partially covalent interactions obtained from NBO analysis are also found to be comparable (Table 2, Figure S7). The acceptor S atom in the solvent molecules has two lone pairs of electrons, labeled LP(1) and LP(2). While the state of hybridization of the


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LP(1) containing orbital is ~sp0.5 for all three thioethers, that of LP(2) has very high percentage p character (> 95%). The NBO method views the H-bonding interaction as a transfer of electron density from the LP of the acceptor to the antibonding orbital (σ*) of the donor. Analysis of the N–H···S bound complexes reveal that both the lone pairs contribute towards the formation of the H-bond. However, the second order perturbation energy of the LP(1)S - σ*(N–H) overlap was only ~10% of the total whereas that of the LP(2)S - σ*(N–H) overlap was > 90%. A major difference between these two classes of Hbonds (N-H···O versus N-H···S) is found to be in the stabilization provided by the electrostatics versus dispersion components towards the overall binding energy, as shown in Figure 6 for the ph type conformer of all the complexes. It is seen that the role of dispersion interactions in stabilizing the N-H···S complexes (> 90%) is much higher than the N-H···O complexes (50-75%), although it must be pointed out that the clear demarcation of electrostatics versus dispersion-dominated stabilization that is noted for O-H···O and O-H···S H-bonded complexes, respectively, is somewhat lacking in this case.

Figure 6: Percentage contributions of the net NEDA interaction energy (inclusive of electrostatics, polarization, charge transfer, and exchange repulsion) and dispersion interaction toward the total binding energy of the N-H···S and N-H···O bound complexes of BIM (ph conformer alone) evaluated at the ωB97xD/aug-cc-pVDZ level of theory.



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Table 3: Summary of the natural bond orbital analysis of N-H···S bound complexes (BIM-Me2S, BIMEt2S, BIM-THT) and N-H···O bound (BIM-Me2O, BIM-Et2O, BIM-THF) complexes computed at ωB97xD/aug-cc-pVDZ (unless otherwise indicated for complexes where the particular conformer was found to be unstable at the chosen level of theory). Complex

Conformer

BIM-Me2S

ph ph

BIM-Et2S

ph1 ph2 ph

BIM-THT im ph BIM-Me2O

im ⊥1 lin2

BIM- Et2O ph lin2 BIM-THF

ph im

Interacting orbitals

Hybridization

LP(1)S—σ*(N-H) LP(2)S—σ*(N-H) LP(1)S—σ*(N-H) LP(2)S—σ*(N-H) LP(1)S—σ*(N-H) LP(2)S—σ*(N-H) LP(1)S—σ*(N-H) LP(2)S—σ*(N-H) LP(1)S—σ*(N-H) LP(2)S—σ*(N-H) LP(1)S—σ*(N-H) LP(2)S—σ*(N-H) LP(1)O—σ*(N-H) LP(2)O—σ*(N-H) LP(1)O—σ*(N-H) LP(2)O— σ*(N-H) LP(1)O— σ*(N-H) LP(2)O— σ*(N-H) LP(1)O— σ*(N-H) LP(2)O— σ*(N-H) LP(1)O— σ*(N-H) LP(2)O— σ*(N-H) LP(1)O— σ*(N-H) LP(2)O— σ*(N-H) LP(1)O— σ*(N-H) LP(2)O— σ*(N-H) LP(1)O— σ*(N-H) LP(2)O— σ*(N-H)

sp0.54 sp36.74 sp0.55 sp28.95 sp0.56 sp26.46 sp0.58 sp25.51 sp0.52 sp34.57 sp0.53 sp29.04 sp1.69 sp19.92 sp1.83 sp14.74 sp1.47 sp49.59 sp1.55 sp99.99 sp1.52 sp65.22 sp1.99 sp16.99 sp1.86 sp14.19 sp1.74 sp16.35

Second order perturbation energy 1.28 16.57 1.59 16.70 1.27 16.39 1.66 17.93 1.27 16.54 1.45 17.04 6.67 10.38 8.95 9.72 2.33 8.50 14.25 0.77 11.51 1.90 11.95 5.03 5.04 14.51 4.36 15.60

1: M06-2X/aug-cc-pVDZ 2: LC-ωPBE/aug-cc-pVDZ 5. Conclusion The N–H···S H-bonding interactions of BIM with three thioethers, namely, Me2S, Et2S and THT are studied and the results are put in perspective with the analogous N–H···O interactions in binary BIMether complexes. The red-shifts in the electronic origins of the sulfur-containing solvents ranged from 129 cm-1 to 222 cm-1 and were found to be higher than those of the corresponding oxygen-containing solvents (102 cm-1 to 192 cm-1). The BO transition of the BIM-Me2S complex was red shifted by 129 cm-1. Upon 18 ACS Paragon Plus Environment

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probing the electronic transitions corresponding to each of the complexes using infrared spectroscopy, it was found that the BIM-Me2S, BIM-Et2S, and BIM-THT complexes possessed one, three, and two conformers, respectively. The structures of the observed conformers are discussed by comparing the experimental spectra with those of the optimized structures obtained at the ωB97x-D/aug-cc-pVDZ level. Interestingly, the red-shifts in the H-bonded N–H stretching frequencies in case of the N–H···S complexes were found to be comparable to those of the N–H···O bound complexes. Moreover, they were found to approximate a linear correlation with the proton affinity of the acceptor molecule but showed differences in the relative role of dispersion or electrostatic stabilization. The results not only show that the strength of the N-H···S H-bonds in BIM is comparable to that of the N-H···O, but also serve as a stepping stone to elucidate the nature of intermolecular interactions in imidazole-based biomolecules, and to understand and predict the relative strengths and occurrences of these important non-covalent interactions.

Supporting Information: Comparison of the FDIR spectra with computed stick spectra for multiple conformers, optimized structures of C-H···S bound conformers, QTAIM and NBO results, and binding energies and hydrogen-bonding parameters of the complexes.

Acknowledgement: A.B. and S.W. gratefully acknowledge funding from the Tata Institute of Fundamental Research, India.



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