first-principle studies of gaseous aromatic amino acid histidine

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Journal of Molecular Structure: THEOCHEM 801 (2006) 7–20

First-principle studies of gaseous aromatic amino acid histidine

Zhijian Huang, Wenbo Yu, Zijing Lin *

Hefei National Laboratory for Physical Sciences at Microscale and Department of Physics, University of Science and Technology of China,

Hefei 230026, China

Received 9 May 2006; received in revised form 22 August 2006; accepted 23 August 2006Available online 1 September 2006

Abstract

The properties of gaseous aromatic amino acid L-histidine depend on the structural forms it may take in gas phase. Systematic ab initiocalculations were employed to characterize the conformational topology of the gaseous histidine. A total of 42 unique local minima con-formers were located at the B3LYP/6-311G* level of theory after geometry optimization of all possible single-bond rotamers. Single-point energy calculations of all conformers were performed at the levels of MP2/6-311++G(d,p), B3LYP/6-311++G(d,p) andB3LYP/6-311G(2df,p). The equilibrium distributions of the gaseous histidine conformers at various temperatures were obtained basedon the principle of thermodynamics. Due to the big energy gap between the lowest energy conformer and the other conformers, the moststable conformer of histidine is dominant in the gas phase, a unique feature that is characteristically different from that of the other threearomatic amino acids, tryptophan, tyrosine and phenylalanine. The measurable quantities such as the rotational constants, dipolemoments, vibrational spectra and ionization energies were also given for comparison with future experiments. In analyzing the structuralcharacteristics, three types of H-bond (OH� � �N3, OH� � �N4 and N3H� � �N4) were identified and characterized in detail by the atoms inmolecules (AIM) theory based upon the B3LYP/6-311++G(d,p) electron density q(r). The H-bonding features of the two most stableconformers are similar for all the aromatic amino acids. The values of vertical ionization energies for all the conformers suggest that theionization depends strongly on the type of intramolecular interaction in the neutral conformers. The average adiabatic ionization energyfor the six lowest energy conformers is lower than the corresponding average vertical ionization energy by an amount of 0.45 eV due tothe structural relaxations.� 2006 Elsevier B.V. All rights reserved.

Keywords: Histidine; Conformer; Conformational distribution; Hydrogen bond; Ionization energy

1. Introduction

The naturally occurring 20 amino acids have the samerelative stereochemistry at the a-carbon. The side chainsof the protein building blocks have different sizes, shapes,hydrogen bonding capabilities and charge distributions,which enable proteins to display a vast array of functions.The biological function of a protein or peptide is often inti-mately dependent upon the conformations that the mole-cule can adopt [1–34].

0166-1280/$ - see front matter � 2006 Elsevier B.V. All rights reserved.

doi:10.1016/j.theochem.2006.08.053

* Corresponding author. Tel.: +86 551 3606345; fax: +86 551 3606348.E-mail address: [email protected] (Z. Lin).

Of the twenty common amino acids, only tryptophan,tyrosine, phenylalanine and histidine have aromatic UVchromophores, and thus have been the subject of mostlaser spectroscopic studies on amino acids [3–12]. Theseexperimental studies have found multiple conformersfor aromatic amino acids in the gas phase. However,UV resonance enhancement of imidazole vibration isweak [13] and there has been no previous detection ofphotoproducts from direct UV irradiation of histidine.On the theoretical side, Chakrabarti and collaborators[14] have investigated the cases that the histidine ringinteracts with other aromatic and basic residues andforms hydrogen bonds with polar and charged (bothnegative and positive) residues. Moreover, many detailedtheoretical studies on the aromatic amino acids

mailto:[email protected]

Fig. 1. Schematic planar structure and atom numbering for the histidinemolecule.

8 Z. Huang et al. / Journal of Molecular Structure: THEOCHEM 801 (2006) 7–20

tryptophan [16,33], tyrosine [15,17–19] and phenylalanine[10–12] have also been reported. However, the detailedresearch on the conformational characteristics of the his-tidine molecule does not appear to be available in theliterature.

Nevertheless, the conformation of histidine is an espe-cially important model for developing the understandingof biologically interesting cation/p interactions due to itsimidazole side chain [35–37]. As experimental and theoret-ical results have shown strong conformational dependenceof phenylalanine properties [2,24,25], there are good rea-sons to believe that the properties of histidine also dependstrongly on the conformations. Therefore, a thorough andreliable theoretical study of the gaseous histidine conform-er is very much in need to provide the structural basis ofthe molecular properties and useful for the understandingof the future experiments.

One aim of the present study is to explore the confor-mational potential energy surface (PES) of gaseous histi-dine that may be helpful to elucidate future experimentsof probing the gas-phase conformers of histidine. TheDFT/B3LYP method [38,39] was used in the search ofhistidine conformers as it was known to provide accuratemolecular structures and the associated vibrational fre-quencies and infrared intensities of amino acids[10,15,20–22]. As the MP2 theory [40,41] provided betterestimate of the conformational energy than that of DFT/B3LYP when stacking interaction was involved [42,43],MP2 electronic energies were used when discussing therelative stabilities of the conformers. Moreover, as elec-trostatic interactions are ubiquitous in many proteinsand affect their structures and functions, the ionizationproperty of amino acids is an important subject on itsown. Here, we also calculated the vertical ionizationenergy of histidine molecule in the gas phase by perform-ing accurate DFT calculations.

Intramolecular hydrogen bonds are considered to bean important factor in the relative stability of amino acidconformers. The existence of an H-bond is usually deter-mined by geometric criteria by taking a cutoff distancefor near atom interactions [15,23]. However, the geomet-ric criteria may be too simplistic, and arbitrary to someextent. As the topology of the electronic charge density(q(r)) may directly characterize the intramolecular effectsand the atoms in molecules (AIM) theory [44,45] pro-vides a mathematically well defined procedure to parti-tion a molecular system into its atomic fragmentsaccording to the gradient vector field of q(r), the intra-molecular interactions and bond nature of chemicalinterest may be investigated by performing an adequateanalysis of the electronic charge density topology usingthe AIM theory [46–48]. Therefore, in addition to thegeometric criteria classification, the AIM theory isemployed here to further characterize the intramolecularhydrogen bonding properties of the histidine conformers.The AIM results are compared with the geometric crite-ria results.

2. Computational details

The conformational space of histidine was exploredthrough a systematic variation of four dihedral angles inthe molecular side chain and the fifth torsion about thebond connecting the aromatic ring with the aliphatic moi-ety, i.e., the C7AN3, C7AC6, C6AO1, C7AC8 and C8AC9

bonds (see Fig. 1). A series of trial structures were conse-quently generated by allowing for all combinations of theinternal single-bond rotamers, as shown in Fig. 2, leadingto a total of 648 possible structures for the histidine mole-cule. These trial geometries were optimized at the B3LYP/6-311G* level of theory with the GAUSSIAN 98 programpackage [49], and a set of unique conformers were locatedin the calculations. The zero-point energies and harmonicfrequencies of conformers obtained were subsequently cal-culated. Since no imaginary frequency was observed, theoptimized structures were considered as true local minima.The five lowest-lying conformers obtained at the B3LYP/6-311G* level have also been reoptimized at the B3LYP/6-311++G** and MP2/6-311++G** levels with no noticeablestructural changes, in consistent with the finding for ala-nine dipeptide [50] and tryptophan [33]. Single-point ener-gy calculations were performed at the MP2/6-311++G**,B3LYP/6-311++G** and B3LYP/6-311G(2df,p) levels oftheory for all the conformers. The conformational distribu-tions at various temperatures were calculated according tothe thermodynamics principle with the accurate ab initiodata.

The energies of the cations at these neutral structureswere calculated by setting the charge and the spin multi-plicity equal to +1 and +2, respectively. It is noted that,despite the fact that the B3LYP method is known to haveproblems with charge transfer excitations [51,52], theB3LYP results agree with the experimental ionization ener-gies of gaseous phenylalanine very well except a constantshift of 0.3 eV [24,25]. The MP2 energies, however, match

Fig. 2. Schematic illustration of the degrees of freedom of rotamers forhistidine molecule. R = imidazole ring. (a) Twofold: 0, 180; (b) sixfold: 30,90, 150, 210, 270, 330; (c) threefold: �120, 0, 120; (d) sixfold: �120, �60,0, 60, 120, 180; (e) threefold: 60, 120, 180.

Table 1Relative energies, relative zero-point vibrational energies, vertical ionization econformers of histidinea

Conformer Relative energies Relative ZPVEs

B3LYP MP2++

1 0.00 0.00 0.002 0.64 1.72 0.023 3.77 2.96 �0.484 4.42 3.30 �0.715 1.40 3.32 �0.086 3.37 3.47 �0.317 2.08 3.50 �0.408 4.62 4.05 �0.509 4.45 4.45 �0.29

10 4.19 4.66 �0.4911 5.88 4.90 �0.5912 5.39 4.97 �0.7413 5.36 5.02 �0.4114 4.74 5.18 �0.5915 6.31 5.31 �0.7516 6.23 5.35 �0.6117 5.80 5.38 �0.8118 5.87 5.40 �0.7319 6.22 5.40 �0.7220 4.72 5.41 �0.6621 5.26 5.59 �0.5222 6.48 5.61 �0.7523 4.39 5.72 �0.2424 6.54 5.85 �0.8525 6.52 5.93 �0.7426 7.29 6.14 �0.8227 5.35 6.39 �0.2528 6.63 6.42 �0.6129 7.50 6.51 �0.8330 6.24 6.56 �0.6731 7.90 6.57 �0.8632 6.85 6.67 �0.8633 7.92 6.72 �0.8734 7.27 7.07 �0.5335 7.77 7.11 �0.5136 7.49 7.13 �0.8437 8.03 7.41 �0.7238 9.66 8.36 �0.9639 9.58 8.72 �0.8040 13.78 12.14 �1.1741 13.52 12.36 �1.0042 14.15 12.68 �1.21

a Geometries optimized at the B3LYP/6-311G* level and relative energies in klevels. Relative zero-point vibrational energies (ZPVE) in kcal/mol and rotatiothe MP2/6-311++G** level. The vertical ionization energies (VIEs) in eV wercorrections at the B3LYP/6-311G* level. Note that the zero-point energies ha

Z. Huang et al. / Journal of Molecular Structure: THEOCHEM 801 (2006) 7–20 9

poorly with the experimental ionization energies of gaseousphenylalanine conformers with unknown reason. As MP2treats the neutral species well [42,43], the probable causefor the poor MP2 ionization energy is due to the inferiortreatment of the open shell systems by the MP2 method.Therefore, the vertical ionization energy here is taken tobe the difference in the B3LYP/6-311G(2df,p) energiesbetween the cationic and neutral histidine at the neutralconformation.

To study the intramolecular interactions, the electronicdensities for the optimized structures were analyzedby the AIM2000 program [53] using the B3LYP/6-

nergies, rotational data and dipole moments for the fifteen lowest energy

VIEs Rotational constants Dipole (D)

A B C

8.30 1.886 0.790 0.712 4.888.42 3.019 0.561 0.493 8.578.29 1.814 0.808 0.725 5.278.22 1.903 0.795 0.703 3.078.43 3.017 0.558 0.484 8.138.50 3.020 0.539 0.516 9.348.44 2.422 0.677 0.555 8.928.13 1.828 0.797 0.724 4.168.30 2.469 0.699 0.621 9.358.05 2.930 0.561 0.496 6.428.13 1.953 0.782 0.698 5.138.16 1.989 0.702 0.637 3.488.18 2.259 0.694 0.602 3.478.18 3.041 0.550 0.486 5.138.08 2.007 0.717 0.645 4.248.05 1.835 0.809 0.733 4.618.23 3.088 0.526 0.511 4.718.17 2.092 0.739 0.623 5.028.16 1.991 0.711 0.649 4.488.12 2.879 0.553 0.486 3.138.06 2.957 0.554 0.498 5.288.07 2.056 0.739 0.628 3.128.11 2.414 0.648 0.539 2.918.24 2.990 0.542 0.514 6.658.17 2.171 0.676 0.587 2.758.05 2.032 0.711 0.640 4.798.25 2.388 0.656 0.544 3.268.43 2.480 0.703 0.625 9.667.96 2.232 0.716 0.634 1.368.06 2.904 0.540 0.494 4.338.23 1.951 0.789 0.700 6.428.12 2.902 0.549 0.508 4.718.03 2.073 0.739 0.636 4.638.35 2.452 0.693 0.629 11.298.14 2.182 0.710 0.636 6.218.10 2.327 0.658 0.581 5.048.04 1.954 0.725 0.701 4.358.09 1.989 0.770 0.696 4.418.21 2.192 0.705 0.601 5.548.29 2.037 0.693 0.620 3.858.34 1.975 0.709 0.646 5.188.10 2.092 0.727 0.641 4.00

cal/mol at the B3LYP/6-311G* (B3LYP) and MP2/6-311++G** (MP2++)nal constants in GHZ at the B3LYP/6-311G* level, and dipole moment ate computed at the B3LYP/6-311G(2df,p) level with the zero-point energyve been scaled by the factor 0.96 [51].


311++G** densities as input, as described in AIM theory.The atomic charges were calculated using the AIM2000program by integration over the basin of every atom inthe AIM’s framework.

3. Results and discussions

3.1. Conformers and energies

From the structural point of view, histidine is a mono-substituted imidazole derivative. In the imidazolyl groupof histidine, the valence orbitals of two N atoms are bothof ‘‘sp2’’ hybridization. The imidazolyl group has the p-bond structure with six delocalized p-electrons. In the pface, the N5 atom provides two p-electrons and the N4

atom provides one p-electron. Consequently, the valenceshell of N4 atom consists of lone pair electrons with orien-tation parallel to the p face, and possesses high electroneg-ativity. The presence of two H-bond donors and fiveH-bond acceptors in histidine allows for a wide range ofH-bonding combinations.

Fig. 3. The fifteen lowest lying conformers of histid

A total of 42 local minima unique conformers of thegaseous histidine have been located in our calculations.Table 1 shows the relative energies, relative zero-pointvibrational energies, vertical ionization energies, rotationaldata and dipole moments obtained for all gaseous histidineconformers (the Cartesian coordinates of the four most sta-ble conformers can be found in the section ‘‘Appendix A’’).The structures of the fifteen lowest energy conformationsare displayed in Fig. 3. We hope that the theoretical rota-tional constants and dipole moments of histidine conform-ers listed in Table 1 can encourage future experimentalstudies of gaseous histidine conformers with the microwaveand permanent electric dipole experiments, as have beendone for alanine [54] and tryptophan [16].

The relative energies of the histidine conformers aredetermined by the interplay of the different types of hydro-gen bonds, the interaction between the amino group andthe imidazolyl ring, the interaction between the carboxyland the imidazole ring, the steric strain and the repulsionof lone pair electrons on the nitrogen and oxygen atomsand of the p electrons on the ring. In the 42 conformers

ine located at B3LYP/6-311G* level of theory.

Fig. 3 (continued )


obtained, their energies vary by �12.7 kcal/mol at theMP2/6-311++G** level of theory. According to the geo-metric criteria of judging the intramolecular hydrogenbonding and a distance of 2.80 A as a cutoff for near-atominteractions and analyzing all the stable conformersobtained, in all we find six types of hydrogen bonds: (1)N3H� � �N4 (conformers 1–3, 5, 8–10, 14, 16, 21 and 34);(2) N3H� � �OCOH (conformers 3, 4, 7, 10, 15, 18, 20, 36and 39); (3) N3H� � �OHCO (conformers 8, 11, 14, 16, 17,19, 21, 22, 24–26, 29–33, 37, 38 and 40); (4) OH� � �N3 (con-formers 1, 2, 5, 6, 13, 23, 27 and 35); (5) OH� � �N4 (con-formers 7, 9, 28 and 34); (6) OH� � �O@C (conformers 3,4, 8, 10–12, 14–22, 24–26, 29–33 and 36–39).

All conformers are stabilized by some kinds of intramo-lecular H-bonds by the geometric criteria. Conformers 1and 2 are the two most stable structures by all MP2/6-311++G**, B3LYP/6-311G*, B3LYP/6-311++G** andB3LYP/6-311G(2df,p) calculations and are stabilized bytwo H-bond interactions between the COOH group andNH2 group and between the NH2 group and the N atomof imidazolyl group. The energy gap between conformer1 and the other conformers is big at the MP2/6-311++G** level (see Table 1) and the content of conformer

1 is dominant if the temperature is not very high. It is notedthat the energy difference between conformer 1 and 2 isabout 0.6 kcal/mol by B3LYP calculations, significantlyless than the MP2 result of 1.7 kcal/mol. As the MP2 cal-culation is better than that of the B3LYP result in estimat-ing the conformational energy when stacking interaction isinvolved [42,43] and MP2 dipole moment for tryptophanagrees well with experiment [16], the MP2 energies anddipole moments are emphasized here.

Conformers 1, 2 and 5 display an intramolecular H-bond (OH� � �N3) and an additional H-bonding interactionbetween the amino group and N atom of the imidazolylring. Their zero-point vibrational energies are relativelyhigh, indicating that these structures are more rigid andcompact. Conformers 3 and 4 both have the bifurcated(N3H� � �OCOH) H-bond, and differ by a flip of the imidaz-olyl ring. Similarly, conformers 8 and 11 both have thebifurcated (N3H� � �OHCO) H-bond, and differ by a flipof the imidazolyl ring. The main difference between con-formers 3 and 8 and that between conformers 4 and 11are that the carboxyl plane rotates 180 degree around thelinking bond. The energy difference of over 1.1 kcal/molbetween conformers 8 and 3 or that between conformers


11 and 4 may be attributed to the relative weakness of theinteraction between the amino group and the hydroxyl oxy-gen atom as compared to that between the amino groupand the carbonyl oxygen atom.

Combined with the results for phenylalanine [10],tryptophan [16] and tyrosine [15], it is found that thelowest energy conformers of all the aromatic aminoacids involves the same H-bond type (COOH� � �NH2)and the attractive interaction between the amino groupand the aromatic ring, while the second lowest energyconformers have the bifurcated (NH� � �OCOH) H-bondand a gauche arrangement of the NH2 and COOHgroup with respect to the aromatic ring. However, therelative energy ordering of corresponding H-bond con-formers in the aliphatic amino acids, glycine [20], ala-nine [21] and valine [22], appear to be inverse. Theirglobal minimum conformers involve the bifurcated(NH� � �OCOH) H-bond. This suggests that the side

Fig. 4. Simulated IR spectra of the three most stable histidine conformers.The IR bands are Gaussians with the full width at half maximum(FWHM) of 8 cm�1. (a) Fingerprint region; (b) OAH stretching and NAHstretching vibration regions.

chain has a significant effect on the relative conforma-tional stability in amino acids.

3.2. IR spectra

Fig. 4 shows the simulated IR spectrum of the threemost stable conformers (the vibrational frequencies andinfrared intensities of the six most stable conformers canbe found in the section ‘‘Appendix B’’). The intramolecularinteraction has a strong influence on the IR spectrum. Forexample, there is a strong band at about 1400 cm�1, corre-sponding to OAH bending and CAO stretching vibration,in the fingerprint region of the IR spectra of conformers 1and 2 due to the formation of the OAH� � �N H-bond(Fig. 4a). This is quite different from that of conformer 3and the calculated and measured spectra of gaseous alanineand valine [21,22]. Moreover, the OAH stretching frequen-cy shifts from 3571 cm�1 for conformer 3 to 3225 and3231 cm�1 for conformers 1 and 2 (a shift of about340 cm�1) due to the OAH� � �N H-bond (Fig. 4b). Howev-er, the corresponding shifts for alanine and valine are only260 and 290 cm�1, respectively. This suggests that theOAH� � �N H-bond in histidine is stronger than that in ala-nine and valine due to the presence of aromatic ring. Weexpect the theoretical IR spectrum of histidine conformersto be useful to the future experiments as the theoretical andexperimental results are easily comparable, as the case forarginine [55,56].

3.3. Conformational distribution

The molecular partition function can be factorized intoits translational, rotational, vibrational, electronic andnuclear parts with the Born-Oppenheimer approximationand neglecting vibro-rotational coupling, i.e., q = qtrans

qrotqvibqelecqnucl. The translational and nuclear partitionfunctions are identical for all of the conformers and areirrelevant for the equilibrium distribution. The expressionsfor the calculations of the rotational, vibrational and elec-tronic partition functions can be found in Ref. [57].

Using the respective ab initio data for the conformers,i.e., rotational constants, vibrational frequencies, andground-state electronic energies, the gas-phase histidinepartition functions can be calculated and the equilibriumdistribution of conformers can be determined for anydesired temperature. The electronic partition functionswere calculated with the MP2/6-311++G** energies. Thevibrational and rotational partition functions were com-puted using the data obtained at the B3LYP/6-311G* leveland the vibrational frequencies were scaled by the factor0.96 [58]. Notice that different tautomeric forms of histi-dine may be of similar energies, e.g., the energies of thetwo most stable conformers of the tautomer with whichH14 is attached to N4 instead of N3 (see Fig. 1) are, respec-tively, 2.3 and 4.5 kcal/mol higher than histidine conformer1, however, they are not considered here as the interconver-sion between the tautomers cannot happen in most gas-


phase experiments due to the high dissociation energy ofthe NAH bond. The aggregations of histidine moleculesas well as other complexities are also not considered hereas it is possible to disperse the sample in such a way to pre-vent aggregation and selectively measure the isolated spe-cies, as has been done for several other amino acids[3–12,16,24,25,32].

Fig. 5. Contour maps of the B3LYP/6-311++G** electron density for conformatoms of the imidazole ring. The circles indicate that the atoms are in the plaindicate critical points. The outer most contour is q(r) = 0.001 au, and the remn = �3, �2, �1 and 0.

At 198 K, the lowest-energy conformer is the dominantisomer with close to 98% concentration in the gasequilibrium distribution. The concentration of the otherconformers increases slowly with increasing temperaturedue to the large electronic-energy gap between conformer1 and the other conformers. At the room temperature,the concentration of conformer 1 is still dominant with

ers 1–4 in the plane containing the alphatic moiety and the C8, C9 and N4

ne and the triangles indicate that the atoms are out of the plane. Crossesaining contours increase in the order of 2 · 10n, 4 · 10n and 8 · 10n, with


more than 80% concentration and that of conformer 2attains about 5%.

Among the four aromatic amino acids, the dominantpresence of the lowest energy conformer in the equilibriumcomposition is a distinct feature of histidine. For example,the concentrations of the most populous conformer and thesecond most populous conformer at 398 K are vastly differ-ent for histidine, while that for tryptophan [33], tyrosine[15] and phenylalanine [6,59] are similar. The conforma-tional distribution at various temperatures should be bene-ficial to future experiments of probing the gaseous histidineconformers, as demonstrated for tryptophan [16] and phen-ylalanine [10–12]. Care should be taken, though, that thetemperature distributions apply only if the equilibrium isattained. For example, it is shown that the relative popula-tions of jet-cooled molecular conformers are not consistentwith the equilibrium distributions [16,60,61]. Due to colli-sional relaxation and the disposition of energy barrierson the conformational potential energy surface, some rela-tive high energy conformers may relax into closely relatedconformers. For instance, the undetected phenylalanineconformers 4 and 8 were due to low transition barriers of0.34 and 0.94 kcal/mol between conformers 4 and 3 andbetween conformers 8 and 2, respectively [11,12,59]. Ascan be seen from Fig. 3, the six lowest lying histidine con-formers may be divided into three structurally similar pairs:conformers 1 and 6, conformers 2 and 5, and conformers 3and 4. Consistent with the extent of the structural similar-ities, the transition barriers for the three pairs are 3.2, 1.6and 0.25 kcal/mol, respectively. Clearly, conformer 5 caneasily go across the energy barrier and relax into conformer2 when cooling down and may not be detectable.

4. Intramolecular hydrogen bond

In addition to the geometric consideration, an H bond ischaracterized by [62]: (i) a weak to medium interaction

Table 2Property analysis of the bond critical points (BCPs) between H-bond acceptoB3LYP/6-311++G** level of theorya

Conformer BCP qb $2qb k1

1 OH� � �N3 0.0403 0.1103 �N3H� � �N4 0.0178 0.0602 �

2 OH� � �N3 0.0394 0.1096 �N3H� � �N4 0.0185 0.0629 �

3 N3H� � �N4 0.0150 0.0511 �5 OH� � �N3 0.0358 0.1073 �

N3H� � �N4 0.0148 0.0482 �6 OH� � �N3 0.0381 0.1096 �7 OH� � �N4 0.0442 0.1053 �8 N3H� � �N4 0.0152 0.0518 �9 OH� � �N4 0.0449 0.1066 �

10 N3H� � �N4 0.0156 0.0520 �13 OH� � �N3 0.0362 0.1082 �14 N3H� � �N4 0.0165 0.0560 �

a qb and $2qb in atomic units are the electron density and its Laplacian at theof the electron density. e is the ellipticity.

b D in A is the distance between the BCP and the corresponding RCP. Con

energy; (ii) a considerable interpenetration of the isolatedelectronic clouds of the two moieties involved; (iii) a cer-tain electron transfer between the two moieties. Combiningthese requirements with the observation based on the anal-ysis of the electron charge density (q(r)) topologies ofmany systems using the AIM theory, Popelier developeda set of eight criteria for the existence of H-bond[45,63,64]. Briefly, the eight criteria are: (1) existence of abond critical point (BCP) for the H� � �A bond; (2) the elec-tron density at the BCP is in the range of 0.002–0.035 au;(3) the Laplacian of the electron density at the BCP is inthe range of 0.024–0.139 au; (4) mutual penetration ofthe hydrogen and the acceptor atom; (5) increased netcharge of the hydrogen atom; (6) energetic destabilizationof the hydrogen atom; (7) decrease of dipolar polarizationof the hydrogen atom; (8) decrease of the hydrogen atomicvolume. In addition to the basic H-bond characteristicsmentioned above, Popelier’s criterions also quantitativelytest the existence of an H-bond. Consequently, we per-formed an analysis of the electron charge density topolo-gies by systemically applying Popelier’s eight criteria inorder to find the true AIM intramolecular H-bonds inthe histidine conformers. The B3LYP/6-311++G** densi-ties were used as they were sufficiently convergent and wereless CPU demanding than that with the B3LYP/6-311G(2df,p) densities. The 15 lowest energy conformerswere emphasized as they involve all the six types of hydro-gen bonds by the geometric criteria. q(r) is plotted for thefour most stable conformers in the plane indicated inFig. 5.

The bond critical point (BCP) and ring critical point(RCP) were found for the H-bonding types of N3H� � �N4,OH� � �N3 and OH� � �N4by the geometric criteria. As shownin Table 2, the distances between the BCPs and the RCPsare reasonably large, indicating true intramolecular H-bonds. However, no BCP and RCP were found for theH-bonds of N3H� � �OCOH, N3H� � �OHCO or OH� � �O@C

rs and H-bond donors for the 15 most stable histidine conformers at the

k2 k3 e Db

0.0582 �0.0525 0.2210 0.1075 1.020.0192 �0.0181 0.0975 0.0615 1.350.0561 �0.0504 0.2162 0.1126 1.000.0206 �0.0187 0.1022 0.1022 1.350.0154 �0.0142 0.0806 0.0856 1.270.0488 �0.0427 0.1988 0.1446 0.940.0142 �0.0125 0.0749 0.1338 1.290.0537 �0.0480 0.2113 0.1193 0.990.0717 �0.0689 0.2460 0.0416 1.910.0155 �0.0144 0.0816 0.0765 1.280.0733 �0.0703 0.2502 0.0436 1.920.0158 �0.0151 0.0829 0.0463 1.300.0498 �0.0438 0.2018 0.1369 0.950.0173 �0.0165 0.0898 0.0504 1.33

BCP. k1, k2 and k3 in atomic units are the eigenvalues of the Hessian matrix

formers are not shown in the table if no corresponding BCPs were found.


by the geometric criteria, indicating that these types ofinteractions are not true H-bonds by the AIM theory. Thatis, no H-bond is found for conformers 4, 11, 12 and 15.

Table 2 lists values of the electron density and its Lapla-cian, qb and $2qb, the bond ellipticity, e, and three eigen-values, k1, k2 and k3, of the Hessian of the density at theH-bond critical point. The qb is related to the bond orderand thus to the bond strength [65]. As shown in Table 2,all H-bonds are typical close-shell interactions as the valuesfor $2qb lie in the proposed range of 0.014–0.139 au [65]. qb

is the biggest (0.442 and 0.449 au, respectively) and e is thesmallest (0.0416 and 0.0436, respectively) in the OH� � �N4

H-bonds of conformers 7 and 9. This suggests that the

Table 4Integrated atom properties of the H12 and H13 atoms in the amino group for

Conformer q (X) E (X)

H12 H13 H12 H

1 0.345 0.393 �0.495 �2 0.339 0.401 �0.498 �3 0.340 0.374 �0.497 �4 0.333 0.341 �0.500 �5 0.329 0.386 �0.501 �6 0.348 0.353 �0.494 �7 0.334 0.341 �0. 501 �8 0.338 0.375 �0. 500 �9 0.334 0.340 �0.500 �

10 0.347 0.373 �0.492 �11 0.331 0.342 �0. 502 �12 0.336 0.336 �0.498 �13 0.347 0.349 �0.494 �14 0.337 0.379 �0.499 �15 0.331 0.342 �0.500 �

H13 denotes the hydrogen with higher AIM atomic charge and is the hydrogea q (X) is the atomic charge, E (X) the total energy, l (X) the dipolar polari

Table 3Integrated atom properties of the H20 atom in the carboxyl group for the15 most stable histidine conformers and the reference conformer 41 whereH20 is not involved in H-bondinga

Conformer q (X) E (X) l (X) V (X)

1 0.599 �0.355 0.140 16.312 0.598 �0.355 0.141 16.573 0.577 �0.372 0.164 22.784 0.583 �0.369 0.162 22.625 0.599 �0.356 0.143 16.896 0.595 �0.358 0.142 16.717 0.617 �0.344 0.118 12.698 0.577 �0.373 0.163 22.749 0.617 �0.345 0.117 12.41

10 0.579 �0.372 0.162 22.7411 0.580 �0.371 0.162 22.6312 0.575 �0.374 0.164 23.0613 0.594 �0.359 0.144 17.0514 0.581 �0.371 0.162 22.6015 0.575 �0.373 0.164 22.9141 0.554 �0.389 0.166 21.86

a q (X) is the atomic charge, E (X) the total energy, l (X) the dipolarpolarization, and V (X) the atomic volume. All values are in atomic units.

OH� � �N4 H-bond is the strongest among the three typesof H-bonds and the N4 atom is the best H-bond acceptor.According to the data for qb and $2qb in Table 2, theN3H� � �N4 bond is much weaker than the OH� � �N4 bond.There are the same intramolecular H-bond interactions inconformers 1, 2 and 5. The values of qb and $2qb of theOH� � �N3 H-bond for conformers 1, 2 and 5 decrease from0.0403 to 0.0358 and from 0.1103 to 0.1073 au, respective-ly, and that of the ellipticity increase from 0.1075 to0.1446, clearly reflecting the energy ordering of the threeconformers.

As noted by passing, some conformers such as conform-ers 23 and 27 seem to have the C@O� � �HC(r) (r denotesthat the C atom is on the imidazolyl ring) H-bonding inter-action. But the C@O� � �HC(r) path (not shown here inFig. 3) is noticeably inwardly curved away from the perim-eter of the ring and qb and $2qb at the RCP are very small,both features indicate that the C@O� � �HC(r) H-bond isvery weak and unstable and is not viewed as a true H-bond[44].

Table 3 lists the AIM integrated properties for the H20

atom on the carboxyl group in the 15 lowest-lying con-formers and conformer 41 where H20 is not involved inH-bonding and used as the reference. As shown in Table3, the increase of hydrogen atomic positive charge, energet-ic destabilization, decrease of dipolar polarization, anddecrease of atomic volume are evident in conformers 1, 2,5, 6, 7, 9 and 13, further confirming the H-bond formationinvolving H20 in these conformers. Moreover, the values ofhydrogen atomic charge and energy of conformers 7 and 9are substantially larger than those for conformers 1, 2, 5, 6and 13, and the values of dipolar polarization and atomicvolume of conformers 7 and 9 are both lower than thoseof conformers 1, 2, 5, 6 and 13. This also validates thatthe OH� � �N4 hydrogen bond is stronger than the OH� � �N3

the 15 most stable histidine conformersa

l (X) V (X)

13 H12 H13 H12 H13

0.471 0.188 0.157 33.31 25.690.468 0.188 0.155 33.44 25.140.481 0.186 0.167 32.50 27.590.495 0.191 0.189 33.91 32.920.475 0.192 0.165 34.32 27.710.489 0.185 0.185 32.91 31.990. 496 0.190 0.187 33.72 32.720. 481 0.184 0.167 32.21 27.540.497 0.189 0.190 32.84 33.810.482 0.189 0.164 31.85 27.400. 496 0.190 0.187 34.10 32.310.498 0.192 0.191 34.24 34.090.492 0.185 0.188 33.06 32.790.478 0.190 0.166 32.79 27.100.494 0.195 0.192 34.53 33.51

n involved in the NH� � �N H-bond wherever exists.zation, and V (X) the atomic volume. All values are in atomic units.


bond. It is worthy noting that conformers with the same H-bond type have similar atomic charges, while atomic charg-es for conformers of different H-bond types are quite differ-ent. The atomic charges for H20 in conformers withOH� � �N3 and OH� � �N4 H-bonds are around 0.597 and0.617 au, respectively, as compared to the reference valueof 0.554 au in conformer 41. Even though not involvedin true AIM H-bonds, the H20 charges for conformers withthe geometric OH� � �O H-bonds are in the range of 0.575 to0.583 au, indicating some stabilization effect andaccounting for the relative low energies of conformers 3and 4.

Table 4 lists the AIM integrated properties for the H12

and H13 atoms on the amino group of the alphatic moietyin the 15 most stable conformers. Compared with noN3H� � �N4 H-bond cases, the atomic charges and energiesincrease and the magnitudes of the dipolar polarizationsand the atomic volumes decrease for all the H atomsinvolved in the N3H� � �N4 H-bond. Like the fulfillment ofthe other AIM criterions, this also validates the existenceof the N3H� � �N4 H-bond.

It is noted that the AIM criterion of mutual penetrationof hydrogen and acceptor atom is fulfilled in all the caseswith BCPs and RCPs, as partially displayed in Fig. 5. Eventhough this criterion concerns a fundamental feature of theH-bond formation, it appears that the criterion can be eas-ily met if other AIM criterions are met.

From the above discussion, three types of interactionsbetween the H-bonding acceptors and H-bonding donors(OH� � �N3, OH� � �N4 and N3H� � �N4) satisfy the eightAIM criterions. According to the relationship betweenthe H-bond energy (EHB) and the potential energy densityat the bond critical point (Vcp) [66], EHB ¼ 1

2V cp, the

average H-bond energies are: EHB(OH� � �N3) = �10.1kcal/mol, EHB(OH� � �N4) = �12.1 kcal/mol and EHB

(N3H� � �N4) = �3.0 kcal/mol, corresponding to moderatelystrong, strong and weak H-bond, respectively [62].However, the N3H� � �OCOH, N3H� � �OHCO andOH� � �O@C H-bonds by the geometric criteria have notbeen found in the AIM study, indicating that the AIM cri-teria for H-bond is more stringent than that of the conven-tional geometric criteria, consistent with the finding ofRefs. [46,67]. As AIM indicates only a weak N3H� � �N4H-bond for conformer 3 and no H-bond for conformer 4,the geometric criteria for H-bond is by itself of supplemen-tal use for explaining the relative conformer stabilities.

4.1. Conformation-dependent ionization energies

B3LYP calculations with quality basis sets are known togive good results for molecular ionization energies [24]. Forexample, the theoretical vertical ionization energy (VIE) val-ue for imidazole is 8.85 eV by our B3LYP/6-311G(2df,p)calculations, in good agreement with the experimental valueof 8.81 eV [68]. The B3LYP/6-311G(2df,p) values of VIE forthe histidine conformers are listed in Table 1. The theoreticalVIE results should be verifiable through measurements such

as the photoionization efficiency experiment for phenylala-nine [24,25].

Notice that the VIE of imidazole is comparable to thatof histidine conformers. This indicates that the first ioni-zation of histidine is the detachment of a delocalized p-electron of imidazolyl group. From Table 1 and Fig. 2,the conformers were found to be of higher VIEs whenthe positively charged hydrogen end of the amino or car-boxyl group interacts with the imidazolyl group of histi-dine. This can be ascribed to that the attractiveinteraction through the intramolecular H-bond betweenthe positively charged hydrogen and p-electron systemof the aromatic ring becomes a repulsive one upon ioni-zation due to the newly formed positive charge on theimidazolyl ring. The VIE of conformer 6 is the highest(8.50 eV) amongst all conformers due to the strongattraction between the amino group and the p-electronsystem of the aromatic ring. On the other hand, the con-formers possess lower VIEs when the lone-pair electronsof the oxygen or nitrogen atom have a direct interactionwith the p-electron system, e.g., the VIEs for conformers22 and 29 are, respectively, 8.07 and 7.96 eV. Whendetaching a delocalized p-electron upon the aromatic ringin these conformers, the repulsive interaction between thelone-pair electrons of the heavy atom and the p-electronsystem becomes an attractive one. That suggests that thevertical ionization energy of histidine depends on the typeof intramolecular interaction in the neutral conformers, asituation similar to that of phenylalanine [24,25]. Weexpect the other aromatic amino acids to behave in asimilar way.

It is worthy noting that the cationic conformers mayexperience significant structural relaxation so as to mini-mize their conformational energies and the equilibrium oradiabatic ionization energies (AIE) may be substantiallylower. For example, five cationic histidine conformers werelocated after the geometry relaxation of the six lowest-lyingionic conformers at the initial neutral conformer geome-tries by the B3LYP/6-311G(2df,p) optimizations, with con-former 5 relaxes to the same ionic structure as that ofconformer 2. No imaginary frequency was found for thefive optimized cationic conformers and they were true localminima. The corresponding adiabatic ionization energiesof the six lowest histidine conformers are 7.92, 8.09, 7.63,7.76, 8.06 and 8.03 kcal/mol, respectively.

5. Summary

With a total of 648 exhaustive trial structures deter-mined by all combinations of internal single-bond rotamersof the gaseous histidine molecule, 42 unique local minimumconformers are identified based on the geometry optimiza-tion at the B3LYP/6-311G* level of theory and their dipolemoments, vibrational frequencies, rotational constants areobtained. Six types of H-bonds, N3H� � �N4, N3H� � �OCOH,N3H� � �OHCO, OH� � �N3, OH� � �N4 and OH� � �O@C, arefound by the geometric criteria with a cutoff distance of


2.8 A. All conformers are stabilized by some kinds ofintramolecular H-bonds. The two most stable structures,conformers 1 and 2, are stabilized by two H-bond interac-tions between the COOH group and NH2 group andbetween the NH2 group and the N atom of imidazolylgroup, a common feature of the gaseous conformationsof all aromatic amino acids. This feature is characteristical-ly different from that of the aliphatic amino acids with theglobal minima involving the bifurcated NH� � �OCOHbonds, suggesting the significant effect of the side chainon the relative stabilities of amino acid conformers.

The theoretical conformational distributions at var-ious temperatures were estimated based on the MP2/6-311++G** electronic energies and B3LYP/6-311G*

frequencies. The conformer 1 is dominant due tothe large electronic energy gap between the conformer1 and the other conformers. However, the gaseoushistidine may be viewed as a genuine multi-conformersystem above the vaporizing temperature as severalconformers are of sufficiently high concentrations formeasurements.

The intramolecular H-bonding properties of the 15 moststable conformers have also been investigated by the AIMtheory with the B3LYP/6-311++G** densities. Only three‘‘real’’ types of H-bonds, namely, OH� � �N3, OH� � �N4

and N3H� � �N4, were found in these conformers. TheOH� � �N4 bond is the strongest while the N3H� � �N4 bondis the weakest. AIM explains the energy ordering well forconformers involving the same H-bond type. Similar tothe previous finding in the other amino acid systems, theH-bond types of N3H� � �OCOH, N3H� � �OHCO andOH� � �O@C by the geometric criteria fail to meet theAIM test. The geometric criteria appears to be useful inexplaining the relatively low energy of conformer 3 involv-

ing a weak AIM N3H� � �N4 bond and that of conformer 4with no AIM H-bond.

The vertical ionization energies of all the neutral con-formers are given at the B3LYP/6-311G(2df,p) level. TheVIEs of histidine conformers are comparable to that ofimidazole, indicating that the first ionization of histidineis the detachment of a delocalized p-electron of imidazolylgroup. Similar to the finding in phenylalanine, the VIEs ofhistidine conformers depend on the types of intramolecularinteraction in the neutral conformers. Higher VIEs arefound for conformers with the amino or the carboxylhydrogen interacting with the imidazolyl group, while low-er VIEs are found for conformers with the lone-pair elec-trons of the oxygen or nitrogen atom interacting with thep-electron system. The adiabatic ionization energies ofthe six lowest-lying conformers are also obtained at theB3LYP/6-311G(2df,p) level. The average AIE for the sixlowest energy conformers is lower than the correspondingaverage VIE by an amount of 0.45 eV due to structuralrelaxation.

There have been numerous experimental studies of ami-no acid conformations in gas phase and there is no princi-ple difficulty associated with histidine in comparison with,say, phenylalanine and valine, we hope there will be mea-surements on histidine soon. The theoretical results forthe conformer distributions, rotational constants, dipolemoments, IR spectra and ionization energies presentedhere should be helpful to the respective measurements inthe future.

Acknowledgement

Z.L. thanks the financial support of the National Natu-ral Science Foundation of China (Grant No. 10574114).

Appendix A

The Cartesian coordinates (A) of the four lowest energy conformers of gaseous histidinea

Numbering Atom Conformer 1 Conformer 2

X
Y Z X Y Z
1
O 1.562044 �0.815730 �2.063600 �1.069043 0.362343 �3.212748 2 O 1.172126 1.378350 �1.839524 �2.367103 �1.061196 �2.065909 3 N �0.790503 �1.599453 �1.346519 0.981120 0.176354 �1.651663 4 N �0.805286 �0.788469 1.573886 1.457062 0.771983 1.253999 5 N 0.544576 0.473795 2.784646 1.129617 �0.100852 3.256370 6 C 0.781018 0.239802 �1.819476 �1.344410 �0.437463 �2.176292 7 C �0.692777 �0.141101 �1.538816 �0.232611 �0.453600 1.105000 8 C �1.266005 0.714874 �0.389017 �0.745625 0.307687 0.135773 9 C �0.626437 0.427136 0.933837 0.180650 0.240256 1.309756
10
C �0.091176 �0.724941 2.674575 1.994659 0.550200 2.430895 11 C 0.214495 1.218841 1.672424 �0.036840 �0.306736 2.548521 12 H �1.623967 �1.975139 �1.781422 1.505295 0.641302 0.913673 13 H �0.832690 �1.818381 �0.352214 1.591138 �0.520346 2.065637
(continued on next page)


Appendix A (continued)

Numbering
Atom Conformer 1 Conformer 2
X
Y Z X Y Z
14
H 1.148609 0.765415 3.535989 1.300736 �0.371230 4.211373 15 H �1.232959 0.119617 �2.455899 �0.080382 �1.502145 �0.824928 16 H �2.343376 0.530001 �0.324471 �1.720914 �0.104069 0.400992 17 H �1.125450 1.765834 �0.646161 �0.904963 1.355152 0.146991 18 H �0.001885 �1.503553 3.417585 2.989785 0.836898 2.737211 19 H 0.611451 2.205428 1.498318 �0.890090 �0.805097 2.979637 20 H 0.970686 �1.598973 �1.951985 �0.170964 0.725909 �3.021590
Conformer 3
Conformer 4
1
O �1.805948 �1.531480 �0.984729 �0.072362 �2.067696 �1.329334 2 O 0.305629 �2.280945 �1.103879 1.312214 �0.622921 � �2.350768 3 N �1.051693 1.055966 �1.894320 �2.071566 0.083022 �1.028900 4 N �0.152890 1.571295 1.005637 1.242805 0.136999 1.140287 5 N 0.641893 0.486324 2.759800 � �0.020070 0.436312 � 2.932901 6 C �0.645477 �1.318699 1.225344 � 0.172761 0.947832 �1.699340 7 C �0.065330 �0.000178 1.745270 � �0.748112 0.262593 �1.526247 8 C 1.120241 0.476817 0.873397 �0.093709 1.335134 �0.617941 9 C 0.782163 0.646300 0.576816 0.131460 0.880695 0.791179
10
C �0.212506 1.447718 2.310174 1.120917 �0.109737 2.422225 11 C 1.283130 �0.037438 1.656211 � �0.665034 1.073881 1.893279 12 H �1.926735 0.663653 2.226573 � �2.513768 �0.737678 �1.666833 13 H �1.239718 1.471884 0.985456 �1.968969 �0.585885 �0.151451 14 H 0.785325 0.210885 3.717754 � �0.331195 0.394659 3.889817 15 H 0.346644 �0.240564 2.735377 � �0.859788 0.714481 �2.518013 16 H 1.446868 1.433311 1.292078 � �0.758047 2.202086 �0.629833 17 H 1.945902 �0.229419 0.974207 0.862269 1.632536 �1.053415 18 H �0.846002 2.019802 2.971966 1.818471 �0.668796 3.028766 19 H 2.013298 �0.826580 1.735780 � �1.601315 1.591625 2.026259 20 H �0.146290 �3.084992 0.804851 1.865643 �1.418516 �2.373426
a Frequencies (mi; freq) in cm�1; intensities (int) in km/mol. All theoretical data were obtained at the B3LYP/6-311G* level of theory. The scale factor of0.96 was used for frequencies. Vibrational mode 39 corresponds to the CAO str & OAH bending, mode 45 corresponds to the C@O str. In the conformers1, 2, 5, and 6, vibrational mode 54 corresponds to the NAH (on the ring) str, modes 52 and 53 correspond to NH2 (str sym) and NH2 (str asym),respectively, and mode 51 corresponds to the OAH str. In the conformers 3 and 4, vibrational mode 54 corresponds to the OAH str, mode 53 correspondsto the NAH (on the ring) str, and modes 51 and 52 correspond to NH2 (str sym) and NH2 (str asym), respectively. Abbreviations: str, stretching; sym,symmetric; asym, asymmetric.

Appendix B

Vibrational frequencies and infrared intensities of the six most stable histidine conformersa

m 1 2 3 4 5 6
i
Freq
Int Freq Int Freq Int Freq Int Freq Int Freq Int
1
48 8.4 48 7.2 42 3.4 32 11.0 39 9.6 39 2.9 2 60 4.3 68 2.8 51 1.2 55 3.7 68 2.2 53 2.1 3 70 9.4 94 2.2 65 1.6 67 0.4 83 1.9 71 1.5 4 150 5.2 117 7.6 139 2.3 105 1.6 126 6.9 98 2.6 5 216 0.4 190 4.4 201 4.2 192 22.0 216 6.4 187 6.1 6 296 16.2 299 3.9 265 33.5 218 55.3 280 16.1 275 26.0 7 332 22.3 318 14.4 291 2.5 267 6.0 307 9.8 284 9.6 8 348 15.7 351 4.5 301 40.8 286 2.4 346 1.2 335 14.2 9 375 2.5 378 27.2 362 13.4 365 13.1 374 29.5 349 8.2


Appendix B (continued)

mi
1 2 3 4 5 6
Freq
Int Freq Int Freq Int Freq Int Freq Int Freq Int
10
477 5.7 413 5.5 439 9.7 417 14.5 428 7.3 403 6.4 11 509 2.3 507 114.4 473 12.5 487 11.9 506 90.6 503 112.1 12 514 112.9 525 6.6 498 110.3 495 103.8 509 27.3 526 4.2 13 565 5.7 617 0.4 570 45.1 580 73.7 580 6.5 621 0.5 14 624 1.1 636 8.5 607 38.9 598 64.1 631 2.1 634 10.5 15 642 0.5 640 2.1 630 12.7 628 3.9 651 5.3 643 2.0 16 687 9.1 685 6.0 649 28.1 649 4.8 685 3.7 684 8.4 17 717 11.4 722 12.3 679 25.3 689 26.0 714 14.9 709 11.5 18 755 4.4 753 4.6 709 29.8 715 18.7 739 7.4 751 5.2 19 779 25.8 779 27.4 734 17.5 740 26.0 778 28.9 786 24.7 20 816 10.2 837 15.6 778 25.8 778 22.4 837 23.4 837 46.7 21 859 84.3 864 17.9 835 8.4 824 5.1 855 88.6 850 4.8 22 889 62.0 892 90.3 872 62.3 879 45.1 867 12.6 869 85.9 23 918 1.5 918 4.6 908 77.3 894 95.0 918 3.8 915 8.0 24 923 50.0 937 25.0 918 9.4 916 1.0 931 106.9 929 14.8 25 945 6.8 948 2.6 951 8.7 945 7.3 944 9.3 944 113.4 26 1000 92.9 979 148.1 975 88.3 975 46.2 1043 31.6 959 14.9 27 1045 23.9 1048 14.9 1048 24.9 1048 25.0 1053 148.7 1047 40.2 28 1058 11.0 1063 23.9 1084 13.0 1085 21.0 1075 0.4 1062 11.4 29 1094 9.8 1093 14.0 1093 136.4 1092 80.9 1093 12.5 1083 14.8 30 1132 7.8 1129 18.6 1115 108.2 1113 164.8 1119 50.7 1118 17.7 31 1175 17.7 1164 15.0 1133 14.6 1142 55.1 1171 3.6 1166 18.7 32 1193 8.7 1201 11.0 1198 4.0 1185 2.7 1189 10.4 1196 8.6 33 1207 4.6 1235 4.2 1218 2.9 1203 4.5 1225 8.7 1235 4.5 34 1234 12.3 1245 6.2 1249 2.3 1246 4.7 1234 9.6 1243 5.7 35 1260 2.5 1286 11.2 1272 1.3 1262 0.9 1250 1.1 1262 2.6 36 1308 3.7 1296 11.1 1291 2.4 1302 5.9 1296 6.2 1300 11.1 37 1324 3.1 1322 10.0 1324 3.8 1314 4.4 1330 11.5 1319 7.4 38 1358 11.9 1336 8.2 1344 3.9 1336 2.2 1362 8.8 1337 13.4 39 1409 427.4 1405 495.7 1352 3.1 1367 3.1 1393 503.8 1396 465 40 1411 32.3 1411 14.9 1409 22.4 1405 24.4 1412 16.6 1407 22.0 41 1427 8.4 1434 7.5 1430 7.2 1424 7.2 1435 4.2 1432 4.7 42 1468 24.0 1469 18.4 1469 23.3 1468 20.3 1468 18.9 1469 19.4 43 1541 14.2 1540 13.6 1536 12.2 1532 10.2 1535 19.3 1533 13.0 44 1652 41.7 1662 34.5 1667 37.9 1651 30.2 1664 36.3 1646 35.5 45 1772 261.5 1778 328.8 1752 265.3 1752 270.3 1778 291.0 1782 330.3 46 2917 15.6 2904 4.4 2881 34.4 2924 17.0 2883 23.0 2919 15.9 47 2927 43.8 2918 39.1 2934 23.2 2945 30.0 2913 20.9 2946 9.0 48 2988 7.6 2985 7.7 2987 13.2 2989 11.0 2977 7.8 2969 11.1 49 3119 3.9 3119 4.2 3117 4.6 3114 5.2 3118 4.6 3115 4.4 50 3145 0.2 3137 0.2 3136 0.5 3136 0.4 3136 0.4 3131 0.6 51 3225 228.7 3231 256.1 3340 27.0 3348 0.6 3300 209.2 3277 212.4 52 3321 70.3 3332 64.9 3416 12.6 3412 0.4 3337 4.1 3366 3.6 53 3437 17.8 3418 21.6 3514 47.7 3513 44.8 3404 24.3 3434 8.6 54 3514 52.8 3513 54.4 3571 24.6 3577 30.9 3514 51.8 3512 50.4
a Frequencies (mi; freq) in cm�1; intensities (int) in km/mol. All theoretical data were obtained at the B3LYP/6-311G* level of theory. The scale factor of0.96 was used for frequencies. Vibrational mode 39 corresponds to the CAO str & OAH bending, mode 45 corresponds to the C@O str. In the conformers1, 2, 5, and 6, vibrational mode 54 corresponds to the NAH (on the ring) str, modes 52 and 53 correspond to NH2 (str sym) and NH2 (str asym),respectively, and mode 51 corresponds to the OAH str. In the conformers 3 and 4, vibrational mode 54 corresponds to the OAH str, mode 53 correspondsto the NAH (on the ring) str, and modes 51 and 52 correspond to NH2 (str sym) and NH2 (str asym), respectively. Abbreviations: str, stretching; sym,symmetric; asym, asymmetric.


References

[1] C. Desfrancois, S. Carles, J.P. Schermann, Chem. Rev. 100 (2000)3943.

[2] P. Hundaky, A. Perczel, J. Phys. Chem A 108 (2004) 6195.[3] T.R. Rizzo, Y.D. Park, L.A. Peteanu, D.H. Levy, J. Chem. Phys. 84

(1986) 2534.[4] A. Lindinger, J.P. Toennies, A.F. Vilesov, J. Chem. Phys. 110 (1999)

1429.[5] F. Piuzzi, I. Dimicoli, M. Mons, B. Tardivel, Q. Zhao, Chem. Phys.

Lett. 320 (2000) 282.[6] L.C. Snoek, R.T. Kroemer, M.R. Hockridge, J.P. Simons, Phys.

Chem. Chem. Phys. 3 (2001) 819.[7] S.J. Martinez III, J.C. Alfano, D.H. Levy, J. Mol. Spectrosc. 156

(1992) 421.[8] L. Li, D.I. Lubman, Appl. Spectrosc. 42 (1988) 418.[9] L.I. Grace, R. Cohen, T.M. Dunn, D.M. Lubman, M.S. de Vries, J.

Mol. Spectrosc. 215 (2002) 204.[10] L.C. Snoek, E.G. Robertson, R.T. Kroemer, J.P. Simons, Chem.

Phys. Lett. 321 (2000) 49.[11] K.T. Lee, J. Sung, K.J. Lee, S. K Kim, Y.D. Park, J. Chem. Phys. 116

(2002) 8251.[12] Y. Lee, J. Jung, B. Kim, P. Butz, L.C. Snoek, R.T. Kroemer, J.P.

Simons, J. Phys. Chem. A 108 (2004) 69.[13] D.S. Caswell, T.G. Spiro, J. Am. Chem. Soc. 108 (1986) 6470.[14] R. Bhattacharyya, R.P. Saha, U. Samanta, P. Chakrabarti, J. Protein

Res. 2 (2003) 255.[15] M.L. Zhang, Z.J. Huang, Z.J. Lin, J. Chem. Phys. 122 (2005) 134313.[16] I. Compagnon, F.C. Hagemeister, R. Antoine, D. Rayane, M.

Broyer, P. Dugourd, R.R. Hudgins, M.F. Jarrold, J. Am. Chem. Soc.123 (2001) 8440.

[17] H.F. Hameka, J.H. Jensen, J. Mol. Struct. (Theochem) 288 (1993) 9.[18] S.J. Martinez III, J.C. Alfano, D.H. Levy, J. Mol. Spectrosc. 158

(1993) 82.[19] A.C. Samuels, J.O. Jensen, H.F. Hameka, J. Mol. Struct. (Theochem)

454 (1998) 25.[20] S.G. Stepanian, I.D. Reva, E.D. Radchenko, M. Rosado, M. Duarte,

R. Fausto, L. Adamowicz, J. Phys. Chem. A 102 (1998) 1041.[21] S.G. Stepanian, I.D. Reva, E.D. Radchenko, L. Adamowicz, J. Phys.

Chem. A 102 (1998) 4623.[22] S.G. Stepanian, I.D. Reva, E.D. Radchenko, L. Adamowicz, J. Phys.

Chem. A 103 (1999) 4404.[23] S. Gronert, R.A.J. O’Hair, J. Am. Chem. Soc. 117 (1995) 2071.[24] K.T. Lee, J. Sung, K.J. Lee, S.K. Kim, Y.D. Park, Chem. Phys. Lett.

368 (2003) 262.[25] K.T. Lee, J. Sung, K.J. Lee, Y.D. Park, S.K. Kim, Angew. Chem. Int.

Ed. 41 (2002) 4114.[26] K. Frimand, H. Bohr, K.J. Jalkanen, S. Suhai, Chem. Phys. 255

(2000) 165.[27] W.G. Han, K.J. Jalkanen, M. Elstner, S. Suhai, J. Phys. Chem. B 102

(1998) 2587.[28] C.D. Poon, E.T. Samulski, C.F. Weise, J.C. Weisshaar, J. Am. Chem.

Soc. 122 (2000) 5642.[29] C.F. Weise, J.C. Weisshaar, J. Phys. Chem. B 107 (2003) 3265.[30] E. Tajkhorshid, K.J. Jalkanen, S. Suhai, J. Phys. Chem. B 102 (1998)

5899.[31] K.J. Jalkanen, R.M. Nieminen, K. Frimadn, J. Bohr, H. Bohr, R.C.

Wade, E. Tajkhorshid, S. Suhai, Chem. Phys. 265 (2001) 125.[32] (a) A. Lesarri, E.J. Cocinero, J.C. Lopez, J.A. Alonso, Angew. Chem.

116 (2004) 615;(b) Angew. Chem. Int. Ed. 43 (2004) 605.

[33] Z.J. Huang, Z.J. Lin, J. Phys. Chem. A 109 (2005) 2656.[34] K.J. Jalkanen, V.W. Juergensen, A. Claussen, A. Rahim, G.M.

Jensen, R.C. Wade, F. Nardi, C. Jung, I.M. Degtyarenko, R.M.Nieminen, F. Herrmann, M. Knapp-Mohammady, T.A. Niehaus, K.Frimand, S. Suhai, Int. J. Quant. Chem. 106 (2006) 1160.

[35] D.A. Dougherty, Science 271 (1996) 163.[36] J.C. Ma, D.A. Dougherty, Chem. Rev. 97 (1997) 1303.[37] R.C. Dunbar, J. Phys. Chem. A 102 (1998) 8946.[38] A.D. Becke, Phys. Rev. B 38 (1988) 3098.[39] C. Lee, W. Yang, R.G. Parr, Phys. Rev. B 37 (1988) 785.[40] C. Møller, M.S. Plesset, Phys. Rev. 46 (1934) 618.[41] R. Krishnan, M.J. Frisch, J.A. Pople, J. Chem. Phys. 72 (1980) 4244.[42] P. Hobza, J. Sponer, Chem. Rev. 99 (1999) 3247.[43] I.L. Shamovsky, R.J. Riopelle, G.M. Ross, J. Phys. Chem. A 105

(2001) 1061.[44] R.F.M. Bader, Atoms in Molecules. A Quantum Theory, Clarendon

Press, Oxford, UK, 1990.[45] P.L.A. Popelier, Atoms in Molecules. An Introduction, Prentice Hall,

Harlow, UK, 2000.[46] L.F. Pacios, O. Galvez, P.C. Gomez, J. Phys. Chem. A 105 (2001)

5232.[47] J.A. Dobado, H. Martınez-Garcıa, J.M. Molina, M.R. Sundberg, J.

Am. Chem. Soc. 121 (1999) 3156.[48] J.A. Dobado, H. Martınez-Garcıa, J.M. Molina, M.R. Sundberg, J.

Am. Chem. Soc. 122 (2000) 1144.[49] M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb,

J.R. Cheeseman, V.G. Zakrzewski, J.A. Montgomery, R.E. Strat-mann, J.C. Burant, S. Dapprich, J.M. Millam, A.D. Daniels, K.N.Kudin, M.C. Strain, O. Farkas, J. Tomasi, V. Barone, M. Cossi, R.Cammi, B. Mennucci, C. Pomelli, C. Adamo, S. Clifford, J. Ochterski,G.A. Petersson, P.Y. Ayala, Q. Cui, K. Morokuma, D.K. Malick,A.D. Rabuck, K. Raghavachari, J.B. Foresman, J. Cioslowski, J.V.Ortiz, B.B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi,R. Gomperts, R.L. Martin, D.J. Fox, T. Keith, M.A. Al-Laham,C.Y. Peng, A. Nanayakkara, C. Gonzalez, M. Challacombe, P.M.W.Gill, B.G. Johnson, W. Chen, M.W. Wong, J.L. Andres, M. Head-Gordon, E.S. Replogle, J.A. Pople, Gaussian 98, Revision A.9,Gaussian, Inc., Pittsburgh PA., 1998.

[50] K.J. Jalkanen, S. Suhai, Chem. Phys. 208 (1996) 81.[51] A. Dreuw, M. Head-Gordon, J. Am. Chem. Soc. 126 (2004)

4007.[52] T. Yanai, D.P. Tew, N.C. Handy, Chem. Phys. Lett. 393 (2004) 51.[53] F. Biegler-Konig, J. Schonbohm, R. Derdau, D. Bayles, R. Bader,

AIM2000 Vision 1.0, 1998.[54] P.D. Godfrey, S. Firth, L.D. Hatherley, R.D. Brown, A.P. Pierlot, J.

Am. Chem. Soc. 115 (1993) 9687.[55] C.J. Chapo, J.B. Paul, R.A. Provencal, K. Roth, R.J. Saykally, J.

Am. Chem. Soc. 120 (1998) 12956.[56] J. Rak, P. Skurski, J. Simons, M. Gutowski, J. Am. Chem. Soc. 123

(2001) 11695.[57] C.J. Cramer, Essentials of Computational Chemistry: Theories and

Models, WIley, Chichester, 2002, p. 324.[58] A.P. Scott, L. Radom, J. Phys. Chem. 100 (1996) 16502.[59] Z.J. Huang, W.B. Yu, Z.J. Lin, J. Mol. Struct. (Theochem) 758 (2006)

195.[60] G. Maccaferri, W. Caminati, P.G. Favero, J. Phys. Chem. Faraday

Trans. 93 (1997) 4115.[61] R. Chelli, F.L. Gervasio, C. Gellini, P. Procacci, G. Cardini, V.

Schettino, J. Phys. Chem. A 104 (2000) 11220.[62] I. Alkorta, I. Rozas, J. Elguero, Chem. Soc. Rev. 27 (1998)

163.[63] U. Koch, P.L.A. Popelier, J. Phys. Chem. 99 (1995) 9747.[64] P.L.A. Popelier, J. Phys. Chem. A 102 (1998) 1873.[65] K.B. Wiberg, R.F.W. Bader, C.D.H. Lau, J. Am. Chem. Soc. 109

(1987) 1001.[66] E. Espinosa, E. Molins, C. Lecomte, Chem. Phys. Lett. 285 (1998)

170.[67] R. Miao, C. Jin, G. Yang, J. Hong, C. Zhao, L. Zhu, J. Phys. Chem.

A 109 (2005) 2340.[68] J.A. Dean, Lange’s Handbook of Chemistry, 15th ed., McGraw-Hill,

1999.

first-principle studies of gaseous aromatic amino acid histidine

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