Infrared Multiple Photon Dissociation Spectroscopy of Cationized

For these complexes, the bidentate [CO,N1] conformer in which the metal .... a reasonable structural description of comparable metal cation–ligand s...
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Infrared Multiple Photon Dissociation Spectroscopy of Cationized Histidine: Effects of Metal Cation Size on Gas-Phase Conformation Murat Citir,† Christopher S. Hinton,† Jos Oomens,‡,§ Jeffrey D. Steill,‡ and P. B. Armentrout*,† †

Department of Chemistry, University of Utah, Salt Lake City, Utah 84112, United States FOM Institute for Plasma Physics “Rijnhuizen”, Edisonbaan 14, 3439 MN Nieuwegein, The Netherlands § Van’t Hoff Institute for Molecular Sciences, University of Amsterdam, Amsterdam, The Netherlands ‡

S Supporting Information *

ABSTRACT: The gas phase structures of cationized histidine (His), including complexes with Li+, Na+, K+, Rb+, and Cs+, are examined by infrared multiple photon dissociation (IRMPD) action spectroscopy utilizing light generated by a free electron laser, in conjunction with quantum chemical calculations. To identify the structures present in the experimental studies, measured IRMPD spectra are compared to spectra calculated at B3LYP/6-311+ G(d,p) (Li+, Na+, and K+ complexes) and B3LYP/HW*/6311+G(d,p) (Rb+ and Cs+ complexes) levels of theory, where HW* indicates that the Hay−Wadt effective core potential with additional polarization functions was used on the metals. Single point energy calculations were carried out at the B3LYP, B3P86, and MP2(full) levels using the 6-311+G(2d,2p) basis set. On the basis of these experiments and calculations, the only conformation that reproduces the IRMPD action spectra for the complexes of the smaller alkali metal cations, Li+(His) and Na+(His), is a charge-solvated, tridentate structure where the metal cation binds to the backbone carbonyl oxygen, backbone amino nitrogen, and nitrogen atom of the imidazole side chain, [CO,Nα,N1], in agreement with the predicted ground states of these complexes. Spectra of the larger alkali metal cation complexes, K+(His), Rb+(His), and Cs+(His), have very similar spectral features that are considerably more complex than the IRMPD spectra of Li+(His) and Na+(His). For these complexes, the bidentate [CO,N1] conformer in which the metal cation binds to the backbone carbonyl oxygen and nitrogen atom of the imidazole side chain is a dominant contributor, although features associated with the tridentate [CO,Nα,N1] conformer remain, and those for the [COOH] conformer are also clearly present. Theoretical results for Rb+(His) and Cs+(His) indicate that both [CO,N1] and [COOH] conformers are low-energy structures, with different levels of theory predicting different ground conformers.

1. INTRODUCTION Histidine is an essential amino acid and chemically one of the most flexible protein residues because of the imidazole side chain, which functions as both an acid and base near neutral pH.1 As a consequence, histidine is often found at the catalytic sites of protein enzymes. It serves as a precursor of the hormone histamine, regulates the proper utilization of trace metals, and is essential in their rapid excretion if present in excessive amounts.2,3 The importance of histidine interactions with metal ions in biological systems has been recognized for some time.3 The histidine molecule presents three potential coordination sites in aqueous solution. The carboxyl group (pKa = 1.9), the imidazole nitrogen (pKa = 6.1), and the amino nitrogen (pKa = 9.1) become available for complexation as pH increases. The imidazole nitrogen of histidine residues is a primary site for binding metal ions to proteins, although various crystal studies have shown that histidine can use each of the three potential coordination sites for metal ion binding.4−9 Such X-ray results provide useful information on the types of complexes that may be present in solution but clearly are incapable of providing definitive solution structures. © 2012 American Chemical Society

Infrared multiple photon dissociation (IRMPD) spectroscopy has been used to probe the structures of ionized complexes in the gas phase, making it a powerful tool for understanding ion−protein interactions. An important advantage of this technique is the ability to investigate the structures of biomolecules in isolation, where complicating structural effects of solvent and counterions are absent. The interactions of metal cations with amino acids, the building blocks of proteins, have been extensively investigated using IRMPD spectroscopy, with results reported for metalated Gly,10 Pro,10−12 Gln,11,13 Trp,14,15 Phe,16 Lys,17,18 Arg,11,19,20 Ser,11,21 Val,11 Thr,22 Asp,23 Glu,23 Asn,24 Met,25 and Cys.26 Although the study of isolated molecules neglects their biological environment, such work allows a more detailed knowledge of the structures and properties of such molecules, which is useful in understanding their static and dynamic properties in larger biosystems.27 Received: October 6, 2011 Revised: January 13, 2012 Published: January 13, 2012 1532

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of the dc bias of the ion transfer octopole allows ions to be captured in the ICR cell without the use of a gas pulse.16 Electrostatic switching of the dc bias of the octopole, where a dc bias voltage is superimposed on the full length of all octopole rods, results in there being no change in the dc electric field along the axis of the ion guide, which decelerates the ions exiting the octopole. In contrast to the conventional gas pulsing method to stop the ions, this technique does not cause collisional heating of the ions. The precursor ions were mass selected using stored waveform inverse Fourier transform (SWIFT) techniques and irradiated by the FEL at pulse energies of 50 mJ per macropulse of 5 μs duration, although they fell off to about 20 mJ toward the blue edge of the scan range. Complexes were irradiated for 2−4 s, corresponding to interaction with 10−20 macropulses. The fwhm bandwidth of the laser was typically 0.5% of the central wavelength. For the present experiments, spectra were recorded over the wavelength range 19.4 μm (520 cm−1) to 5.5 μm (1820 cm−1), which can be covered with a single setting of the electron beam energy of FELIX. 2.2. Computational Details. Our protocol for finding all low-lying conformations of metal cation−amino acid complexes has been described elsewhere.37 To find the global energy minimum and all low-energy geometries, a large number of possible conformations were screened as follows. A simulated annealing methodology using the AMBER program and the AMBER force field based on molecular mechanics38 were used to search for possible starting structures in each system’s conformational space for higher level optimizations. This procedure was used for Li+(His) and K+(His) complexes. All possible structures identified this way were subsequently optimized using NWChem39 at the HF/3-21G level.40,41 Unique structures for each system (∼230 for each complex) were optimized using Gaussian0942 at the B3LYP/6-31G(d) level of theory43,44 with the loose keyword (maximum step size 0.01 au and an rms force of 0.0017 au) to facilitate convergence. Unique structures obtained from this procedure (∼50) were then chosen for higher level geometry optimization and frequency calculations using density functional theory (DFT) at the B3LYP/6311+G(d,p) level of theory.45,46 Single point energy calculations were carried out at the B3LYP, B3P86, and MP2(full) levels using the 6-311+G(2d,2p) basis set.45 Zero point vibrational energy (ZPE) corrections were determined using vibrational frequencies calculated at the B3LYP/6-311+G(d,p) level scaled by a factor of 0.989.47,48 For the Na+(His), Rb+(His), and Cs+(His) complexes, all conformations located for K+(His) were used as starting points for geometry and vibrational frequency calculations optimized at the B3LYP/ HW*/6-311+G(d,p) level where HW* indicates that Rb+ and Cs+ were described using the effective core potentials (ECPs) and valence basis sets of Hay and Wadt49 with a single d polarization function (exponents of 0.24 and 0.19, respectively) included.50 This level of theory has been shown to provide a reasonable structural description of comparable metal cation− ligand systems.21,22,24−26 Relative energies of various conformers are determined using single point energies at the B3LYP, B3P86, and MP2(full) levels using the HW*/6-311+G(2d,2p) basis set, Table S1, Supporting Information. Relative energies at 0 K are converted to 298 K free energies using the rigid rotor/ harmonic oscillator approximation with rotational constants and vibrational frequencies calculated at the B3LYP/6-311+G(d,p) level, Tables 1 and S2, Supporting Information. In general,

Interactions of metal ions with His have direct biological significance but generally involve multiply charged metal cations of Fe, Co, Ni, Cu, Cd, Mn, or Zn.3,28,29 Recently, Dunbar et al.30 used IRMPD spectroscopy to study complexes of Ba2+, Ca2+, and Na+ with histidine. These results reveal a crossover from dominance of the zwitterion (salt bridge, SB) conformation with Ba2+ to substantial presence of the canonical (charge-solvated, CS) conformation with Ca2+. Theory30 predicts that metal ion complexes of histidine favor the CS conformation for singly charged metal ions and smaller doubly charged alkaline earth ions with the SB conformation becoming increasingly favorable for larger alkaline earth metal ions. Williams and co-workers investigated the interactions of halide anions (X− = Cl−, Br−, and I−) with His and their effects on the zwitterion stability using IRMPD spectroscopy and theory.31 They found that anion size has little effect on the structures and relative zwitterion stabilities, which can be attributed to the large size of the halide anions investigated compared to that of metal cations where size effects are more pronounced. The IRMPD spectra of X− (His) have many sharp bands corresponding to the side chain that are not reproduced well in calculated spectra of low-energy conformers of X−(His), making assignments ambiguous. This group has also examined H+(HisArg) and H22+(HisArg) with IRMPD spectroscopy and theory,32 identifying a signature peak due to a neutral histidine side chain at 1080 cm−1. Our group recently investigated gas phase structures of singly and doubly charged complexes involving the transition metal cations, Zn and Cd, bound to the amino acid histidine and deprotonated His (His−H) using IRMPD spectroscopy and theory.33 The monomeric species, CdCl+(His) and [M(His−H)]+ where M = Zn and Cd, were unambiguously assigned as tridentate complexes of histidine coordinated to the metal center. In contrast, spectra of the dimeric Cd2+(His)2 and Zn2+(His)2 complexes had characteristics indicating that at least one of the His ligands is chargesolvated; however, there were also signatures for a SB structure for the second His ligand. Both experimental spectra had a large number of bands making it difficult to definitively assign a single configuration for these species. In the present study, we examine effects of metal cation size on gas phase conformations by measuring the IRMPD action spectra for dissociation of His cationized by Li+, Na+, K+, Rb+, and Cs+. The conformations are identified by comparing the experimental spectra to IR spectra of the low-lying structures of the cationized His complexes predicted by quantum chemical calculations at the B3LYP/6-311+G(d,p) level of theory.

2. EXPERIMENTAL AND COMPUTATIONAL SECTION 2.1. Mass Spectrometry and Photodissociation. Experiments were performed at the FOM-Institute for Plasma Physics “Rijnhuizen” in Nieuwegein (The Netherlands) by using the Free Electron Laser for Infrared eXperiments (FELIX) facility.34 The home-built Fourier transform ion cyclotron resonance (FTICR) mass spectrometer has been described in detail elsewhere.16,35,36 The metal cation−histidine complexes were generated using a Z-spray (Micromass UK Ltd.) electrospray ionization source. Solutions of 1.0−3.0 mM His with 0.5−1.0 mM alkali-metal chloride in 50% MeOH and 50% H2O were used. Solution flow rates were about 10 μL/min, and the electrospray needle was held at a voltage of ∼3.2 kV. Ions were accumulated in a hexapole trap for about 4 s followed by pulsed extraction through a quadrupole bender prior to being injected into the ICR cell via a radio frequency (rf) octopole ion guide. Electrostatic pulsing 1533

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Table 1. B3LYP, B3P86, and MP2(full) 298 K Relative Free Energies (kJ/mol) of Low-Lying Conformers of M+(His)a structure

dihedralb

Li+(His)

Na+(His)

K+(His)

Rb+(His)

Cs+(His)

[CO,Nα,N1] [CO,N1]

tgcg ctg−g+ ctg+g− cgg+g− cN1ggc(t) tgcg tggg tgtg cggg ctg−g+ ctg+g− cNαgg−g+ cggg tgtg tttc tggg cNαgcg

0.0, 0.0, 0.0 23.0, 21.1, 30.9 19.4, 18.6, 32.2 [CO2−]-cgg+g− 44.3, 41.7, 57.2 27.8, 29.5, 24.9 [CO,Nα,N1]-tgcg 30.1, 31.2, 35.8 35.0, 29.5, 45.6 49.9, 46.5, 55.4 45.4, 43.0, 57.7 58.5, 53.3, 53.9 [CO,N1]-ctg+g− 77.3, 81.9, 83.2 90.8, 90.3, 92.1 101.3, 97.9, 100.8 138.0, 131.3, 123.8

0.0, 0.0, 0.0 12.1, 8.4, 15.8 15.1, 12.8, 25.0 [CO2−]-cgg+g− 21.7, 17.4, 32.9 26.9, 28.2, 24.2 [CO,Nα,N1]-tgcg 25.0, 25.2, 29.8 24.5, 18.2, 31.9 [CO2−,N1]-cNαgg−g+ [CO,N1]-ctg+g− 40.8, 34.6, 36.0 [CO,N1]-ctg+g− 61.7, 64.0, 64.2 68.4, 66.5, 68.2 65.1, 61.1, 62.7 99.8, 93.0, 87.4

1.6, 4.6, 0.0 0.0, 0.0, 2.2 7.3, 8.8, 16.6 4.4, 2.0, 11.6 5.4, 3.9, 18.4 26.2, 30.3, 21.9 21.4, 24.0, 18.8 20.6, 23.7, 24.5 9.2, 7.3, 17.1 [CO2−,N1]-cNαgg−g+ [CO,N1]-ctg+g− 26.0, 23.1, 22.0 15.5, 16.3, 11.9 46.5, 52.1, 47.2 49.4, 51.7, 50.4 38.7, 39.9, 38.6 74.0, 71.6, 64.6

9.1, 13.3, 4.4 0.0, 1.3, 0.0 9.8, 12.5, 16.9 0.4, 0.0, 6.7 [COOH]-cggc(t) 32.1, 37.3, 24.5 22.3, 26.3, 16.7 [CO,Nα,N1]-tgtg 8.7, 8.7, 15.3 [CO2−,N1]-cNαgg−g+ [CO,N1]-ctg+g− 28.4, 26.5, 23.4 14.0, 16.3, 8.6 41.7, 48.3, 40.5 45.3, 49.2, 45.9 31.3, 34.2, 32.3 68.5, 67.1, 58.4

16.5, 19.9, 14.2 0.0, 0.4, 0.0 12.2, 14.3, 22.0 0.4, 0.0, 10.2 [COOH]-cggc(t) 38.6, 42.9, 33.9 25.5, 28.8, 21.8 [CO,Nα,N1]-tgtg 10.5, 10.5, 18.6 [CO2−,N1]-cNαgg−g+ [CO,N1]-ctg+g− 30.9, 28.3, 30.7 15.3, 17.1, 13.4 42.0, 47.9, 43.1 45.6, 48.9, 49.6 29.8, 32.4, 33.8

[COOH] [CO2−] [OH,Nα,N1] [Nα,N1] [CO,Nα] [CO−,N1] [CO2−,N1] [COOH,N1] [OH,N1] [OH,Nα] [N3] [CO2−,N3] a

B3LYP, B3P86, and MP2(full) values calculated using the 6-311+G(2d,2p) basis set with structures and zero point energies calculated at the B3LYP/6-311+G(d,p) level of theory. Values for Rb and Cs use the HW* basis set on the metal. Bold indicates the ground state. Entries having alternate structures indicate the calculation collapsed to the indicated structure. bDihedral angles for ∠HOCC, ∠OCCC, ∠CCCC, and ∠CCCN1, and in some cases, another dihedral angle is added to define the lone pair orientation of the NαH2 group (see text for detail).

the relative ΔG298 excitation energies are comparable to the analogous differences in the ΔH0 values. Vibrational frequencies and intensities were calculated using the harmonic oscillator approximation and analytical derivatives of the energy minimized Hessian calculated at the B3LYP/ HW*/6-311+G(d,p) level of theory. Each of the resulting structures was found to have all real harmonic vibrational frequencies at this level of theory indicating that they are local minima on the potential energy surface. For comparison to IRMPD spectra, frequencies were scaled by 0.975 as this scaling factor leads to good agreement between calculated and experimentally well-resolved peaks and is in accord with previous IRMPD studies of amino acid complexes in this spectral region as well.11,13,14,24−26 Calculated vibrational frequencies are broadened using a 20 cm−1 fwhm Gaussian line shape for comparison with experimental spectra.

3. RESULTS AND DISCUSSION 3.1. IRMPD Action Spectroscopy. Photodissociation spectra of His complexed with Li+, Na+, K+, Rb+, and Cs+ were examined. For metalated His complexes with K+, Rb+, and Cs+, photodissociation results in the loss of the intact ligand to form the atomic metal cation. This result is consistent with the observation of intact ligand loss as the sole pathway observed in the collision-induced dissociation (CID) spectra of K+(His), Rb+(His), and Cs+(His).51 For the K+, Rb+, and Cs+ complexes of His, Figure 1 shows IRMPD action spectra taken from the relative intensity of the M+ product cation as a function of laser wavelength. Unfortunately for these three systems, laser power was inadequate to acquire data below 650 cm−1. In contrast, Li+(His) and Na+(His) display alternative decomposition pathways, consequently reducing the signal-tonoise for the former two spectra. For Li+(His), four IR photodissociation pathways were observed corresponding to the loss of H2O, CO2, NH3 + CO (or HCN + H2O), and NH3 + CO2, each with identical spectra. Observation of a Li+ product is beyond the accessible mass range of the FTICR. The sum of these four decomposition pathways is shown as the IRMPD

Figure 1. Infrared multiple photon dissociation action spectra of M+(His) complexes where M+ = Li+, Na+, K+, Rb+, and Cs+.

action spectrum in Figure 1. However, only loss of NH3 + CO (or HCN + H2O) was observed upon IR photodissociation for Na+(His), even though the CID spectrum exhibits only a loss of the intact ligand.51 Comparison of the IRMPD spectra in Figure 1 shows that the features observed in the relatively simple Li+(His) spectrum are generally retained for all of the metal cation complexes but that new spectral features begin to appear for K+(His) and become very obvious for Rb+(His) and Cs+(His). The major band at 1732 cm−1 for Li+(His) shifts to the blue, and the bands at 1157 and 589 cm−1 shift to the red as the metal cation becomes heavier. Spectral features at 1596, 1434, and 1079 cm−1 remain largely unchanged as the size of the metal 1534

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Figure 2. Structures of the K+(His) complexes calculated at the B3LYP/6-311+G(d,p) level of theory. Also shown is the [CO−,N1]-ctg−g+ structure(circled), which is stable only for Li+(His). Dashed lines indicate interactions of hydrogens with adjacent atoms that help constrain the geometry shown.

Relative energies at 0 K including ZPE corrections with respect to the ground state calculated at three different levels of theory (B3LYP, B3P86, and MP2(full)) for M+(His) complexes, where M+ = Li+, Na+, K+, Rb+, and Cs+ can be found in the Supporting Information, Table S1. The relative Gibbs free energies at 298 K may be more relevant in describing the experimental distributions investigated here, and these are provided in Tables 1 and S2, Supporting Information. The overall trends in relative Gibbs free energies at 298 K calculated at the MP2(full) level for the lowest energy conformer of each type are shown in Figure 3. These results are qualitatively similar to those calculated at the B3LYP and B3P86 levels for which figures can be

ion increases, although the photodissociation signal at these frequencies increases for K+(His), Rb+(His), and Cs+(His). A new band emerges at 1647 cm−1 for K+(His) and blue shifts to 1666 cm−1 in Cs+(His). Other new bands arise at ∼1390, ∼1320, 823, and 758 cm−1 for K+(His) with increasing signal intensity as the size of the metal ion increases. These progressions suggest multiple conformers are present in the IRMPD spectra for the K+, Rb+, and Cs+ complexes. 3.2. Theoretical Results (Structures). Low-lying and representative higher energy conformations of K+(His) are shown in Figures 2 and S1 (Supporting Information), respectively. The nomenclature used to identify these different structural isomers is based on that established previously for M+(Gly).37,52−54 Briefly, conformations of cationized His are identified by their metal binding sites in brackets, followed by a description of the histidine orientation, named by a series of dihedral angles starting from the carboxylic acid hydrogen of the backbone and going to the imidazole side chain nitrogen (N1) (∠HOCC, ∠OCCC, ∠CCCC, and ∠CCCN1, respectively). Dihedral angles are distinguished as cis (c, for angles between 0−45°), gauche (g, 45−135°), or trans (t, 135−180°), and + or − indicating their sign when necessary to distinguish similar structures. In some cases, these four dihedral angles are insufficient to distinguish similar conformers and a fifth dihedral angle is added in parentheses to define the lone pair orientation of the NαH2 group. In most conformations, this orientation is cis with respect to the adjacent backbone CC bond, such that only alternate orientations (gauche or trans) are indicated by this fifth dihedral angle. For salt-bridge conformations, the proton originally on the carboxylic acid is attached to either the alpha-amino (Nα) or the imidazole nitrogen (N1) groups. For these conformers, the first dihedral angle remains ∠HOCC (where the H is only hydrogen bonded to O) but is labeled using a subscript identifying where the proton is located (either Nα or N1). The remaining three dihedrals are the same as above.

Figure 3. Gibbs free energies (kJ/mol) at 298 K calculated at the MP2(full)/6-311+G(2d,2p)//B3LYP/6-311+G(d,p) (and MP2(full)/ HW*/6-311+G(2d,2p)//B3LYP/HW*/6-311+G(d,p) for Rb+ and Cs+ complexes) level of theory for thirteen distinct conformation types of M+(His) (lowest energy stable structure of each type), where M+ = Li+, Na+, K+, Rb+, and Cs+, as a function of the alkali-metal cation relative to the energy of the [CO,Nα,N1] conformer. 1535

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the [CO,Nα,N1]-tgcg conformer correspond reasonably well with the observed spectrum in terms of both band positions and relative intensities (especially because the spectrum has not been power corrected, which would increase the intensity of the band at 1732 cm−1). The calculated IR spectra and frequencies for higher energy structures are included in the Supporting Information (Figure S3 and Table S3−S15), but no other distinct conformers, including alternative side chain orientations of the [CO,Nα,N1] conformer, are predicted to be low enough in energy to contribute to the experimental spectrum. The band observed at 1732 cm−1 is attributed to the carbonyl stretch of the carboxylic acid group on the basis of the present calculations as well as previous results for Na+(His),30 H+(HisArg), H22+(HisArg),32 and X−(His) (X− = Cl−, Br−, and I −).31 (It can be noted that the assignment of observed bands to particular normal mode vibrations in the histidine molecule is largely a qualitative assessment on the basis of visualizing the calculated motions. Perturbations from the metal cation exist in most of these modes, but the normal modes in the metal ion complex remain very comparable to those in bare His.) Interaction with the lithium cation results in a red shift of this band with respect to free His, calculated at 1769 cm−1 for the GS conformation, (His)-ctg−g+ (Figure S4, Supporting Information). The carbonyl stretch predicted by the [CO,Nα,N1]-tgcg conformer at 1719 cm−1 agrees reasonably well with the observed band. Similar carbonyl stretches are found in five ([CO,Nα,N1], [CO,N1], [Nα,N1], [N3], and [COOH]) of the twelve distinct conformers of Li+(His) (Figures 4 and S3, Supporting Information). If the metal cation binds to the hydroxyl group of the backbone rather than to the carbonyl, as in [OH,Nα,N1], [OH,N1], and [OH,Nα], the carboxylic acid CO stretch is blue-shifted to 1827, 1841, and 1846 cm−1, respectively. For the zwitterionic structures, [CO2−], [CO2−,N1], and [CO2−,N3], the carboxylate functionality is predicted to have a CO stretch that is significantly redshifted to 1553, 1664, and 1665 cm−1, respectively (Figure S3, Supporting Information). The last distinct conformer, [CO,Nα], has a predicted CO stretch of 1675 cm−1, considerably red-shifted with respect to the observed band at 1732 cm−1. Similar trends are found for all other metal complexes as well. The weak band observed at 1596 cm−1 has the largest deviation with the calculated spectra for the [CO,Nα,N1] conformer, which has a band predicted at 1623 cm−1. This band is associated with the bending motion of the NH2 group, and its predicted position is largely unaffected compared to the 1618 and 1628 cm−1 bands for neutral His in the (His)-ctg−g+ and (His)-tgtg type conformations (Figure S4, Supporting Information), respectively. Such deviations between experiment and theory have been observed for NH2 bending modes in other systems21,22,55,56 and are believed to result from strong anharmonic effects. The bands observed at 1157, 1079, and 1007 cm−1 are probably the most diagnostic bands for the [CO,Nα,N1]-tgcg structure. The positions of these bands are nicely reproduced by the predicted IR spectrum for this conformer, whereas no other conformation is predicted to have dominant bands at these same characteristic frequencies, except [Nα,N1]-tgtg. The bands at 1157 and 1007 cm−1 are primarily associated with a hydroxyl in-plane bend and NH2 wagging motion, with the predicted bands slightly blue-shifted by 12 and 6 cm−1, respectively. The observed band at 1157 cm−1 with a shoulder at 1218 cm−1 corresponds particularly well with the calculated ground state conformer, as this has the most intensity at 1169 cm−1 with a shoulder at ∼1220 cm−1. The sharp band at

found in the Supporting Information, Figure S2. The MP2 results are highlighted here as previous work on other metalated amino acids suggests it does a slightly better job at predicting the relative energies of different conformations.21 At all levels of theory, the ground state structure for Li+(His) and Na+(His) is the [CO,Nα,N1]-tgcg conformer, a tridentate charge-solvated structure in which the metal ion binds to the backbone carbonyl oxygen, backbone amino nitrogen, and imidazole side chain nitrogen. According to the DFT results, the ground state structure for K+(His) has a bidentate [CO,N1] geometry in which the metal cation binds to the backbone carbonyl oxygen and imidazole side chain nitrogen, and there is an OH···Nα hydrogen bond, Figure 2. MP2(full) calculations indicate that the [CO,Nα,N1]-tgcg conformer remains the ground state structure for K+(His). For Rb+(His) and Cs+(His), the B3P86 level of theory predicts that the [COOH] structure is the lowest energy complex, whereas the B3LYP and MP2(full) levels of theory calculate the [CO,N1] conformer as the lowest energy structure. For Rb+(His) and Cs+(His), all three levels of theory predict that the [CO,Nα,N1]-tgcg conformer lies 4−13 and 14−20 kJ/mol, respectively, above the lowest energy conformation. 3.3. Comparison of Experimental and Theoretical IR Spectra: Li+(His). Figure 4 compares the experimental IRMPD

Figure 4. Comparison of the experimental IRMPD action spectrum for Li+(His) with IR spectra for three low-lying conformations predicted at the B3LYP/6-311+G(d,p) level of theory.

action spectrum with calculated IR spectra for three distinct conformers of Li+(His): the [CO,Nα,N1] GS at all levels of theory and the lowest energy excited conformers predicted at the DFT, [CO,N1], and MP2, [OH,Nα,N1], levels of theory. The calculated IR intensities may not be in direct accord with the IRMPD action spectrum because the latter is a multiple photon process, whereas the theoretical IR spectra are based on single photon absorption. Nevertheless, the bands predicted by 1536

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Figure 5. Comparison of the experimental IRMPD action spectrum for K+(His) with IR spectra for seven low-lying conformations predicted at the B3LYP/6-311+G(d,p) level of theory. Shading indicates the major experimental bands observed.

1079 cm−1 is reasonably reproduced by the predicted IR spectra and is attributed to CN stretches and in-plane CH and NH bends of the side chain. This assignment is supported by the present calculations, previous results for H+(HisArg) and H22+(HisArg) IRMPD spectra,32 as well as the IR spectrum of condensed-phase imidazole.57 The intense peak observed at 588 cm−1 is a combination of vibrations corresponding to out-of-plane bending motions of the carboxylic acid hydrogen atom and out-of-plane C−H and N−H bends of the imidazole side chain. Some minor bands predicted are not observed experimentally, notably between 650−950 cm−1 and 1250−1600 cm−1, although hints of these bands are seen at 774 and 829 cm−1. The weak band at 1434 cm−1 is a conglomerate of vibrations corresponding to HCH bends in the amino acid side chain. Overall, the experimental IRMPD action spectrum for Li+(His) can be explained completely by the calculated spectrum of the ground state [CO,Nα,N1]-tgcg conformer. 3.4. Comparison of Experimental and Theoretical IR Spectra: Na+(His). Figure 1 shows that the IRMPD action spectra for Na+(His) and Li+(His) are very similar, exhibiting all of the same major spectral features. Comparison of experimental and theoretical spectra for Na+(His) can be found in Figure S5 of the Supporting Information. The predicted spectrum for the [CO,Nα,N1]-tgcg conformer shows a close correspondence to the observed spectrum for Na+(His), with agreement comparable to that obtained for Li+(His). The intense band observed at 1747 cm−1 agrees well with the predicted carbonyl stretch for the lowest energy [CO,Nα,N1]-tgcg conformer at 1731 cm−1. The calculated spectra predict a blue shift in this band of 12 cm−1 from Li+(His) to Na+(His), in agreement with the experimental observation. Likewise, the bands at 1157 and 588 cm−1 in the

Li+(His) spectrum are red-shifted for Na+(His) to 1144 and 583 cm−1 (shifts of 13 and 5 cm−1), respectively, in reasonable agreement with predicted red shifts of 15 and 14 cm−1 for [CO,Nα,N1]-tgcg. The bands at 1434 and 1079 cm−1 do not shift with metal cation identity, in agreement with the predictions for the [CO,Nα,N1] conformers. The band at 1007 cm−1 in the Li+(His) spectrum is not observed in the Na+(His) spectrum. Predicted weak bands in the region of 650−1050 cm −1 are not evident in the Na+(His) spectrum, except for that at ∼830 cm−1. Weak bands observed in the Na+(His) spectrum at 1350−1700 cm−1 can all be found in the predicted spectrum for [CO,Nα,N1]-tgcg. Despite the limited signal-to-noise, the predicted spectra for the GS [CO,Nα,N1] conformers of Li+(His) and Na+(His) accurately represent the changes observed with metal cation identity. Previously, Dunbar et al. reported an IRMPD spectrum of Na+(His) over the wavelength range 950 cm−1 to 1850 cm−1.30 These authors also reported good agreement between the experimental and predicted spectra of Na+(His) for the chargesolvated conformer.30 There are some differences between the two experimental Na+(His) spectra, including a 20 cm−1 red shift in all major bands. This shift is believed to be the result of inadequate frequency calibration in the previous work, as the present wavelength scale was carefully calibrated. In addition, the new spectrum now includes the wavelength range from 550 to 950 cm−1 and has somewhat better resolution between 1380 to 1700 cm−1. 3.5. Comparison of Experimental and Theoretical IR Spectra: K+(His), Rb+(His), and Cs+(His). Figures 5 and S6 (Supporting Information) show the experimental IRMPD action spectrum of K+(His) compared with theoretical predictions for the thirteen lowest energy distinct conformations (those having different metal cation binding modes). Comparison of the 1537

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agrees with a weak band at ∼1585 cm−1 in the K+(His) spectrum and more obvious peaks in the Rb+(His) and Cs+(His) spectra at ∼1580 and ∼1585 cm−1, respectively. In all three systems, the observed intensities of these bands are comparable to those at ∼1493 [1496,1495] cm−1, as predicted. The most intense band in the predicted spectra of [COOH] lies at 1695 [1707,1711] cm−1, which does not agree with the new peak at 1647 [1650,∼1670] cm−1 in the observed spectra for K+(His) [Rb+(His),Cs+(His)]. However, this peak is not reproduced by any of the calculated spectra. Its frequency suggests the presence of the [COOH] or zwitterionic [CO2−] conformers, as both of these conformers have red-shifted carbonyl stretches. Specifically, calculated spectra for [COOH]cgg+g− and [CO2−] conformers (cN1ggc(t), cN1gg−g+(g), and cN1cgc conformers for K+(His), Rb+(His), Cs+(His), respectively) predict bands at 1695 [1707,1711] and 1591 [1594,1624] cm−1 for K+(His) [Rb+(His),Cs+(His)], which fall on either side of the experimental bands at 1647 [1650,∼1670] cm−1. (Interestingly, calculation of the frequencies of the transition state connecting these two conformers in the case of K+(His) finds that the CO stretch shifts to 1647 cm−1, comparable to that observed experimentally, Figure S9, Supporting Information.) These observations may suggest that theory has difficulty properly predicting the red shift in the carbonyl stretch for these types of structures, which are closely related, differing primarily in the slight change in position of the proton shared by the carboxylic and imidazole groups. Figure 6

experimental and theoretical spectra for Rb+(His) and Cs+(His) can be found in the Supporting Information, Figures S7 and S8, respectively. Overall, results for Rb+(His) and Cs+(His) are very similar to those shown for K+(His), and therefore, these are discussed together. Compared to the experimental spectra for Li+(His) and Na+(His), the IRMPD spectra of K+(His), Rb+(His), and Cs+(His) retain all the same bands, but new features are present, Figure 1. New bands in the observed spectrum of K+(His) [Rb+(His),Cs+(His)] occur at 758 [762,762], 823 [826,828], 1326 [1318,1319], ∼1390 [1382,∼1390], and 1647 [1650,∼1670] cm−1. The appearance of these new bands could be evidence for new conformers or could be the result of better sensitivity associated with more facile dissociation of these more weakly bound systems. However, we find that the bands at 1079 [1083,1079], ∼1390 [1382,∼1390], and 1647 [1650,∼1670] cm−1 grow in intensity compared to that for Na+(His), whereas those at 1140 [∼1135,1125] and 1750 [1753,1753] cm−1 decrease in relative intensity. These changes suggest multiple conformers are present, as discussed further below. The [CO,Nα,N1] conformer may still be present as the predicted carbonyl stretch of 1736 [1743,1745] cm−1 agrees well with the corresponding band observed at 1750 [1753,1753] cm−1. The frequency for the bending mode of the NH2 group in the [CO,Nα,N1] spectra (1620 [1620,1619] cm−1) is blueshifted by ∼30 cm−1 with respect to the observed band at ∼1591 [∼1587,∼1570] cm−1, consistent with the observed shifts for Li+(His) and Na+(His). The calculated band at 1150 [1146,1143] cm−1 corresponding to the COH bending mode of the [CO,Nα,N1] conformer matches the observed bands at 1140 [∼1135,1125] cm−1 for K+(His) [Rb+(His),Cs+(His)]. This band is particularly diagnostic for the presence of the [CO,Nα,N1] conformer as only this conformer and the higher energy [Nα,N1]-tggg and [N3]-tggg conformers show an intense band at this frequency. The other potentially diagnostic band corresponds to the NH2 wagging mode, predicted to be at 992 [987,978] cm−1 for the [CO,Nα,N1] conformer, but this band is weak in the observed spectra. The [CO,N1]-ctg−g+ conformer must also be considered as it is predicted to be the ground state by some levels of theory for K+(His)−Cs+(His), Table 1. The intense band observed at 1750 [1753,1753] cm−1 agrees well with the predicted carbonyl stretch for the [CO,N1]-ctg−g+ conformer at 1739 [1748,1755] cm−1 but overlaps directly with the carbonyl stretch in the [CO,Nα,N1] spectrum. The new band observed at ∼1395 [∼1380,∼1390] cm−1 is attributed to the hydroxyl in-plane bend (COH) (1398 [1395,1394] cm−1) of the [CO,N1] conformer. A new band at 823 [826,828] cm−1 also matches the next most intense band predicted for this conformer, Figure 5, although not the adjacent band observed near 760 cm−1. The new bands observed at ∼1493 [1496,1495] and 1209 [∼1215,∼1200] cm−1 are matched by predicted bands for the [COOH] conformer at 1481 [1485,1485] and 1221 [1224,1225] cm−1. The only other conformer having a band in the former region is the [CO,Nα] conformer, with an intense band at 1484 [1480,1482] cm−1, but this species is ∼5 [8,10] kJ/mol higher in energy. Bands observed at 823 [826,828] and 758 [762,762] cm−1 can also be described by bands calculated at 814 [817,816] and 747 [747,747] cm−1 in the calculated [COOH] spectra. The relative intensities of these bands seem more consistent with the [COOH] predicted spectrum than that for [CO,N1]. Another intense band in the predicted [COOH] spectrum lies at 1579 [1575, 1573] cm−1, which

Figure 6. Potential energy surface along the N1−H−OC coordinate linking the [CO2−]-cgg+g− (left side) and [COOH]-cgg+g− (right side) conformers calculated at the B3LYP/6-311+G(d,p) level, with the HW* basis set for Rb and Cs and the SDD basis set and relativistic ECP for Ba. Color coded dashed lines represent the zero point energies for the harmonic oscillators associated with the proton motion along the N1−H−OC coordinate for each well. Red shading shows the range of zero point energies for the harmonic oscillators associated with the proton motion for the K+(His) double-well potential energy surface.

shows potential energy surface scans of this proton motion for the cgg+g− conformer, demonstrating that these two structures are intimately linked together. It seems plausible that this coupling of these conformers also influences the frequency of the carbonyl stretch calculated harmonically. The [COOH] and [CO2−] conformers lie 2−12 and 4−18 kJ/mol, respectively, higher in energy than the K+(His) GS. For Rb+(His) and Cs+(His), the [COOH]-cgg+g− conformer is the predicted 1538

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the increasing cation size, being predicted at 1398, 1395, and 1394 cm−1 for K+(His)−Cs+(His). These predicted frequencies lie close to the observed peaks of ∼1390, ∼1385, and ∼1394 cm−1 for K+(His)−Cs+(His), respectively, suggesting the presence of this conformer. The observed band at ∼1650 cm−1 in the K+(His)−Cs+(His) spectra is not accurately predicted for any of the conformations. This band is attributed to a CO stretch and first appears in the IRMPD action spectrum for K+(His) at 1647 cm−1 and blue shifts to ∼1670 cm−1 for Cs+(His). Calculated spectra of [COOH] conformers predict this band shifts from 1695 to 1711 cm−1 in going from K+(His) to Cs+(His), values that are too high compared to the observed bands. Calculated spectra for [CO2−] conformers indicate this band should appear at 1591, 1594, and 1624 cm−1 for K+(His)−Cs+(His), respectively, which are too low compared to the observed bands. As suggested above, this may indicate the inability of theory to properly describe the CO stretch for these related conformers. For the [COOH] conformers, the 1100−1600 cm−1 region contains several modes of mixed character that explain the broader peak observed around 1400 cm−1. Prominent new peaks emerging at ∼1493, 1209, 823, and 758 cm−1 for K+(His), 1496, ∼1215, 826, and 762 cm−1 for Rb+(His), and 1495, ∼1200, 828, and 762 cm−1 for Cs+(His) are predicted by [COOH] conformers well. 3.7. Comparison to Ca2+(His) and Ba2+(His). Previously, Dunbar et al. reported IRMPD spectroscopy of gas phase doubly charged alkaline earth complexes of histidine.30 Supported by theory, they found a transition from predominantly salt-bridge (SB) [CO2−] complexation for Ba2+ to a substantial presence of the charge-solvated (CS) structure [CO,Nα,N1] for Ca2+ and to completely CS [CO,Nα,N1] binding for Na+.30 The carbonyl stretching mode in the observed Ca2+(His) spectrum at 1680 cm−1 is reproduced well by the predicted spectrum of the [CO,Nα,N1] conformer and is red-shifted by ∼70 cm−1 compared to Cs+(His). The [CO,Nα,N1] calculated spectrum for Ca2+(His) also predicts a band associated with the COH bending mode at 1170 cm−1, which is blue-shifted by ∼15 cm−1 from Cs+(His). The shifts in both bands are consistent with a larger perturbation on the carbonyl by the much stronger binding dication. These two characteristic IR bands for the CS [CO,Nα,N1] conformation are not observed in the Ba2+(His) spectrum. Instead, both Ca2+(His) and Ba2+(His) exhibit a band at ∼1600 cm−1, which Dunbar et al. assign to a CO stretch of the SB [CO2−] conformation. The comparable band in the Cs+(His) spectrum is at 1647 cm−1, ∼50 cm−1 higher, a comparable red shift as for the CS [CO,Nα,N1] carbonyl stretch, but for Cs+(His), this band is most probably assigned to the CS [COOH] structure, as detailed above. One possible explanation for this difference in assignments (CS versus SB) is that Dunbar et al. did not completely explore all possible CS structures, as they do not mention [CO,N1] and [COOH] conformations, which are low-lying here, nor [HO,Nα,N1], [Nα,N1], [CO,Nα], [COOH,N1], [OH,N1], and [OH,Nα] conformers. To evaluate this possibility further, we have explored conformations of Ca2+(His) and Ba2+(His) more thoroughly, with the results obtained shown in Table 2. Notably, we find a lower energy salt-bridge conformer for Ca2+(His) than previously located. The [CO2−,N1]-cNαgg−g+ structure is a lower energy version (by 5−8 kJ/mol for both Ca and Ba complexes) of the [CO2−,N1]-cNαgg+g− structure (called SB3 by Dunbar et al.) found previously and differs only in the side chain conformation such that it has a nearly identical predicted IR spectrum. As Dunbar et al. find evidence for the population of a SB conformer

ground state at the B3P86 level and still low in energy at the other levels of theory. This trend in relative energies is consistent with the observation that this band grows in intensity as the metal gets heavier, Figure 1. The [CO2−] conformer lies 11−19 and 29−42 kJ/mol higher than the Rb+(His) and Cs+(His) GSs, respectively, and for some variants (such as the cgg+g− conformer shown in Figure 6) collapses to the [COOH] conformer (see Table S2, Supporting Information). Overall, the experimental spectra for K+(His)−Cs+(His) appear to have features commensurate with contributions from the [CO,N1], [CO,Nα,N1], and [COOH] conformers, consistent with the relative free energies calculated for these systems, Table 1 and Figure 3. In addition, the intensity of the modes associated with [CO,Nα,N1] for Cs+(His) are less intense compared to the K+(His) and Rb+(His) spectra, consistent with the change in relative energies of these conformers with metal ion, Figures 3 and S2, Supporting Information. Contributions from [CO2−], [CO,Nα], and [COOH,N1] conformers cannot be ruled out experimentally, and indeed the relative free energy for K+(His) [CO2−] could be as low as ∼4 kJ/mol, but this conformer collapses to [COOH] for Rb+(His) and Cs+(His). The [CO,Nα] and [COOH,N1] conformers lie 7−19 and 22−50 kJ/mol above the GS, suggesting they should not be highly populated for any of the three metal complexes. Also, calculations for K+(His)− Cs+(His) indicate that any of the other conformers lie at least 16 kJ/mol higher in 298 K free energy, suggesting that they contribute much less than 1% to the overall population. 3.6. Overview. We can now provide a more global comparison of the main features in all five spectra in Figure 1. The predicted frequencies for the CO stretch of the [CO,Nα,N1]tgcg conformer change from 1719 cm−1 for Li+(His) to 1731, 1736, 1743, and 1745 cm−1 for Na+(His)−Cs+(His) respectively, in agreement with the observed blue shift in the experimental spectra from 1732, 1747, 1750, 1753, and 1753 cm−1, respectively. The CO stretch of the [CO,N1]-ctg−g+ conformer shows a similar shift changing from 1739, 1748, and 1755 cm−1 for K+(His)−Cs+(His). These blue shifts result from decreased perturbations on the CO stretch as the metal cation binding strength decreases. The observed band at 1157 cm−1 in the Li+(His) spectrum red shifts to 1125 cm−1 for Cs+(His). This shift is consistent with that predicted for the COH bending motion of [CO,Nα,N1]-tgcg conformers with predicted frequencies of 1169, 1154, 1150, 1146, and 1143 cm−1 for Li+(His)−Cs+(His). The observed band at ∼1590 cm−1 in all of the spectra is not accurately predicted because of the anharmonicity in the bending motion of the NH2 group. This band does not shift with metal cation identity, in agreement with the predictions for the [CO,Nα,N1]-tgcg conformers (as well as other conformers). Bands near 1430 cm−1, which become a high-frequency shoulder of the more intense band near 1390 cm−1 in the spectra for K+(His)−Cs+(His), are observed in all of the spectra, Figure 1, and no shifts are predicted for the [CO,Nα,N1] conformers. The band at ∼589 cm−1 observed in the Li+(His) spectrum is red-shifted to 583 cm−1 for Na+(His). The good agreement in these trends provides further evidence that contributions from the [CO,Nα,N1]-tgcg conformer are present in all the IRMPD action spectra in Figure 1. The theoretical results for K+(His), Rb+(His), and Cs+(His) indicate that the [CO,N1] conformers are low-energy structures and could contribute to the IRMPD action spectra. This conformer has an intense band predicted near 1400 cm−1, corresponding to the COH bending motion, and is the most diagnostic band for this species in the calculated spectra. This motion is largely unaffected by 1539

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present in the IRMPD spectra for the K+, Rb+, and Cs+ complexes, consistent with the relative energetics calculated for various conformers, Figure 2. For Li+ and Na+ complexes of His, the charge-solvated, tridentate structure that binds the metal cation to the backbone carbonyl oxygen, backbone amino nitrogen, and imidazole side chain nitrogen, [CO,Nα,N1], is the only structure needed to reproduce the IRMPD action spectra, in agreement with the predicted ground states of these complexes. The photodissociation spectra of K+(His), Rb+(His), and Cs+(His) have very similar spectral features and are considerably more complex than IRMPD spectra of Li+(His) and Na+(His). For these complexes, the bidentate [CO,N1] conformer in which the metal cation binds to the backbone carbonyl oxygen and imidazole side chain nitrogen, is a dominant contributor, although contributions from the tridentate [CO,Nα,N1] conformer remain, and evidence for the bidentate [COOH] structure is also present.

Table 2. B3LYP/6-311+G(d,p) 298 K Free Energies (0 K Relative Enthalpies) in kJ/mol of Low-Lying Conformers of Ca2+(His) and Ba2+(His)a structure

ref 30b

dihedralc

Ca2+(His)

Ba2+(His)

[CO,Nα,N1] [CO2−,N1] [CO2−,N1] [CO2−] [CO−,Nα] [CO,Nα] [CO−,N1] [CO−,N1] [CO2−] [CO2−] [CO,N1] [CO,N1] [OH,Nα,N1] [COOH,N1] [Nα,N1] [OH,N1] [OH,Nα]

CS1

tgcg cNαgg−g+ cNαgg+g− cN1cgc cggg cggg ctg+g− ctg−g+ cN1ggc(t) cN1gg+g− ctg+g− ctg−g+ tgcg cggg tggg tgtg tttc

0.0(0.0) 17.9(18.2) 23.8(23.5) 24.1(28.4) 32.5(35.4) [CO−,Nα] 38.8(41.3) 42.5(45.8) 48.8(54.6) 49.0(54.0) 52.3(54.4) 58.8(60.4) 59.0(59.7) 94.2(94.0) 99.7(104.2) 165.2(170.6) 188.4(191.4)

7.6(4.3) 11.7(8.7) 19.5(15.9) 0.0(0.0) 12.3(11.0) [CO−,Nα] 32.1(31.0) [CO2−,N1] 24.5(25.6) 22.4(23.2) 38.5(36.8) 40.1(37.9) 63.2(60.7) 68.3(65.3) [CO,Nα,N1] 141.2(142.4) 151.7(151.4)

SB3 SB1 SB2 SB4

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ASSOCIATED CONTENT

S Supporting Information *

Structures of the M+(His) complexes calculated at the B3LYP/ HW*/6-311+G(d,p) level of theory; 298 K Gibbs free energies calculated at the R/6-311+G(2d,2p)//B3LYP/6-311+G(d,p) (M+ = Li+, Na+, K+) and R/HW*/6-311+G(2d,2p)// B3LYP/ HW*/6-311+G(d,p) (M+ = Rb+ and Cs+) levels, where R = B3LYP and B3P86 for thirteen distinct conformations; theoretically predicted IR spectra of low-lying conformations of His with structures calculated at the B3LYP/6-311+G(d,p) level of theory; theoretically predicted IR spectra of representative higher energy conformations of Li+(His) and K+(His); comparison between the experimental IRMPD spectrum and theoretically predicted IR spectra of low-lying conformations of Na+(His), Rb+(His), and Cs+(His); relative energies at 0 K and free energies at 298 K (kJ/mol) of low-lying conformers of M+(His); vibrational frequencies and IR intensities for the different conformations for M+(His) calculated at the B3LYP/6-311+G(d,p) (M+ = Li+, Na+, and K+) and B3LYP/HW*/6-311+G(d,p) (M+ = Rb+ and Cs+) levels of theory. This material is available free of charge via the Internet at http://pubs.acs.org.

a

Structures and zero point energies calculated at the B3LYP/6311+G(d,p) level of theory. The SDD basis set and relativistic ECP was used for Ba. Bold indicates the ground state. Entries having alternate structures indicate the calculation collapsed to the indicated structure. bStructural designation from ref 30. cDihedral angles for ∠HOCC, ∠OCCC, ∠CCCC, and ∠CCCN1, and in some cases, another dihedral angle is added to define the lone pair orientation of the NαH2 group (see text for detail).

along with the dominant CS contribution, this lower energy conformer brings experiment and theory in closer agreement. With this one exception, the lowest energy structures found by Dunbar et al. are confirmed to be the low-energy structures here, although we find several additional structures at somewhat higher energies, including [CO− ,N 1 ], [CO,N 1 ], [OH,Nα ,N 1 ], [Nα ,N 1 ], [COOH,N1], [OH,N1], and [OH,Nα] conformers ([CO,Nα] collapses to [CO−,Nα]). In all cases, these structures lie below the three highest energy structures reported by Dunbar et al., which all involve binding to the N3 position. Ultimately, the existence of these additional conformers do not alter the conclusions of Dunbar et al.; therefore, we believe the distinction between the CS and SB assignments again lies in the dichotomy presented by the double well potentials shown in Figure 6, which blur the distinction between the SB [CO2−] and CS [COOH] conformations. As shown in Figure 6, the higher charge density of the doubly charged ions shifts the potentials strongly in favor of the salt bridge, even more so than the small alkali cations, Li+ and Na+.

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AUTHOR INFORMATION

Corresponding Author

*Tel: +1 801 581 7885. Fax: +1 801 581 8433. E-mail: armentrout@ chem.utah.edu. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Financial support was provided by the National Science Foundation, Grants PIRE-0730072 and CHE-1049580. This work is also part of the research program of FOM, which is financially supported by the Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO). The skillful assistance of the FELIX staff is gratefully acknowledged. In addition, we thank the Center for High Performance Computing at the University of Utah for the generous allocation of computer time.

4. CONCLUSIONS IRMPD action spectra of cationized histidine in the region of 550−1800 cm−1 have been obtained for complexes with Li+, Na+, K+, Rb+, and Cs+. Comparison of these experimental spectra with IR spectra calculated at the B3LYP/6-311+G(d,p) (Li+, Na+, and K+ complexes) and B3LYP/HW*/6-311+G(d,p) (Rb+ and Cs + complexes) levels of theory allow the conformations likely to be present in the experiment to be identified. Comparison of the IRMPD spectra shows that the features observed in the Li+(His) spectrum are retained for all of the metal cation complexes but that new spectral features begin to appear for K+(His) and become very obvious for Cs+(His). These progressions suggest multiple conformers are

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REFERENCES

(1) Roth, A.; Breaker, R. R. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 6027−6031. (2) Dodson, G.; Wlodawer, A. Trends Biochem. Sci. 1998, 23, 347−352.

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