Electronic Circular Dichroism Spectroscopy of Jet-Cooled

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Letter

Electronic Circular Dichroism Spectroscopy of JetCooled Phenylalanine and Its Hydrated Clusters Aram Hong, Heeseon Jang, Changseop Jeong, Myoung Choul Choi, Jiyoung Heo, and Nam Joon Kim J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.6b01894 • Publication Date (Web): 21 Oct 2016 Downloaded from http://pubs.acs.org on October 21, 2016

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The Journal of Physical Chemistry Letters

Electronic Circular Dichroism Spectroscopy of Jetcooled Phenylalanine and Its Hydrated Clusters Aram Hong,† Heeseon Jang,† Changseop Jeong,† Myoung Choul Choi,‡ Jiyoung Heo, *, § and Nam Joon Kim*,†

†Department

‡Mass

of Chemistry, Chungbuk National University, Chungbuk 28644, Korea

Spectrometry & Advanced Instrument Group, Korea Basic Science Institute, Ochang Center, Chungbuk 28119, Korea

§Department

of Biomedical Technology, Sangmyung University, Chungnam 31066, Korea

Corresponding Author * E-mail: [email protected] (N.J. Kim) and [email protected] (J. Heo).

ACS Paragon Plus Environment

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ABSTRACT

We obtained resonant two-photon ionization circular dichroism (R2PICD) spectra of jet-cooled phenylalanine (Phe) and its hydrated clusters (Phe(H2O)n, n=1-2) near the origin band of the S0S1 transition. The R2PICD spectra of Phe exhibit well-resolved CD bands of six different conformers present in the jet, which vary in sign and magnitude depending on their conformations. We revised the previous structural assignments of the Phe conformers based on the comparison between the experimental and theoretical CD signs, infrared spectra, and rotational band contours. The R2PICD spectra of Phe(H2O)n reveal that hydration with one or two water molecule(s) does not affect the CD signs of Phe conformers but significantly increases their CD magnitudes. Furthermore, conformational selection by solvation alters relative populations of Phe conformers, leading to a sign inversion in the CD spectra of Phe(H2O)n compared with that of Phe monomer.

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Since its first introduction in 18951, circular dichroism (CD) spectroscopy has provided a powerful tool to investigate the structures and structural changes of chiral compounds, particularly proteins and peptides in various environments because it is fast, inexpensive, and effective compared with other sophisticated tools, such as X-ray crystallography and nuclear magnetic resonance spectroscopy2,3. The CD spectra of proteins in the far-ultraviolet (UV) region reflect the secondary structures2, whereas those in the near-UV region provide information on the tertiary structures. The absorption of proteins in the near-UV region arises mainly from the π-π* transitions of the aromatic amino acids tryptophan (Trp), tyrosine (Tyr), and phenylalanine (Phe). Thus, the CD spectral features in this region are largely determined by the CDs of aromatic amino acids reflecting their mobility, spatial disposition, and environment in a protein. The site-directed substitution of a single aromatic amino acid has thus been used to probe local tertiary structures of proteins using near-UV CD spectroscopy4. However, gaining significant structural insights from near-UV CD spectra has been challenging because aromatic amino acids in different locations of a protein exist in many different conformations. Because CD is sensitive to the molecular conformation, each conformational isomer of an aromatic amino acid gives rise to its own CD spectral feature, which is averaged out by overlap with those from the other conformers. Based on this averaged CD spectrum, it is nearly impossible to collect detailed information about the individual conformations of aromatic amino acids. Therefore, CD spectroscopy must be applied to isolated molecules in the gas phase, where different conformers can be distinguished spectroscopically5, 6. CD spectroscopy of gas-phase molecules has been challenging to achieve because of the weak CD effects (10-5−10-3) that are aggravated by their low number density7-10. The CD for ion


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yields of 3-methylcyclopentanone in a molecular beam was investigated at selected wavelengths by resonance-enhanced multiphoton ionization (REMPI) using nanosecond and femtosecond lasers11-13. Velocity map imaging photoelectron spectroscopy has also been employed to investigate the CD effect of ionization of jet-cooled molecules14. However, CD spectra of jetcooled molecules over a wide wavelength range had not been measured until we obtained resonant two-photon ionization CD (R2PICD) and fluorescence-detected CD (FDCD) spectra of jet-cooled ephedrines using a new CD spectroscopic technique employing a photoelastic modulator (PEM)15,16. Both spectra exhibited well-resolved CD bands that were specific for the structures and vibrational modes of each conformer. Phe is a biological precursor of Tyr, L-DOPA, epinephrine, and thyroid hormones, and its conformational preference in jet-cooled conditions has been extensively studied for several decades17-20. Levy and coworkers17 first identified the origin bands of five Phe conformers in a supersonic jet. The structures of those conformers, and a sixth, were assigned using IR-ion dip spectroscopy18, which was later revised to incorporate the results of rotational band contour analysis19. Here, we obtain the first R2PICD spectra of phenylalanine (Phe) and its hydrated clusters (Phe(H2O)n, n=1–2) produced in a supersonic jet using the new CD spectroscopic technique15. The R2PICD spectra of L- or D-Phe exhibit well-resolved CD bands, which vary in sign and magnitude depending on the conformation. We verify the previous structural assignments of the conformers by comparing the experimental and theoretical CD values, infrared (IR) spectra, and rotational band contours. The solvation effects on CD values of each Phe conformer are also investigated using R2PICD spectroscopy of Phe solvated with one or two water molecule(s).


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1.0

(a)

D X

0.5

A B C

E

h g

f

i 0.0 (b)

R

0.01

L

I -I

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Ion signal (arbitrary unit)

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0.00

-0.01

37550

37600

37650 -1

Wavenumber (cm )

Figure 1. (a) R2PI spectrum of L-Phe recorded at the parent mass channel of m/z=165. The labels of the bands are adopted from the literature18. (b) R2PICD spectra of L- and D-Phe (blue and red lines, respectively) obtained by monitoring the difference between the ion signals produced by LCP and RCP pulses (IL-IR).

Figure 1a shows the R2PI spectrum of jet-cooled L-Phe near the origin band of the S0-S1 transition. The bands A~E and X were previously assigned as the origin bands of six different conformers of Phe (Fig. S1), and the bands f~i were the vibronic bands of those conformers18,19. Figure 1b is the R2PICD spectra of L- and D-Phe obtained by subtracting the ion signals produced by the right circularly polarized (RCP) pulses from those produced by the left CP (LCP) pulses. Both spectra exhibit mirror images of each other. The origin bands of different conformers have different CD signs despite having the same handedness. For instance, the CD signs of the bands B, D, E, and X of L-Phe are positive, but those of the bands A and C are negative. These results demonstrate that the CD signs of chiral molecules are determined not solely by their handedness but also by their conformations. This dependence of CD signs on


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molecular conformations results because CD arises from the interaction between the electric (µ) and magnetic transition dipole moments (M), which varies sensitively with the molecular structure15,21.

Table 1. Asymmetry factors, rotatory strengths, angles between µ and M, and relative Gibbs free energies of the low-energy conformers of L-Phe. band

ga

Conformer b

Rc

θd

∆Ge

A

−0.8±0.2

VII

+0.58

100.3

1.46

IIIb1f

+0.04

90.6

1.33

III

−0.53

83.3

0.54

IVf

+0.26

93.1

0.00

B

+1.4±0.3

C

−1.1±0.2

VI

−0.29

83.5

1.33

D

+1.2±0.2

II

+0.58

101.4

0.91

E

+1.3±0.5

IX

+0.31

95.6

1.15

X

+1.7±0.5

I

+0.65

102.7

0.05

A’

−5.7±0.9

D’

+3.8±0.6

α

−10.7±0.6

a

Asymmetry factors g of the bands A~E and X in percentage. bConformers previously assigned to each band in the first column19. cRotatory strengths of the Phe conformers in cgs (10-40 erg·esu·cm/Gauss) predicted by TDDFT at the ωB97XD/6-311++G(d,p) level. dAngles between µ and M in degree. eRelative Gibbs free energies in kcal/mol estimated at 298.15 K. f Conformers newly assigned to the A and B bands in this work.

Table 1 lists the experimental asymmetry factors, g, of the bands A~E and X estimated from the R2PICD spectrum of L-Phe and the theoretical rotatory strengths, R, of the conformers


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assigned to each band. The g value is given as g=2(IL ‒ IR)/(IL + IR), where IL and IR are the ion signals produced by the LCP and RCP pulses, respectively11. The R value, which is given as the imaginary part of the dot product µ and M, represents the CD value21. The g values of the bands A~E and X are all in the range of 1~2%. The g signs of the C~E and X bands coincide well with the R signs of the conformers assigned previously to each band19, but those of the A and B bands do not. The disagreements between the g and R signs of bands A and B may result from the theoretical uncertainty of predicting the R value, which is determined by µ and M. The calculations of µ and M require the properties of the electronic excited state to be estimated, which are less accurate than those of the electronic ground state. However, the possibility that the theoretical uncertainty causes the disagreement between the g and R signs is low for the following reasons. First, the R values of conformers VII and III (+0.58 and −0.53, respectively), which were previously assigned to bands A and B, respectively, are as large as those of other conformers of bands C~E and X, which agree well with their g signs (Table 1). Because R is given as the dot product between µ and M, its sign varies depending on whether the angle between µ and M is smaller or larger than 90o. The magnitude of R also depends on that angle. As the angle gets closer to 90o, R value becomes smaller and its sign changes easily with a slight variation of the angle. In contrast, as the angle deviates farther from 90o, R value becomes larger. With a large R value, in spite of a certain degree of the theoretical uncertainty in estimating the angle between µ and M, the R sign is likely to remain unaltered. Indeed, the R sign of ephedrine (R=0.91) agrees well with its experimental CD sign but those of pseudo-ephedrine (R=0.01~0.17) do not15,16. Second, the R signs of conformers VII and III are all consistent, even in calculations with other exchange-correlation functionals, such as M06-2X and CAM-B3LYP.


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This may indicate that the theoretical uncertainties in predicting the R signs of conformers VII and III are very small. Another explanation for the disagreement between the g and R signs of bands A and B is that R2PICD, in principle, represents the cumulative CD of two-photon processes and does not necessarily correspond to the R value representing the CD of one-photon absorption. In other words, if we measure the CD of the one-photon absorption process of the S0–S1 transition, the R signs will agree with the g signs of bands A and B, respectively. We examined this possibility by measuring the FDCD spectrum of D-Phe (Fig. S2). In this case, the fluorescence is generated by one-photon absorption, and FDCD has been suggested to represent the CD of one-photon excitation, similar to the conventional CD or R value22. Notably, the CD signs of bands A and B in the FDCD spectrum are identical to those in the R2PICD spectrum. Therefore, we disregard the possibility that the disagreement between the experimental g and theoretical R signs of bands A and B may arise because R2PICD represents the CD of the two-photon absorption process. The other possibility is that this disagreement may result from incorrect assignments of the conformers to the bands A and B. Previously, the Phe conformers were assigned to each origin band based on the agreement between their experimental and theoretical IR spectra and rotational band contours18,19. However, those agreements may not be sufficient to unambiguously assign the conformers to bands A and B, especially for Phe, which has low-lying conformers that differ only in the conformation of the long and flexible backbone. Furthermore, the previous assignments were made by comparing those experimental results with the theoretical results of only nine Phe conformers originally found by Snoek et al.18 A larger number of low-lying Phe conformers has been reported within an energy range of 10 kJ/mol23,24. Here, we extend the


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comparisons to all of the low-lying conformers reported in the literature19,23-25, including 28 conformers we found using the CONFLEX program26. Band A was first assigned as the origin band of conformer V18, but this assignment was later corrected to conformer VII to incorporate the results of the rotational band analysis19. Of all Phe conformers investigated here, we found that conformer IIIb1, which is labeled according to the literature24, is the most probable conformer that can be assigned to band A. Conformer IIIb1 has nearly the same IR spectrum, rotational band contour, and relative Gibbs free energy as conformer VII (Figs. 2 and 3, and Table 1). However, uncertainty remains in the R sign of conformer IIIb1, which is positive for L-Phe and opposite to the CD sign of band A.

Figure 2. Structures of Phe(H2O)n (n=0–2) assigned to the bands A(VII, IIIb1), B(III, IV), A’(IIIb1-W1), α(IIIb1-W2), D(II), and D’(II-W1). All of those structures were optimized using DFT at the ωB97XD/6-311++G(d,p) level of theory.


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Figure 3. . Theoretical IR spectra and rotational band contours of conformers (a) IIIb1 (red) and (b) IV (red), which are nearly identical to those of conformers VII (blue) and III(blue), respectively. The theoretical IR spectra were computed using DFT at the B3LYP/6-311++G(d,p) level of theory. Rotational band contours were calculated using the AsyrotWin program with the rotational constants calculated with the optimized geometries in the S0 and S1 states at the ωB97XD/6-311++G(d,p) level of theory27.

However, we note that the R value of conformer IIIb1 is very small; in fact, it is an order of magnitude smaller than the R values of the other conformers in Table 1. This small R value of conformer IIIb1 results not from the small magnitudes of µ and M but from the angle between them, which is very close to 90o (Table 1). Thus, a slight alteration of the angle, possibly because of a slight variation in the molecular structure, can change the R sign. Therefore, considering the uncertainty in the theory used to estimate the geometric and electronic structures in the S0 and S1 states, unambiguously determining the R sign of conformer IIIb1 using time-dependent density functional (TDDFT) seems impossible at present.


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Recently, Lin et al.28 developed a theoretical method to simulate the vibrationally resolved electronic CD spectra considering both structures optimized at the S0 and S1 states. In this method, the vibronic profile is computed by considering both Franck-Condon (FC) and Herzberg-Teller (HT) contributions, which describe the vibronic coupling between different electronic states. Using this method, we estimated the CD sign of the 0-0 band of conformer IIIb1 to be identical to that of band A (Fig. S3). The assignment of conformer IIIb1 to band A is further supported by the agreement between the experimental and theoretical IR spectra (Fig. S4). The vibrational frequencies of conformer IIIb1 predicted using DFT at the B3LYP/6-311++G(d,p) level coincide better with the experimental frequencies than those of conformer VII. Band B was previously assigned as the origin band of conformer III, for which the R sign is opposite to its experimental g or CD sign. We found that conformer IV has nearly the same IR spectrum and rotational band contour as conformer III and that its R sign coincides with the CD sign of band B (Figs. 2 and 3, and Table 1). The relative Gibbs free energy of conformer IV is also the lowest for all Phe conformers (Table 1). Therefore, we suggest that conformer IV should be assigned to band B instead of conformer III. It was previously proposed that the isomerization barrier between conformers III and IV is so low that either of the conformers could be easily converted to the other, even under jet conditions29.


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D

Ion signal

0.8

A

(a)

D'

A'

0.1

(b)

L

I -I

R

0.02 0.00 -0.02

Ion signal

0.3

(c)

α

0.1

(d)

R

0.02

L

I -I

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0.00 -0.02

37500

37550

37600

37650 -1

Wavenumber (cm )

Figure 4. R2PI spectra of L-Phe(H2O)n (n=1–2) recorded at the mass channels of (a) Phe (m/z=165) and (c) Phe(H2O)1 (m/z=183). R2PICD spectra of L-Phe(H2O)n and D-Phe(H2O)n (blue and red, respectively) were recorded at the mass channels (b) m/z=165 and (d) m/z=183. The bands A’, D’, and α were labeled as in the literature30.

Figure 4 shows the R2PI and R2PICD spectra of Phe(H2O)n (n=1–2) produced in a supersonic jet using Ne carrier gas mixed with water vapor. Figures 4a and b were recorded at the mass of Phe (m/z=165), and Figures 4c and d were collected at the mass of Phe(H2O)1 (m/z=183). The bands A’ and D’ in Figure 4a were previously assigned to monohydrated clusters of the conformers of bands A and D, respectively, which were detected in the mass channel of Phe caused by fragmentation following ionization30,31. Similarly, the band α in the mass channel of Phe(H2O)1 (Fig. 4c) was assigned to a dihydrated cluster of the conformer of band A. Because


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we assign the band A to conformer IIIb1 in this work, the bands A’ and α are assigned to mono and dihydrated clusters of conformer IIIb1. Figures 4b and d are the R2PICD spectra of Phe(H2O)n. The CD spectra are also mirror images of each other. The CD signs of bands α and A’ are identical to that of band A, and the CD sign of band D’ is consistent with that of band D. The same CD signs of bare Phe and its hydrated conformers may indicate that the influence of hydration on the conformations of bare Phe is small, which is consistent with a previous report30. Water molecules are predicted to bind preferentially to the carboxyl group, forming a cyclic hydrogen bond that hardly affects the conformation of Phe (Fig. 2). Although the CD sign of bare Phe does not change following hydration, its magnitude increases significantly (Table 1). The increase of the CD magnitudes may be attributed to increased rigidity of the flexbile backbone of Phe by forming a cyclic hydrogen bond between the carboxyl group and water molecules. It was reported previously that the binding of water molecules to the imide group of poly(L-proline) rigidifies the chain32 and that CD spectra of rigid molecules are generally more intense than those of flexible molecules33. Further investigations are necessary to unravel the reason for such a large increase of the CD magnitude by hydration.

Among the six conformers of Phe present in the jet, only the conformer of band A forms both Phe(H2O)1 and Phe(H2O)2. This structural selection by microsolvation has also been observed for 3-indole-propionic acid and tryptamine34,35. As a result of the structural selection, the conformer of band A becomes dominant in the hydrated clusters, whereas those of bands D and X are dominant in bare Phe. Interestingly, the CD sign of band A and thus the signs of A’, and α are all opposite to those of bands D and X, which leads to a sign inversion between the CD


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spectra of bare Phe and its hydtared clusters. This illustrates the solvent effect on CD spectra that arises from the change in relative populations of different conformers by solvation.

The solvent effects on CD spectra were previously classified to two types, “primary” and “secondary” effects36. The primary effect is a change in the relative populations of different conformers present, and the secondary effect involves a shift in the spectral peak positions through stabilization of conformers by solvents. The primary solvent effect, however, cannot be demonstrated in solution because of the absence of conformational selectivity. The CD spectroscopy of jet-cooled molecules and their solvated clusters provide a powerful tool to investigate the solvent effects on CD spectra in a molecular level.

In conclusion, conformation-specific CD values of jet-cooled Phe measured by R2PICD spectroscopy provided crucial information to unambiguously determine the structures of the long and flexible aromatic amino acid. Among the six conformers of Phe present in the jet, two conformers have CD signs that are inconsistent with their theoretical values predicted by TDDFT. We raised the possibility that the previous structural assignments of the two conformers might be incorrect. We suggested two new structures for the conformers after extensive comparisons of the experimental and theoretical CD signs, IR spectra, and rotational band contours of low-lying Phe conformers. In the R2PICD spectra of Phe(H2O)n (n=1-2), we observed that solvation by one or two water molecule(s) does not affect the CD sign of bare Phe but increases its CD magnitude, which was attributed to increased rigidity of the Phe backbone through the formation of a cyclic hydrogen bond with water molecules. Conformational selection by solvation also plays a role in the sign inversion between the CD spectra of bare Phe and its


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hydrated clusters. Further investigation of larger hydrated clusters of Phe will reveal the effects of zwitterion formation on their CD values.

ASSOCIATED CONTENT Supporting Information The supporting information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpclett. Experimental and theoretical methods, and Figures S1~S4. (PDF)

AUTHOR INFORMATION Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT This work was supported by the Korea Basic Science Institute Grant (D36613) and the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2013R1A2A2A01014547 and 2015R1D1A1A01056663 (NJK), and NRF-2014R1A1A2055150 (JH)).


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