Solving the Tautomeric Equilibrium of Purine through Analysis of the

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Letter

Solving the Tautomeric Equilibrium of Purine through the Analysis of the Complex Hyperfine Structure of the Four N Nuclei 14

Laura Bianca Favero, Iciar Uriarte, Lorenzo Spada, Patricia Ecija, Camilla Kumar Calabrese, Walther Caminati, and Emilio J. Cocinero J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.6b00374 • Publication Date (Web): 10 Mar 2016 Downloaded from http://pubs.acs.org on March 14, 2016

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The Journal of Physical Chemistry Letters

Solving the Tautomeric Equilibrium of Purine through the Analysis of the Complex Hyperfine Structure of the Four 14N Nuclei Laura B. Favero1, Iciar Uriarte2, Lorenzo Spada2,3, Patricia Écija2, Camilla Calabrese2,3, Walther Caminati3*, Emilio J. Cocinero2* 1

Istituto per lo Studio dei Materiali Nanostrutturati (ISMN), Sezione di Bologna CNR, Via Gobetti

101, I-40129, Bologna, Italy. 2

Departamento de Química Física, Facultad de Ciencia y Tecnología, Universidad del País

Vasco (UPV/EHU), Apartado 644, E-48080 Bilbao, Spain. 3

Dipartimento di Chimica “G. Ciamician” dell’Università, Via Selmi 2, I-40126 Bologna, Italy.

Corresponding Authors: Walther Caminati3*, E-mail: [email protected]

Emilio J. Cocinero2* E-mail: [email protected] Homepage: http://www.grupodeespectroscopia.es/MW

ACS Paragon Plus Environment

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ABSTRACT. The rotational spectra of two tautomers of purine have been measured by pulsed jet Fourier Transform microwave spectroscopy coupled to UV ultrafast vaporization system. The population ratio of the two main tautomers [N(7)H]/[N(9)H] is about 1/40 in the gas phase. It contrasts with the solid state where only the N(7)H species is present, or in solution where a mixture of both tautomers is observed. For both species, a full quadrupolar hyperfine analysis has been performed. This has lead to the determination of the full sets of diagonal quadrupole coupling constants of the four

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N atoms, which have provided crucial information for the

unambiguous identification of both species. This work shows the great potential of microwave spectroscopy to study isolated biomolecules in the gas phase. All the work was supported by theoretical calculations. TOC Graphics


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Conformational/tautomeric equilibria of isolated biomolecules in the gas phase have been investigated during the last years, thanks to the developments of techniques mainly based on laser spectroscopy: resonant-enhanced multiphoton ionization (REMPI), laser-induced fluorescence excitation (LIF),1 rotationally resolved laser induced fluorescence,2 stimulated emission pumping (SEP)-population transfer spectroscopy (SEP-PTS), SEP-hole filling (SEPHF)3 or double/triple resonance methods IR or UV with mass selected and conformer specific coupled to laser spectroscopy experiments.4-8 Chiral recognition by mass spectrometry,9 or Helium nanodroplets techniques have also been applied to investigate vibrational spectra of biological molecules.10 However, they produce an over-simplification of the spectra, resulting in a loss of spectral content. Conformational or tautomeric assignments require, within the above mentioned techniques, the support of accurate theoretical calculations. Even so, the assignments are not always conclusive. Due to its inherent spectral resolution (7 kHz in the present case), rotational spectroscopy provides the most accurate vision of the molecular structure. It was initially restricted to the investigation of small molecules but in the last years, with the advent of pulsed jet Fourier transform microwave (FTMW) spectroscopy11,12 and broadband (chirped pulse) CP-FTMW spectroscopy,13 it has turned into a very competitive technique in the studies of moderate-size biomolecules. It can indeed provide many fine details (tunneling splitting, quadrupole hyperfine structures, interaction energies…) which supply chemical information difficult to be achieved otherwise. More recently, laser vaporization techniques have been combined with microwave spectroscopy,14 to unravel conformational equilibria of several amino acids,15,16 to study the conformational/tautomeric

forms

of

some

nucleobases,17,18

and

to

resolve

the

conformational/tautomeric scope of some sugars.19-21


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Nucleobases (nitrogenous bases or bases in genetics) are organic compounds with 2 or more nitrogen atoms, see Scheme 1. These biological compounds are found linked to a sugar within nucleosides, the building blocks of DNA or RNA. The rotational spectra of nucleobases are complicated because of the nuclear quadrupole coupling effects. The 14N nuclei posses a nuclear spin I = 1 and each one produces a splitting of the rotational transitions into several hyperfine components. Nucleobases have 2-5 nitrogen atoms which generate indeed very complex hyperfine pattern. Occasionally, this hyperfine structure of the 14N nuclei has been eliminated (or simplified) by replacing one or several 14N with 15N nuclei, which have a nuclear spin I = 1/2. So far, it has been possible to analyze the quadrupolar effect of up to three 14N nuclei (e.g. in cytosine18). But this hyperfine analysis was not possible for guanine,19 which contains five

14

N

nuclei. In this case, no attempt was made to assign the quadrupole hyperfine components and the rotational frequencies were measured as the intensity-weighted mean of the line clusters. However a provisional set of rotational constants was estimated for tautomers. Purine belongs to a series of molecules characterized by two aromatic rings, one six- and one five-membered, fused together to give a planar aromatic bicycle. Indene would be the prototype of this family, while purine would be its most important member. The compounds have an interesting electronic system which generally allows the observation of the electronic transition A1A'(π*-π)-X1A'. The tautomeric behaviour of purine consists of two main forms, N(9)H and N(7)H, drawn in Figure 1. The physicochemical properties of purine, a keystone of important biological bases, are useful for the interpretation of several biochemical processes. The knowledge of the N(9)H

N(7)H

tautomeric equilibrium is particularly relevant in this respect, as it can play a role in chemical mutagenesis.22


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N(9)H

N(7)H

Figure 1. The two main tautomers of purine. In the solid state purine exists as the N(7)H tautomer23 and in solution as a mixture of N(7)H and N(9)H tautomeric forms.24 A gas-phase UV PES study suggests - rather indirectly - the dominance of the N(9)H species,25 while contradictory results have been obtained with matrix isolation techniques.26 Several DFT and ab initio calculations predict the N(9)H form to be more stable by 15-40 kJ·mol-1.26-29 In a previous free jet absorption millimeter wave spectrum of purine, obtained by heating the sample to 140ºC in a pre-expansion furnace, only the N(9)H tautomer was detected.30 Purine, as shown in Scheme 1, is the mainframe of two of the five nucleobases: adenine and guanine.

Thymine

Uracil

Pyrimidine Bases

Cytosine

Adenine

Guanine

Purine Bases

Scheme 1. Purine is the mainframe of two of the five nucleobases. Our interest in studying purine was fueled mainly by two factors. First, purine has a high energy tautomer, not observed previously in the gas phase. Second, it has a very complicated hyperfine structure due, similarly to adenine and guanine, to four quadrupolar nuclei. Our goal is to unravel these two challenging tasks.


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Although several theoretical works – mentioned above - have been published on purine, no data concerning the spectroscopic parameters (rotational and quadrupole coupling constants, and electric dipole moment components) useful to analyze the rotational spectrum are available. For this reason, we performed several new calculations. The structures of the N(9)H and N(7)H species of purine have been optimized at MP2/6-311++G(d,p) level using GAUSSIAN09 package.31 Tautomer N(9)H has been predicted to be more stable than the N(7)H by 16.9 kJ⋅mol1

, a value which is reduced to 15.9 kJ·mol-1 when including the zero point energy corrections.

These data, together with the calculated spectroscopic parameters, are reported in Table 1. The meaning of the quadrupole coupling constants is explained later. Table 1. MP2/6-311++G(d,p) calculated spectroscopic parameters of the N(9)H and N(7)H tautomers of purine.

A, B, C/MHz N1: χaa, χbb, χcc, χab/MHz N3: χaa, χbb, χcc, χab/MHz N7: χaa, χbb, χcc, χab/MHz N9: χaa, χbb, χcc, χab/MHz |µa|, |µb|/Da ∆Ε , ∆Ε0/kJ⋅mol-1 a

N(9)H

N(7)H

4099, 1750, 1227 -3.502, 0.381, 3.121, 2.540 1.659, -4.663, 2.630, 0.111 1.567, -3.171, 1.605, -1.690 1.432, 1.508, -2.940, -0.118 3.0, 2.3 0.0,b 0.0c

4101, 1745, 1224 -3.553, 0.367, 3.187, -2.478 1.427, -4.633, 3.207, -0.098 1.680, 1.488, -3.168, -0.138 1.373, -3.379, 2.005, -1.570 3.1, 5.0 16.9, 15.9

µc = zero due to the planarity. bAbsolute energy = -410.922989 Eh. cZero point corrected

absolute energy = -410.829145 Eh. The rotational and centrifugal distortion constants of the N(9)H tautomer were available from the mmw study mentioned above.30 Based on these data, we could easily locate the 303 ← 202 transition. It appeared as a ~ 3.5 MHz wide band, centered at about 8660.7 MHz. Several other µa-type R-branch and four µb-type R-branch transitions were identified. Transitions with J = 1 to 5 and with K-1 = 0 to 2 could be measured.


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Once the N(9)H tautomer was measured, we performed the search of the rotational spectrum of the high energy N(7)H tautomer. First we empirically corrected the ab initio rotational constants by the observed-calculated values determined for the N(9)H species. We could detect in this way the 404 ← 303 transition. Later on, one additional µa and some stronger µb-type R-branch transitions were measured, to a total of nine transitions. For each transition we could measure many hyperfine component lines (from 4 to 41, depending on the transition and on the tautomer). An example of the complexity of hyperfine structure is shown in Figure 2 for the 221 ← 110 transition of the N(9)H tautomer. In that figure, the experimental spectrum (positive values, black) is compared to the calculated one (negative values, red). The simulated pattern has been obtained by using the AABS package (Assignment and Analysis of Broadband Spectra).32

Figure 2. The recorded (positive values, black) 221 ← 110 transition of the N(9)H tautomer is compared to its simulated pattern (negative values, red).


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All measured hyperfine component lines could be fit, independently for each tautomer, with Pickett’s SPFIT program33 and within Watson’s semirigid Hamiltonian (S-reduction; Irrepresentation),34 according to the following Hamiltonian: H = HR + HQ(14N1) + HQ(14N3) + HQ(14N7) + HQ(14N9)

(1)

HR represents the rigid-rotor Hamiltonian (no centrifugal distortion parameters were required) and HQ are the operators associated with the quadrupolar interactions of the four 14N nuclei with end-over-end rotation. The hyperfine correction calculations follow the coupling schemes F3=J+I(14N1), F2=F3+I(14N3) , F1=F2+I(14N7) and F=F1+I(14N9). The obtained spectroscopic constants are reported in Table 2. The defects of inertia ∆c are also showed in that table; their values are very close to zero, indicating the planarity of both tautomers. Comparisons of theoretical and experimental values of the rotational constants already outline the tautomeric assignment reported in Table 2 (there is a perfect agreement between the calculated and experimental differences of the rotational constants of the two tautomers). However, the definitive proof can be obtained from the values of the quadrupole coupling constants of the four 14N nuclei which act as a finger print for the correct assignment of the two spectra to the right tautomers. These parameters are very sensitive to small structural changes around of

14

N nucleus. Hence, they serve as a powerful tool to discriminate between different

conformers or tautomers.35 In particular, the χgg (g = a, b, c) parameters of nuclei N9 and N7, which interchange their values in going from N(9)H to N(7)H, are very significant in this sense. The quadrupole coupling constants are related to the gradient of the electric field at the quadrupolar nucleus within the inertia principal axes system, through the relation χgg = eQ(∂2V/∂c2)g=0 (g = a, b, c) and are less adequate to distinguish between different bonding situations of N atoms. These parameters only have a physical meaning if the quadrupole tensor is expressed within its principal axes system, generally labeled as χx, χy and χz. Then, iminic and


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pyrimidinic nitrogen atoms have quite different values from each other. In our case, purine being planar, χcc ≡ χy. For this reason, we can use these values to discriminate between the different kinds of N nuclei. We list the eight experimental χcc values in Table 3.

Table 2. Experimental spectroscopic parameters of the observed N(9)H and N(7)H tautomers (Sreduction, Ir representation).

A/MHz B/MHz C/MHz

N(9)H

N(7)H

4125.8895(2)a 1755.1720(1) 1231.55819(6)

4127.3813(3) 1749.7594(3) 1229.42760(7)

[N1]

χaa/MHzb χbb/MHz χcc/MHz

-3.343(5) 0.440(6) 2.904(6)

-3.560(15) 0.566(17) 2.994(17)

[N3]

χaa/MHz χbb/MHz χcc/MHz

1.673(7) -4.229(9) 2.555(9)

0.695(11) -2.744(20) 2.049(20)

[N7]


1.547(7) -3.379(9) 1.833(9)

1.254(11) 1.532(16) -2.786(16)

[N9]


1.489(5) 1.495(7) -2.985(7)

1.541(11) -3.239(18) 1.699(18)

-0.0693(3)

-0.2046(4)

∆c/uÅ2 σ /kHzc Nd

4.8 251

4.9 95

a

Error in parentheses in units of the last digit. bOff-diagonal χab quadrupole coupling constants are undetermined from the fit and have been fixed to the ab initio values (Table 1). cRMS error of the fit. dNumber of distinct frequency lines in the fit.


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Table 3. χcc of the four 14N nuclei of the N(9)H and N(7)H tautomers.

χcc values (MHz) of 14N nuclei in isolated

N(9)H

N(7)H

χcc[N1]/MHz

2.904(6)

χcc[N3]/MHz

2.555(9)

χcc[N7]/MHz

1.833(9)

χcc[N9]/MHz

-2.985(7)

2.994(17) Pyrimidine N: 3.5584(7)a b 2.049(20) Pyrrole N: -2.704(4) c -2.786(16) Imidazole N1 (pyrrole-like): -2.559(9) Imidazole N3 (pyrimidine-like): 2.228(8)c 1.699(18)

a

pyrimidine, pyrrole and imidazole

From Ref. [36]. bFrom Ref. [37]. cFrom Ref. [38]. From the χcc values of Table 3 one can note that N1 and N3 are pyrimidine-like nuclei for both

tautomers. Instead, N7 is pyrimidine-like in tautomer N(9)H and pyrrole-like in N(7)H; the contrary is true for N9, providing a doubtless identification of the two tautomers. The pyrimidinic χcc values of N1 and N3 are on the average 30% smaller than χcc in isolated pyrimidine. A similar decrease is observed in the pyrimidine-like imidazolic

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N (N7 or N9)

nucleus with respect to isolated imidazole, while an increase in the absolute value is observed in

χcc values (which are negative) in the pyrrole-like N7 or N9 nucleus. Probably this effect is related to the higher π-electrons delocalization in purine with respect to isolated pyrimidine and imidazole rings.

Relative intensity measurements of some pairs of nearby transitions allowed the estimation of the relative population of the two tautomers. µa-type and µb-type rotational transitions were used for this task. We obtained NN(9)H/NN(7)H ≈ 40(15)/1. As outlined in other works,39 the observed relative abundances of tautomers in the jet plume is the consequence of a series of processes that include the laser vaporization, a complex process which could alter the thermodynamic equilibrium situation. In addition, the relative concentration of the two species could also be related to their molecular fractions in the solid state sample.20 Despite this, our study clearly


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demonstrates the high dominance of the N(9)H tautomer, a fact that generated controversy in previous studies.25-26 In case of a Boltzmann distribution in the pre-expansion (but this is not certain), this ratio would correspond to ∆E = 9(1) kJ⋅mol-1 in favour of N(9)H, against the 15.9 kJ⋅mol-1 predicted theoretically. Although the calculated value is also very dependent on the method used.26-29 Details of the methodology are given in SI.

In summary, with the combination of Fourier transform microwave technique and ultrafast laser vaporization, we unambiguously confirmed the N(9)H tautomer and extended the measurements to the centimeter region. We also assigned the rotational spectrum of the very high energy N(7)H tautomer and for both species we unraveled the very complex hyperfine structure due to interaction of the angular momenta generated by the end-over-end rotation with the spins of the four

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N quadrupolar nuclei. The full sets of diagonal quadrupole coupling

constants allow for a definitive tautomeric assignment, difficult to be achieved with other techniques.

Experimental

A solid target rod was prepared by pressing a mixture, beforehand stirred, composed of few drops of a commercial binder and of ∼0.8 g of purine (Sigma Aldrich, 98%, mp = 214-217 °C). A picosecond-pulsed Nd:YAG laser, operating in the third harmonic (355 nm), vaporized the rod in the presence of a mixture of Ne:He 80:20 at stagnation pressure of 6 bar. Then, through the 1.0 mm ablation nozzle, the sample was supersonically expanded into the Fourier-transform microwave (FTMW) spectrometer described elsewhere.19,40 The rotational spectrum was recorded in the operating range of the instrument (4-18 GHz) built at the UPV/EHU. The


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accuracy of the frequency measurements is below 3 kHz. Rotational transitions separated less than 7 kHz are resolvable.

ASSOCIATED CONTENT Supporting Information. 1) Completion of Reference 31; 2) Tables of transition frequencies; 3) Ab initio geometries of the N(9)H and N(7)H tautomers of purine. This material is available free of charge via the Internet at http://pubs.acs.org. Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. All authors contributed equally. Funding Sources We thank the MINECO (CTQ-2014-54464-R), the Basque Government (IT520-10) and the UPV/EHU (UFI11/23) for funds. E.J.C. and I.U. acknowledge a “Ramón y Cajal” contract and FPU grant from the MICINN. Computational resources of SGIker and laser facilities at the UPVEHU were used in this work (SGIker). W.C. and L.B.F. thank Italian MIUR (PRIN project 2010ERFKXL_001). L.S. thanks the University of Bologna for a scholarship. REFERENCES (1)

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Pratt, D. W. Molecular Dynamics: Biomolecules see the Light. Science. 2002, 296, 23472348.


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Solving the Tautomeric Equilibrium of Purine through Analysis of the

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