Microhydration Prevents Fragmentation of Uracil and Thymine by Low

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Microhydration Prevents Fragmentation of Uracil and Thymine by Low-Energy Electrons Jaroslav Kocisek, Andriy Pysanenko, Michal Farnik, and Juraj Fedor J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.6b01601 • Publication Date (Web): 15 Aug 2016 Downloaded from http://pubs.acs.org on August 15, 2016

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The Journal of Physical Chemistry Letters

Microhydration Prevents Fragmentation of Uracil and Thymine by Low-Energy Electrons J. Koˇciˇsek,∗ A. Pysanenko, M. Fárn´ık, and J. Fedor J. Heyrovský Institute of Physical Chemistry v.v.i., The Czech Academy of Sciences, Dolejˇskova 3, 18223 Prague, Czech Republic E-mail: [email protected]

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Abstract When ionizing radiation passes biological matter, a large number of secondary electrons with very low energies (< 3 eV) is produced. It is known that such electrons cause an efficient fragmentation of isolated nucleobases via dissociative electron attachment. We present an experimental study of the electron attachment to micro-hydrated nucleobases. Our novel approach allows a significant control over the hydration of molecules studied in the molecular beam. We directly show for the first time that the presence of a few water molecules suppresses the dissociative channel and leads exclusively to formation of intact molecular and hydrated anions. The suppression of fragmentation is ascribed to caging-like effects and fast energy transfer to the solvent. This is in contrast with theoretical prediction that microhydration strongly enhances the fragmentation of nucleobases. The current observation impacts mechanisms of reductive DNA strand breaks proposed so far on the basis of gas-phase experiments.

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Bond-breaking reactions induced by secondary low-energy electrons play crucial role in the interaction of ionizing radiation with living matter. 1 The seminal demonstration that DNA strand breaks can be caused by electrons with subionization 2 and even sub-excitation 3 energies with a resonant character has initiated much activity on electron-triggered fragmentation of building blocks of nucleic acids. 4 Especially, the second, lower, range of electron energies (below 3 eV) has been attracting much attention. This attention has been motivated by a high abundance of such slow electrons in the typical secondary-electron distribution, 1 and by the new discoveries concerning their generation (e.g., interatomic coulombic decay 5 ) and reactivity (e.g., electron pre-solvation 6,7 ). At electron energies below those of electronically excited states, the only elementary process leading to bond-cleavage in molecules is dissociative electron attachment, i.e., capture of incoming electron into an antibonding orbital forming a transient negative ion (resonance) and subsequent fragmentation of the molecule. All components of DNA (purinic and pyrmidinic bases, sugar and phosphate fragments) are susceptible to such fragmentation, 4 when probed in the gas phase. For example, all nucleobases (NB) form several resonances (NB∗− ) at electron energies below 3 eV that lead to a very efficient loss of a hydrogen atom from the nitrogen-site 4

NB + e− → NB∗− → (NB − H)− + H.

(1)

The natural question appears how this type of fragmentation is influenced by the presence of water, a vital component of a cell. Experimental approaches for answering such question are either “top-down”, trying to unravel the elementary processes in bulk aquaeous solution using recently developed techniques such as ultrafast electron-transfer spectroscopy 8 or liquid-jet photoelectron spectroscopy; 9 or “bottom-up”, in a molecular beam, microhydrating the target molecule by progressively adding water around it. Here we present, to our knowledge, the first study using the second approach in a well-defined manner: electron attachment to uracil and thymine with several water molecules attached. The basic question

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is if the transient anions still fragment. On one hand, it is well known that already the presence of single water molecule significantly increases the electron affinity of uracil 10 and all nucleobases commonly exist as intact molecular anions in bulk solution. 11 A fast stabilization of the resonant state NB∗− to bound molecular nucleobase anion is an important assumption in several models for reductive DNA damage. 4,12 On the other hand, it has been recently theoretically predicted 13 that microhydration of uracil actually strongly enhances the cross section for the fragmentation process (1) with the conclusion that the probability of such damage can be much higher than that in the gas-phase. Producing molecular beam of neutral hydrated biomolecules is not trivial. Even though there has been a significant progress 14–19 in producing mixed water/molecule cluster beams since the pioneering work of Hershbach, 20 the main complication remains in the composition of the beam. The pressures of the water and the biomolecule are difficult to control and the results are influenced by the clustering of molecules with each other or with the buffer gas. 21,22 Another persistent problem is the stability of the beam. In the present study we reach a significant control over the hydration process by humidification of the helium buffer gas through a membrane. Low stagnation pressures of He and evaporation temperatures of nucleobases are used so that pure molecular clusters of uracil and thymine are not generated. This way we are able to produce very stable beam of hydrated nucleobases. Figure 1 shows the negative ion mass spectra upon electron irradiation of the molecular beam with various composition. Three different conditions were probed for both uracil and thymine: pure molecular beam (no humidification), low degree of hydration (low stagnation pressure of the humidified buffer gas) and higher hydration degree (higher stagnation pressure). Electron attachment to pure nucleobases leads to their prompt fragmentation via loss of an H-atom and produces dehydrogenated anions (NB-H)− via process (1). This dramatically changes upon microhydration: spectra do not show any evidence of the (NB-H)− anions and fragmentation is completely suppressed. Upon electron attachment, only stable anions of the form NB(H2 O)− are formed. For uracil, even the isolated parent anion U− is clearly

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Uracil

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(U-H)

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0 100

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Figure 1: Cumulative negative ion mass spectra in the energy range from 0 to 3.5 eV (sum of all the mass spectra in the energy range with the step of 0.25 eV) for different targets. (a), (d): molecular beams of uracil and thymine without any humidification; (b), (e): mimimal degree of microhydration in the beam; (c), (f): higher degree of microhydration in the beam. detected which has to originate from electron attachment to hydrated uracil and subsequent evaporation of the water molecules. Figure 2 shows energy dependent ion-yield curves for the observed fragments. Our electron gun has been designed for operation at much higher electron energies for standard electron-impact mass spectrometry and the electron current below approx. 1.3 eV (shaded area in figure 2) is difficult to control. Nonetheless, the (NB-H)− ion yields for isolated nucleobases are in good agreement with the convoluted high-resolution gas-phase data. 23,24 Upon hydration, no (NB-H)− anions are observed within the detection limits of our experiment. What can be the reason for such inhibition of the dissociative channel 1? While in the gas phase, nucleic acid base anions exist in weakly bound dipole-supported states, 25 the hydrated anions are covalently bound. 10 The adiabatic electron affinity shifts form few tens

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Figure 2: Ion yield curves obtained from the dependence of mass-peak intensities on the electron energy. Solid lines are present data, the dashed lines in bottom panels are the gas-phase ion yields 23 convoluted with a Gaussian of 600 meV FWHM. The shaded areas indicate electron energy range where the confidence level of ion yield curves is lower. The signal-to-noise ratio in the molecular beam data is considerably worse: in order to prevent NB-NB clustering, the partial pressure (numerical density) of the bases in the dry buffer gas had to be kept very low. of meV to up to 1 eV (depending on number of water molecules) upon such transformation in uracil. 10,12 The asymptotic energetics upon hydration thus changes such that it indeed favors the non-dissociatve channel. However, fragmentation of resonant states is rarely driven by asymptotic energetics but rather by gradient of the resonant potential energy surface at the geometry of vertical electron attachment. 26 There are two possible causes for favoring the non-dissociative channel: (i) change of the electronic structure of NB due to the hydration prior to the attachment or (ii) initial motion in the direction of the dissociative channel (1) followed by the fast energy transfer to solvent that leads to redistribution of internal energy (caging) and stabilization of the intact anion. The second option seems to be much more probable: the scattering calculations 13 on small uracil-water clusters did not predict any dramatic change in the character of the resonant states, apart from their shift towards lower energies (approximately by 0.3 eV). Actually, the right shoulder of the present ion yields of hydrated species (figure 2) do show cutoff at lower electron energies when compared to (NB-H)− gas phase ion yields. Unfortunately, this effect cannot be interpreted unambiguously as a shift towards lower energies bearing in 6


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mind the electron gun resolution and the decrease of electron current in the shaded areas. Nonetheless, the present results are in a strong disagreement with the theoretical prediction 13 that the cross section for the dissociative channel in uracil substantially increases upon its microhydration. However, the dynamical part of that model did not take into account possible caging of the abstracted H-atoms by the water molecules that seems to be crucial. With this respect it is interesting to note, that the hydrogen abstraction is site-selective. 23 In the studied energy range, N1-H bond is cleaved preferentially around 1 eV and N3-H bond is cleaved preferentially around 2 eV. Since the (NB-H)− channel is completely suppressed, the H-atom caging and stabilization of molecular anion has to be very effective for both sites. In uracil, it even leads to dehydrated molecular anion U− . The Rydberg electron transfer experiments 27 have shown existence of such valence-bound monomer anion with the geometry considerably distorted when compared to the neutral uracil. Interestingly, at the same hydration conditions, we observe T(H2 O)− n with more water molecules attached (n > 0). This can be caused by better clustering of thymine with water (prior to the electron attachment) or by more effective evaporative cooling of the hot thymine anion-water complex after the electron attachment. The parent nucleobase anions have been also observed after electron interaction with nucleobase clusters in superfluid helium droplets. 28 On the other hand, the same experiments with only single nucleobases in He droplets do not show any evidence for parent anions. 29 In He, hydrogen abstraction becomes the most intense reaction channel in a strong contrast to present results for water. This difference is important in the context of biologically related studies, because it shows that model rare gas solvent can not fully reproduce the effects caused by more realistic solvent such as water. To our knowledge the only previous experimental work on electron attachment to hydrated biomolecular model compound is the recent study of pyrimidine-water clusters. 21 In contrast to present systems, the (Pyr-H)− channel has been observed in Ref. 21 as the only molecular fragmentation channel after hydration, albeit shifted to higher electron energies

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when compared to isolated molecule. However, in isolated pyrimidine, this fragmentation channel is mediated by a core-excited resonance, occurs at much higher electron energies (around 5 eV); and has actually minor abundance when compared to fragments resulting from the ring-opening (that are quenched upon clustering). Also, in contrary to the present single microhydrated biomolecules, the target beam in Ref. 21 was a mixture of pure pyrimidine clusters, hydrated clusters and pure water clusters, the pyrimidine-pyrimidine interaction could thus prevail the pyrimidine-water interaction. A similar effect has been recently observed by us in the hydrated nitrophenol clusters. 22 How do the present findings influence the picture of the electron-induced damage of living matter? Initially, it has been suggested 30 that process (1) produces H-radicals that eventually cause strand breaks. The occurrence of such direct fragmentation of nucleobases (especially thymine and guanine) even in solution by prehydrated electrons was later supported by the ultrafast spectroscopy data. 6 Our results suggest that in water environment the anions are quickly stabilized and form bound states. (Here, one should distinguish between the ballistic electrons in the present work and prehydrated electrons in the Ref. 6.) Such stabilization is an important part of different, widely accepted, model 31–34 that the nucleobase serves as an ’electron antenna’ and captures the electron, which is through-bond transferred to the backbone where it triggers fragmentation. However, from the electron attachment to the entire gas-phase nucleotide 35 it was estimated that such electron transfer is responsible for only 15% of the fragmentation, the rest is initiated by the direct electron attachment to the backbone where it causes cleavage of C-O or P-O bond between the sugar and phosphate moiety. The dramatic increase of the lifetime of the nucleobase anion upon hydration shown in this work can considerably increase the importance of the electron-transfer channel. 31,36 Even though we did not study a whole nucleotide, it has been theoretically suggested that in solution the excess electron in the vicinity of nucleotide is quickly localized around the nucleobases. 37 More recently, it has been proposed that in aqueous environment a proton transfer to a nucleobase anion significantly influences the barriers for strand-breaking reac-

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Figure 3: Schema of the experimental setup. tions.

33,38

Finally, the caging of transient anions by water is accompanied by fast energy

transfer to the solvent. Such heating may cause temperature and pressure spikes and cause additional damage to DNA. 39 In conclusion, we present a simple approach to study microhydrated biomolecules in molecular beams. In uracil and thymine, such microhydration prevents fragmentation via dissociative electron attachment. In aqueous environment, the involved resonant states thus serve as doorways to intact bound anions of these nucleobases. The quenching causes a significant energy transfer to the solvent, which has to proceed on a very short timescale.

Setup: The experimental configuration (figure 3) is identical to that described recently, 22,40 apart from the molecular beam source. The principle is as follows: the mixture of humidified helium and nucleobase vapor is expanded into the vacuum, the molecular beam is skimmed, crossed by an electron beam with a variable energy and the negatively charged products are mass-analyzed by a reflectron time-of-flight mass spectrometer. The humidification of helium is achieved using Pergo gas humidifier, a device commercially available from Elemental Scientific, originally intended for humidification of argon in inductively coupled-plasma mass spectrometry. It utilizes Nafion tubing that selectively permeates water vapor through its membrane, which humidifies the helium line. The humidified

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buffer gas then passes through an oven filled with uracil or thymine powder, which is connected to a conical nozzle with 90 µm diameter. The oven reservoir and the nozzle are both separately temperature-controlled, the latter is kept at slightly higher temperature in order to prevent sample condensation. The expansion conditions are summarized in table 1. The beam is skimmed and passes three differentially pumped vacuum chambers where it can be probed by other techniques not used in this work. The interaction point with the electron beam is thus located 1.5 meters downstream from the nozzle. The electron beam is produced in a pulsed electron gun (pulsing frequency 10 kHz). The electrons pass the interaction region for 2 µs and after a 0.5 µs delay, a 2 µs long negative high-voltage pulse is applied to extract the created anions to a reflectron time-of-flight mass spectrometer (RTOF). The mass resolution of the RTOF is 5 ×103 . Table 1: Conditions in the molecular beam source. P0 , Tr , Tp and Tw represent stagnation pressure, and temperatures of the nucleobase reservoir, nozzle and water reservoir, respectively. sample species Uracil Thymine Hydrated Hydrated Hydrated Hydrated

Uracil I Thymine I Uracil II Thymine II

P0 [bar]

Tr [K]

Tn [K]

Tw [K]

1.5 1.5 0.8 0.8 1.5 1.5

463 468 458 458 458 458

463 473 463 468 463 468

301 301 301 301

The electron-energy scale is calibrated using the 2.2 eV band in the O− ion yield from N2 O. The energy spread of the electron beam is approximately 600 meV. Test experiments with SF6 revealed that below 1.3 eV the electron current passing the interaction region with target gas quickly drops, and the current recorded in the Faraday cup does not correspond to the actual current in the interaction region. This is caused by the construction of the electron gun which was optimized for operation at energies of several tens of electronvolts. The present ions yields are thus reliable at energies above 1.3 eV. Composition of the beam Both positive and negative ionization can induce fragmen10


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tation of the weakly bound species, the unambiguous determination of the beam composition is thus not possible using mass spectrometric techniques. However, two observations can be immediately made from the negative ion mass spectra of the hydrated beams (figure 1): (i) no U or T dimer anions (neither pure nor hydrated) are observed and (ii) the hydration conditions I clearly result in much smaller NB(H2 O)− n anions than the hydration conditions II. The observation (i) shows that the partial pressures are set such that the adiabatic cooling in the expansion leads largely to the nucleobase-water clustering. The cooling (resulting from the collisions with helium in the expanding gas flow) is of course more efficient if the higher stagnation pressure is used. Hence larger nucleobase-water complexes are produced at conditions II, still without evidence for the formation of pure nucleobase clusters. The production of the smallest anions NB(H2 O)− n , n = 0, 1, 2 at conditions I suggests that the number of water molecules around the nucleobase is in the order of units, just from the energetical reasons. Taking the electron-complex collision energy of 1.5 eV and adiabatic electron affinity of hydrated anions 0.5 eV, 12 gives 2 eV that is available for evaporation of water monomers in the course of electron attachment. If the binding energy of one water molecule to the complex is 0.3 eV, 41 the excess energy is sufficient to evaporate six H2 O molecules. However, the number of evaporated molecules will certainly be lower, since considerable amount of the excess energy will be carried away as the kinetic energy of evaporating units. The target beam is thus indeed composed of individual microhydrated nucleobase molecules.

Acknowledgement This work has been supported by the Czech Science Foundation grant No. 16-10995Y.

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