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Clustering of Uracil Molecules on Ice Nanoparticles Andriy Pysanenko, Jaroslav Kocisek, Dana Nachtigallova, Viktoriya Poterya, and Michal Farnik J. Phys. Chem. A, Just Accepted Manuscript • DOI: 10.1021/acs.jpca.6b12594 • Publication Date (Web): 18 Jan 2017 Downloaded from http://pubs.acs.org on January 23, 2017

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The Journal of Physical Chemistry

Clustering of Uracil Molecules on Ice Nanoparticles Andriy Pysanenko,† Jaroslav Koˇcišek,† Dana Nachtigallová,∗,‡ Viktoriya Poterya,† and Michal Fárník∗,† J. Heyrovský Institute of Physical Chemistry, The Czech Academy of Sciences, Dolejškova 3, 182 23 Prague, Czech Republic, and Institute of Organic Chemistry and Biochemistry v.v.i., The Czech Academy of Sciences, Flemingovo nám. 2, 160610 Prague 6, Czech Republic E-mail: [email protected]; [email protected]

Phone: +420 2 6605 3206. Fax: +420 2 8658 2307

∗

To whom correspondence should be addressed J. Heyrovský Institute of Physical Chemistry ‡ Institute of Organic Chemistry and Biochemistry †

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Abstract ¯ ≈ 130 - 220, which We generate a molecular beam of ice nanoparticles (H2 O)N , N pick up several individual gas phase uracil (U) or 5-bromouracil (BrU) molecules. The mass spectra of the doped nanoparticles prove that the uracil and bromouracil molecules coagulate to clusters on the ice nanoparticles. Calculations of U and BrU monomers and dimers on the ice nanoparticles provide theoretical support for the cluster formation. The (U)m H+ and (BrU)m H+ intensity dependencies on m extracted from the mass spectra suggest a smaller tendency of BrU to coagulate compared to U, which is substantiated by a lower mobility of bromouracil on the ice surface. The hydrated Um ·(H2 O)n H+ series are also reported and discussed. Based on comparison with the previous experiments, we suggest that the observed propensity for aggregation on ice nanoparticles is a more general trend for biomolecules forming strong hydrogen bonds. This, together with their mobility, leads to their coagulation on ice nanoparticles which is an important aspect for astrochemistry.

Introduction In the search for origins of life in the universe, propositions were made that biomolecules were synthesized in the space and delivered to the early earth by meteorites or comets. 1,2 Among others, the ice grains and ice mantles in the interstellar space were proposed as the possible interstellar laboratories for biomolecule synthesis. 3–8 To investigate such prospects in laboratory conditions the coagulation and reactivity of molecules on clusters can be studied. 9,10 Large water clusters composed of hundreds of water molecules (ice nanoparticles) represent model systems where a detailed molecular-level understanding of such processes can be achieved. One way to approach this task is to generate molecular beams of ice nanoparticles in vacuum which are subsequently doped by precursor molecules by a pickup technique. 11–16 The experiments with the doped nanoparticles address the questions such as: Are the individually picked up molecules mobile on the nanoparticles or stay put where they 2 ACS Paragon Plus Environment

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landed? Do they coagulate to clusters on the nanoparticles? How do they react upon the nanoparticle excitation with energetic photons or electrons? We have recently investigated these questions for a series of atmospherically relevant chlorine-containing molecules on argon and ice nanoparticles. 10 All the studied molecules coagulated to relatively large clusters on argon nanoparticles, but surprisingly, no evidence for any clusters generated on ice nanoparticles was observed. The same behavior – i.e., coagulation on argon and non-coagulation on ice nanoparticles – was observed in our photodissociation studies 9,17,18 for some other molecules as well. Only very recently, we have observed clustering of molecules on the ice nanoparticles for hydroxypyridine, where dimers and even larger clusters composed of up to about 10 molecules were generated. 19 It ought to be mentioned that the clustering of biomolecules in water cluster was demonstrated previously in experiments where, rather than the pickup, the co-expansion of biomolecules with the water vapor was used. 20–22 It has been demonstrated, that in the co-expansion experiments the composition of clusters and number of incorporated biomolecules can be controlled by expansion conditions in supersonic expansions. 23 The microhydration of single uracil and thymine molecules with only a few water molecules has also recently been reported 24 in an electron attachment experiment. However, here we use a different approach, where the biomolecules are deposited one-by-one on the surface of ice nanoparticles. ¯ between 130 and 220 In the present experiment, large water clusters (H2 O)N with N molecules are generated and undergo multiple pickup collisions with uracil (U) or 5-bromouracil (BrU) molecules in a pickup cell. Subsequently we probe the clusters by 70 eV electrons and record the mass spectra of the positively charged ions. We complement our experiments by theoretical calculations of U and BrU monomers and dimers on ice nanoparticles and in small water clusters. The present observations combined with the previous results, 9,10,19 provide an evidence that biomolecules and their analogues which can generate strong hydrogen bonds with each other tend to form aggregates on cold ice nanoparticles. However, the mobility of the molecules on the surface can influence the aggregation. The aggregation of molecules on



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the ice nanoparticles is the necessary condition for the generation of larger biomolecules on the icy grains, e.g., in astrobiology.

Experimental and theoretical methods Experiment This study was performed on CLuster Beam (CLUB) apparatus, which is a complex experiment dedicated to photochemistry, 18,25 mass spectrometry, 26,27 and pickup 14,16 studies of clusters in molecular beams. Detailed descriptions of the apparatus is given in the mentioned publications. In the present experiments, the setup was used in a similar way as in our recent study of hydroxypyridine pickup and coagulation on ice nanoparticles. 19 The ice nanoparticles were generated in a continuous supersonic expansion of water vapor into the vacuum through a conical nozzle. Different expansion conditions were exploited. Resistively heated water reservoir inside the vacuum chamber was kept at constant temperatures between TR = 393 K and 403 K, and the nozzle was heated to somewhat higher temperature T0 = 413 K. The mean particle size corresponding to these expansion conditions ¯ = 130 − 220. could be calculated using a modified Hagena’s formula 27,28 as N The molecular beam emerging from the nozzle was skimmed and after passing a differentially pumped vacuum chamber it entered a chamber equipped with a home built pickup oven containing uracil (Sigma Aldrich, ≥99%) or 5-bromouracil (Sigma Aldrich, 98%) samples. The oven was heated resistively to a temperature TP , which was varied between 473 K and 518 K for uracil, and between 493 K and 518 K for bromouracil. Then the molecular beam entered an UHV chamber hosting Reflectron Time of Flight mass spectrometer (RTOF) mounted perpendicularly to the beam. For the electron ionization, we used a pulsed electron gun with frequency of 10 kHz and 70 eV electrons. The ionized species were extracted by a 10 kV pulse and accelerated to the kinetic energy of 8 kV, and passed the effective flight path of 0.95 m. The mass spectra were recorded with a typical 4 ACS Paragon Plus Environment

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resolution of M/∆M ∼ 2 × 103 .

Calculations The calculations were performed on dimers of uracil and bromouracil, on clusters of uracil and bromouracil with n = 4 to 7 water molecules (Br)U·(H2 O)n , and on uracil and bromouracil monomers and dimers on ice nanoparticle surfaces. The ice was modeled using 47-48 water molecules. The procedure to model the ice surface was described elsewhere. 29 The structures were optimized at the DFT level using B97D functional 30 and TZVP 31 basis set. The character of interactions of uracil monomers with the ice surface was analyzed in terms of strengths of hydrogen bonds between uracil and water molecules and interactions of π-electrons with dangling hydrogens of the ice surface. The relevant interaction energies with respect to their optimized monomer species were calculated at the same level and corrected for basis set superposition error (BSSE). Stability of the protonated dimers (U)2 H+ and (BrU)2 H+ ions were calculated at the MP2 level with spin-component scaling approach (SCS-MP2) 32 using aug-cc-pVDZ basis. 33 The same method was used to describe the dissociation of the dimer ion (U)2 H+ →UH+ +U (and analogically for BrU). The DFT and MP2 calculations were performed using Gaussian 09 34 and Turbomole 35 program packages, respectively.

Results Mass spectra ¯ = 170 which picked The mass spectrum of the water clusters (H2 O)N with the mean size N up several individual uracil molecules while passing through the pickup cell containing uracil powder heated to the temperature TP = 518 K are shown in Fig. 1. The main series in the spectrum corresponds to the protonated water clusters (H2 O)n H+ , and there is also a strong uracil monomer U+ peak. Further relatively strong series could be identified in 5 ACS Paragon Plus Environment


the spectrum (labeled by symbols) corresponding to the protonated and hydrated uracil molecules and clusters Um ·(H2 O)n H+ with m = 1 − 4 (weak m = 5 and 6 series, not shown in Fig. 1, were also identified in the spectrum). Similar spectra were obtained at different pickup pressures and water reservoir temperatures and some of them are displayed in the accompanied Supporting Information (SI) in Fig. SI2 (and SI3 for BrU). Rel. Abundance (arb. units)

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¯ = 170. The pickup Figure 1: Mass spectra of uracil picked up on water clusters (H2 O)N , N cell temperature was TP = 518 K. The uracil containing series of peaks Um ·(H2 O)n H+ for m = 1 − 4 are labeled by different symbols; the non-labeled peaks correspond to the protonated water clusters (H2 O)n H+ . The same experiments were performed with bromouracil. The mass spectra were essentially the same only more congested due to the isotopic contribution of 79 Br and 81 Br. These spectra seem to exhibit somewhat smaller tendency to BrU coagulation on the (H2 O)N ice nanoparticles. To quantify this effect, we compare the integrated intensities of protonated uracil (U)m H+ and bromouracil (BrU)m H+ mass peaks in Fig. 2 (for BrU both isotopic contributions were integrated). Both spectra were normalized on the maximum water cluster peak at m/e = 181, (H2 O)n H+ n = 10. In both cases the protonated water clusters (H2 O)n H+ series showed essentially the same distributions suggesting that the neutral ice nanoparticles were the same. The spectra normalization was not necessary for the discussion below, which is based on the difference between the slopes of the (U)m H+ and (BrU)m H+ dependencies on m. We show the normalized intensities in Fig. 2 to bypass the day-to-day 6 ACS Paragon Plus Environment

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fluctuations in signal and beam intensities and other experimental settings. The original spectra are shown in SI as Figs. SI2 and SI3. The pickup cell temperature was identical for uracil and bromouracil TP = 513 K. In Fig. 2, we plot also the unprotonated cluster peak intensities U+ and BrU+ (arbitrarily at the position m = 0). The intensities of the unprotonated peaks reflects the amount of uracil and bromouracil evaporated in the pickup cell. To our best knowledge, the information about the ionization cross sections for BrU molecules relative to U is not available. If these cross sections were comparable, similar U+ and BrU+ intensities in Fig. 2 would suggest similar amount of uracil and bromouracil molecules in the pickup cell in these experiments. Integral Intensity (arb. units)

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Figure 2: Comparison of protonated uracil (U)m H+ and bromouracil (BrU)m H+ cluster peak intensities. The intensities of unprotonated U+ and BrU+ monomers are plotted arbitrarily at m = 0 (see the text for details). Finally, we extract the integrated mass peak intensities for the above mentioned (U)m ·(H2 O)n H+ series and plot them as a function of the number n of the hydrating water molecules. Fig. 3 shows these dependencies for m = 1 − 4 series. The intensities of the strongest non-hydrated ions (U)m H+ are omitted from these plots, their intensities can be seen in the mass spectrum in Fig. 1. The pure protonated water (H2 O)n H+ series is also indicated by opened circles for comparison. All these dependencies exhibit some intensity maxima which will be further discussed below.


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Figure 3: Integrated mass peak intensity dependencies of the (U)m ·(H2 O)n H+ series on n for m = 1 − 4 series. The pure protonated water (H2 O)n H+ series scaled by a factor of 0.03 is also indicated by opened circles for comparison.

Structures and energetics Uracil: Using microwave 36 and infrared laser spectroscopy 37 only the keto-form of uracil was observed in the U·H2 O complex. Several computational studies of small U·(H2 O)n complexes 38–44 have reported on the character of these clusters up to the formation of the first hydration shell around uracil. The relative stabilities of keto and enol forms in the water environment have been studied as well. 45,46 The dissociation energies of water molecule bound to N1 and O2, O2 and N3, and N3 and O4 atoms (for numbering see Fig. 4) were estimated in the range of 7 - 9 kcal/mol. 39 At the ice surface uracil monomer can form up to six hydrogen bonds with water molecules. To obtain the interaction energies of water molecules with all binding sites (oxygen and nitrogen atoms) the calculations were performed on the U·(H2 O)6 cluster. In the agreement with previously reported studies 45,46 the keto-form of uracil was found to be more stable than the enol-form. The calculated strengths with each binding site of uracil (see Fig. 4) are given in Table 1. The interaction of uracil monomer with water clusters using 50 water molecules has been already studied 46 to discuss the possibility of keto-enol tautomerization. It has been suggested that the keto-form is preferred in the water environment. Therefore, only ketoform of uracil has been considered in our calculations. As already stated, 43 the character


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of the interaction of uracil with water results from the competition between the interactions within the water (ice) cluster and the uracil-water(ice) interactions. In addition, uracil can possess several local minima on the ice surface due to the random structure of water molecules at the ice surface. To account for this, different possible arrangements of uracil on the ice surface were considered in our study. Two representative examples of binding of U monomer on the ice surface, U-ice1 and U-ice2, directly interacting with four and six water molecules, respectively, are shown in Fig. 4. The interaction energies with each separate binding sites are compared to the total binding energies in table 1. Relatively rigid character of the ice surface prevents the water molecules to reach the optimal orientation with respect to the uracil. As a result, the orientation does not always allow the hydrogen bond formation to all possible binding sites of the uracil, and the interaction energies are smaller compared to those found in U·(H2 O)6 cluster optimization. A semiquantitative estimate of the strength of the interaction of uracil with ice surface can be obtained from interaction energies calculated for the U with H2 O molecules directly bound to the base (Einter -cluster, table 1). These results show the large differences in the complex stability for different arrangements. Note that water molecules which would contribute with interaction of H-dangling bonds with uracil aromatic ring were not obtained during the structure optimization.

A

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Figure 4: Optimized structures of U·(H2 O)6 clusters (A) and uracil monomer on ice clusters: (B) U-ice1 and (C) U-ice2. The red, blue, grey and white colors stand for oxygen, nitrogen, carbon and hydrogen, respectively. Examples of the possible arrangements of uracil dimers on the ice surface are illustrated 9 ACS Paragon Plus Environment


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Table 1: The interaction energies Einter (kcal/mol)a of uracil and bromouracil with water molecules in U·(H2 O)6 and BrU·(H2 O)7 and in (Br)U-ice complexesb . Einter -(binding site)c Binding site N1 O2 N3 O4 Br5 Einter -cluster U·(H2 O)6 -5.20 -8.53 -3.81 -10.25 BrU·(H2 O)7 -6.40 -8.51 -5.24 -7.91 0.80 U-ice1 (4) 0.75d -4.65 -5.83e -8.26 e e U-ice2 (6) -4.23 -2.57 -3.43 -5.57 -24.10 BrU-ice1 (4) -7.13 -0.9d -5.28 -1.78d -18.96 e e BrU-ice2 (6) -4.87 -5.41 -3.48 -4.47 -27.01 a b corrected for BSSE; number of H2 O molecules in the cluster is given in parenthesis; c calculated for clusters with H2 O molecules directly interacting with (Br)U; d one H2 O binds to the site; e two H2 O bind to the site. in Fig. 5 and in SI (Fig. SI4). The mutual orientations of the two uracil monomers include stacked and hydrogen bonded structures. According to Hunter and Mourik 47 the stacking conformation of uracil dimer is stabilized by about 9 kcal/mol. Larger interaction energies, up to 16 kcal/mol were found for hydrogen bonding complexes. 48,49 The character of the interaction between the uracil dimers and ice surface water molecules found in the current study are reported in table 2. Considering the H2 O molecules which are directly interacting with the uracil dimer, the resulting stabilization energies are in the range of 24 - 43 kcal/mol. In addition to these interactions, also the binding between the two monomers contributes to the stabilization of the dimers on the ice surface. The gas phase interaction energies between the two uracil monomers calculated at the mutual orientation found on the ice cluster are smaller than those found in the gas phase optimization 47–49 due to the constraints caused by the ice cluster. As expected, the resulting hydrogen-bonding and stacked interactions are further decreased in the water(ice) environment. Still, they significantly contribute to the final stability of the uracil dimer on ice. Our calculations show that both uracil monomer and dimers can bind to the ice surface with a large variety of binding energies. Among the calculated structures, there are arrangements for which binding of the dimer is preferred over the binding of two independent monomers. Bromo-Uracil: The strengths of interaction of H2 O molecules with binding sites of BrU 10 ACS Paragon Plus Environment

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Figure 5: Optimized structures of (U)2 dimer on ice structures: (A) (U)2 -ice1, (B) (U)2 -ice2. obtained by the optimization of the BrU·(H2 O)7 cluster and two possible BrU monomer arrangements optimized on the ice surface are reported in Fig. 6 and Table 1. In the BrU·(H2 O)7 the interaction with H2 O molecule with Br5 binding site was also considered. The interaction energies agree within 1.5 kcal/mol with those found in the U·(H2 O)6 . The only exception appears for binding to O4 site which is probably caused by a less stable arrangement due to the presence of H2 O molecule binding to Br5. As suggested by Danilov et al. 46 in the water environment the enol-form of BrU is preferred over the keto-form. This is in contrary to results of Orozco et al. 50 To account for the possibility of the keto-enol tautomerization the enol form of BrU on the ice surface was considered. In all these calculations the stability of keto-form is larger than that of enol-form (with the differences of total energies in the rangel of 10 - 17 kcal/mol). Therefore, only keto-form is discussed below. The results obtained for the BrU· · · H2 O interactions give similar picture as for uracil, in particular smaller BrU· · · H2 O interaction energies on ice compared to BrU·(H2 O)7 cluster due to the restricted motion of water molecules in the ice structure. The results obtained for the clusters of BrU monomer and H2 O molecules in direct bonding show somewhat larger



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Table 2: The interaction energies Einter (kcal/mol)a of uracil dimer in (U)2 -ice complexes. nb

Einter (U·(H2 O))c

Einter (U·U) Einter (sum)f d e cluster gas phase (U)2 -ice1 6 -24.02 -11.13 -14.88 -35.16 (U)2 -ice2 7 -29.21 -5.26 -8.68 -34.47 (U)2 -ice3 6 -29.16 -1.42 -5.88 -30.58 (U)2 -ice4 6 -33.46 1.13 -3.32 -32.33 (U)2 -ice5 6 -42.59 -0.89 -5.90 -43.48 (U)2 -ice6 7 -30.81 -7.11 -12.38 -37.92 a b c corrected for BSSE; number of H2 O molecules in the interaction; interaction energy with H2 O directly bound to U2 ; d calculated from the ice cluster; e calculated at the geometry from the ice cluster; f sum of the interaction energies with directly interacting H2 O and interaction within the dimer. interaction energies compared to U-ice, namely the BrU-ice1 with four H2 O molecules present in the cluster (see table 1). Regardless of the starting structure the water molecules always arranged to interact via hydrogen bonds with nitrogen and oxygen atoms. Binding to Br atom was obtained when the cluster was enlarged by additional water molecules. In such case the interaction energy of H2 O with Br binding site was about -0.5 kcal/mol resulting, however, in smaller interaction energies between H2 O and N or O atoms.

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Figure 6: Optimized structures of BrU·(H2 O)7 clusters (A) and bromouracil monomer on ice clusters: (B) BrU-ice1 and (C) BrU-ice2. The red, blue, grey, black and white colors stand for oxygen, nitrogen, carbon, bromine and hydrogen, respectively. To allow for the investigation of the effect of Br substitution on the character of interactions the optimization of (BrU)2 dimer associates started from the same initial structures as those of U2 dimers. Additionally, clusters with Br directly interacting with the ice surface 12 ACS Paragon Plus Environment

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were also considered. Such optimizations, however, resulted in the formation of less stable structures. The examples of optimized structures are shown in Fig. 7. As in the case of uracil dimer, the strengths of binding energies of bromouracil with water molecules of the ice surface are similar to those calculated for monomers and contribute to the dimer stabilization with the binding energies in the range of 18 - 45 kcal/mol, Table 3. Additional interactions between the two monomers can be as strong as 11 kcal/mol, in particular in the hydrogen-bonded structures. Although the interaction energies calculated for the gas phase stacked BrU dimer accounts for about 10 kcal/mol, 51 in our optimization procedure performed on the ice surface the two BrU monomers tend to adopt slightly displaced structures. The calculations provide similar picture as for uracil, in particular, variety of binding motives to the ice cluster resulting in a large range of binding energies. The calculations suggest somewhat stronger binding of the BrU monomer to the ice surface compared to U, assuming that the optimization of BrU monomer on the ice started from the same initial orientation as that of U. Again, arrangements can be found where the formation of dimers on the ice surface is energetically preferred over the binding of two separate monomers.

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Figure 7: Optimized structures of (BrU)2 dimer on ice structures: (A) (BrU)2 -ice(1), (B) (BrU)2 -ice(2). Color coding as in Fig. 6



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Table 3: The interaction energies Einter (kcal/mol)a of bromouracil dimer in (BrU)2 -ice complexes. nb

Einter (BrU·(H2 O)c

Einter (BrU·BrU) Einter (sum)f d e cluster gas phase (BrU)2 -ice1 6 -18.37 -10.82 -14.61 -29.19 (BrU)2 -ice2 10 -44.91 0.90 -4.47 -44.01 (BrU)2 -ice3 6 -38.45 -6.72 -9.27 -45.17 (BrU)2 -ice4 4 -18.32 -0.65 -6.12 -19.07 (BrU)2 -ice5 8 -30.47 -6.73 -11.71 -37.19 a b c corrected for BSSE; number of H2 O molecules in the interaction; interaction energy with H2 O directly bound to BrU2 ; d calculated from the ice cluster; e calculated at the geometry from the ice cluster; f sum of the interaction energies with directly interacting H2 O and interaction within the dimer.

Discussion Coagulation of uracil on ice nanoparticles The presence of the mass peaks corresponding to uracil clusters Um H+ with m ≥ 2 (and their hydrated series Um ·(H2 O)n H+ ) in the mass spectra points to the coagulation of the neutral uracil molecules to clusters on the ice nanoparticle surface. The possibility that the uracil molecules would penetrate deep into the ice nanoparticle and coagulate inside is a less likely scenario in the view of relatively rigid ice nanoparticle surface and the uracil molecule size. The time scale available for the cluster formation corresponds to the flight time of the ice nanoparticles from the pickup cell, where the molecules were deposited on the ice, to the RTOF ionizer, which was about 0.7 ms. Until quite recently, there was no experimental evidence for molecules clustering on isolated ice nanoparticles in molecular beams. We have demonstrated non-clustering for quite a few molecules on free ice nanoparticles. 9,10 The first molecule which has recently been shown to coagulate on ice nanoparticles was hydroxypyridine. 19 Hydroxypyridine forms hydrogen bonded (dimer) clusters related to the base-pairing in RNA and DNA. The present case, uracil, as the nucleobase in the nucleic acid of RNA, also forms strong hydrogen doublebonds. We propose that the tendency to clustering on ice nanoparticles may be a common


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feature of the biomolecules generating strong hydrogen bonds between each other, partly overwhelming the hydrogen bonds to the water molecules in ice. Our theoretical calculations show that for both U and BrU among all the investigated structures many arrangements exist where the formation of their dimer associates is energetically more favorable than the binding of two isolated monomers. The experiment confirms that such arrangements, in which the dimers (and even larger clusters) are generated, are clearly present on the ice nanoparticles.

Comparison of uracil and bromouracil on ice nanoparticles Our second point concerns the comparison between uracil and bromouracil, which was summarized in Fig. 2. It showed that the cluster abundance for bromouracil (BrU)m H+ decreases faster than for uracil (U)m H+ with the increasing cluster size m. Although the difference in the slopes in these dependencies is not large, it exceeds the experimental error bars. Possible reasons for the different slopes can be either that the bromouracil tends to coagulate to clusters on ice nanoparticles less than uracil, or that the bromouracil clusters on the ice nanoparticles fragment more efficiently upon the ionization than the uracil ones. A smaller tendency to coagulate on ice nanoparticles for bromouracil compared to uracil could lead to the smaller BrU clusters. There is essentially very little difference between uracil and bromouracil for the generation of dimers in terms of energetics (see Tabs. 2 and 3). Although, the reported structures do not cover all possible arrangements of dimer associates which can be found on the ice surface, they clearly show the trends. However, the coagulation of the molecules depends also on their mobility on the ice surface. Assuming, that the interaction energies of U and BrU with H2 O molecules directly bound to the base species provide a semiquantitative picture, the binding of the bromouracil monomer is slightly stronger than the uracil one. The slightly stronger binding of BrU to the ice suggests a lower mobility of BrU. Besides, BrU molecules are almost twice as heavy as U which can also contribute to their lower mobility, and thus to their lower tendency to coagulate. 15 ACS Paragon Plus Environment


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In principle, a more efficient fragmentation of bromouracil clusters upon ionization could also justify the observed smaller bromouracil clusters fragments. Therefore we analyze this possibility as well. However, it should be noted that any significant fragmentation is not expected for any of the species. The much larger size of the ice nanoparticles compared to the uracil or bromouracil clusters suggests much higher probability of ionizing a water molecule first and producing the final ion (U)m H+ or (BrU)m H+ fragment via a proton transfer process, rather than a direct ionization of the embedded cluster. The protonated fragments support this scenario, as well as the prevailing contribution of pure protonated water peaks (H2 O)n H+ in all the spectra, see Fig. 1. The proton transfer is a gentle process compared to the direct electron ionization. Besides, the ice nanoparticles serve as an efficient heat bath absorbing the excess energy. Moro et al. 12,13 reported almost negligible fragmentation of aminoacids after they were picked up on water clusters, in contrast to their rich fragmentation in the gas phase. Also a recent investigation of uracil fragmentation in clusters induced by collisions with highly energetic ions demonstrated the protective effects of the surrounding uracil and water clusters. 52 In addition, the protective role of even single water molecule attached to the uracil was also shown in multiphoton ionization. 53 Considering all these arguments, the fragmentation of the embedded cluster is probably not extensive, neither for uracil nor for bromouracil. Consequently we do not expect a large difference in the fragmentation pattern between the two types of clusters. Nevertheless, in order to substantiate this qualitative argument further quantitatively, we have performed calculations in which the protonated dimers were dissociated to protonated and neutral monomer (U)2 H+ → UH+ +U (and analogically for BrU). In these calculations the fragmentation was investigated for the dimer structure localized on the ice surface. The details of calculations are given in SI. The results show very similar behavior of uracil and bromouracil protonated dimers with respect to fragmentation to protonated and neutral monomers. The stabilization energies are in the range of 22 - 30 kcal/mol and 21 - 27 kcal/mol for (U)2 H+ and (BrU)2 H+ , respectively.


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Therefore the experimentally observed smaller slope of (U)m H+ fragment intensity in dependence on m, compared to the slope of (BrU)m H+ dependence, points to a larger tendency of uracil molecules to clusters on the ice nanoparticle surface, which in turn can be explained by their higher mobility. Further investigations of uracil and bromouracil mobility on bulk ice surfaces can support this conclusion.

Ionization of uracil clusters on ice nanoparticles Another interesting experimental observation is the ionization pattern of uracil on ice presented in Fig. 3. The ionization of uracil clusters on ice nanoparticles leads to the series of hydrated Um ·(H2 O)n H+ fragment ions where peaks with m = 1 − 4 and n = 1 − 20 are observed. Interestingly, the series Um ·(H2 O)n H+ exhibit some pronounced intensity maxima, consistent for different m. The first one appears at n = 2 for hydrated uracil dimers to tetramers (m = 2 − 4). The second maximum for n = 4 is common for uracil monomer through trimer (m = 1 − 3). It should be noted that although there is no strong maximum for the tetramer U4 ·(H2 O)4 H+ , it could be obscured by the overall lower intensity of the tetramer mass peaks and consequently large error bars. A particularly strong maximum is at n = 9 for the hydrated monomer m = 1. It is interesting to compare these dependencies to the (H2 O)n H+ fragment ions depicted in Fig. 3. The maxima at n = 4 are consistent with the (H2 O)4 H+ maximum. Also, at least the U·(H2 O)n H+ dependence roughly follows the water clusters (H2 O)n H+ . This may suggest that the ice nanoparticle is ionized and the protonated water fragment (H2 O)n H+ leaves the particle in some cases accompanied by the uracil molecule. The maximum appears for (H2 O)10 H+ and U·(H2 O)9 H+ fragment -i.e. one water molecule replaced by the uracil molecule. It should be noted that the neutral species ionized here are the ice nanoparticles with about 170 water molecules and a few uracil molecules coagulated to clusters on the ice. Therefore the maximum in the ion fragment intensity cannot reflect some special stability 17 ACS Paragon Plus Environment


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of the neutral precursors but rather express a favorable geometry and stability of the corresponding cluster ion. From the comparison with the water clusters it seems that it is the stability of the protonated water clusters, which is reflected in the spectra, rather than a special stability of the mixed species; e.g. the abundant protonated tetramer (H2 O)4 H+ appears also accompanied by the uracil molecules Um ·(H2 O)4 H+ with higher probability. Theoretical studies of the mixed Um ·(H2 O)n H+ clusters could provide further insight into the present dependencies. However, our preliminary theoretical investigations showed, that there are numerous cluster structures possible and their detailed investigation goes beyond this study. For BrU the mass spectra are more congested due to the presence of two almost equally populated Br isotopes (see Fig. SI3). Therefore similar dependencies for BrU could not be reliably extracted from the spectra.

Conclusion ¯ ≈ 130 - 220, picked up several individual A molecular beam of ice nanoparticles (H2 O)N , N gas phase uracil or 5-bromouracil molecules, and the mass spectra of the nanoparticles with the embedded molecules were measured. Complementary theoretical calculations help to elucidate the experimental observations. Several conclusions could be drawn: • We observe coagulation of the individual uracil and bromouracil molecules to clusters on the ice nanoparticles. Clusters with more than 6 molecules in the case of uracil, or 4 molecules for the bromouracil, were detected. • Our theoretical calculations substantiate the uracil and bromouracil coagulation on the ice nanoparticles from energetic point of view. They show structural arrangements, where the dimers are energetically favored over the two isolated monomers, and the experiment proves that the generation of the clusters on ice nanoparticles actually occurs. 18 ACS Paragon Plus Environment

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• The bromouracil shows a lower tendency to clustering on the ice nanoparticles compared to uracil. The theory suggests somewhat higher binding of individual bromouracil molecules to the ice compared to uracil molecules, which together with the higher BrU mass can lead to their lower mobility. • Series of protonated Um ·(H2 O)n H+ fragment ions as a function of n are presented. They reflect at least partly the abundance of the pure protonated water clusters (H2 O)n H+ generated after the nanoparticle ionization. The major contribution of the present investigation is the observation of uracil and bromouracil cluster coagulation on the ice nanoparticles within approximately 0.7 ms after their pickup. So far three molecules – hydroxypyridine, uracil and bromouracil – were found to coagulate to clusters on the free ice nanoparticle, while a number of other molecules was demonstrated not to coagulate. 9,10 We suggest that the tendency to coagulation stems from the interplay of the interactions between the adsorbed molecules and the interactions of the adsorbed molecules to the ice surface, and in their mobility on ice. The molecules, which were shown to coagulate on ice, exhibited strong hydrogen bonds with each other, overwhelming the hydrogen bonds of water to these molecules. Such molecules in general may coagulate on ice nanoparticles. These molecules are biologically relevant, and therefore our findings are important for astrobiology, where the synthesis of biological molecules on ice particles was proposed. 3,4

Acknowledgement This work was supported by the Czech Science Foundation under grant no. 14-14082S.

Supporting Information Available Additional mass spectra and calculation results: dimer structures on ice, and protonated dimer ion structures and energetics. 19 ACS Paragon Plus Environment


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This material is available free of charge via the Internet at http://pubs.acs.org/.

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