Size-Induced Segregation in the Stepwise Microhydration of

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Size-Induced Segregation in the Stepwise Microhydration of Hydantoin and Its Role on Proton-Induced Charge Transfer Florent Calvo, and Marie-Christine Bacchus-Montabonel J. Phys. Chem. A, Just Accepted Manuscript • DOI: 10.1021/acs.jpca.7b10291 • Publication Date (Web): 12 Jan 2018 Downloaded from http://pubs.acs.org on January 12, 2018

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The Journal of Physical Chemistry

Size-Induced Segregation in the Stepwise Microhydration of Hydantoin and its Role on Proton-Induced Charge Transfer F. Calvo∗,† and M.-C. Bacchus-Montabonel‡ †LiPhy, Université Grenoble 1 and CNRS UMR 5588, 140 Avenue de la Physique, 38402 St Martin d’Hères, France ‡Univ Lyon, Université Claude Bernard Lyon I, CNRS, Institut Lumière Matière, 69622, Villeurbanne, France E-mail: [email protected]

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The Journal of Physical Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Abstract Recent photochemistry experiments provided evidence for the formation of hydantoin by irradiation of interstellar ice analogues. The significance of these results and the importance of hydantoin in prebiotic chemistry and polypeptide synthesis motivate the present theoretical investigation, in which we analyzed the effects of stepwise hydration on the structures, electronic and thermodynamical properties of microhydrated hydantoin using a variety of computational approaches. We generally find microhydration to proceed around the hydantoin heterocycle until 5 water molecules are reached, at which stage hydration becomes segregated with a water cluster forming aside the heterocycle. The reactivity of microhydrated hydantoin caused by an impinging proton was evaluated through charge transfer collision cross sections, for microhydrated compounds but also for hydantoin on icy grains modeled using a cluster approach mimicking the true hexagonal ice surface. The effects of hydration on charge transfer efficiency are mostly significant when few water molecules are present, and progressively weaken and stabilize in larger clusters. On the ice substrate, charge transfer essentially contributes to a global increase in the cross sections.

1 Introduction Prebiotic chemistry aims to understand how complex biological molecules could be formed from much simpler building blocks under the harsh environments of primitive Earth or the extreme density and temperature conditions of extra-terrestrial objects such as comets or meteorites. An increasing range of prebiotic molecules has now been conclusively identified in astrophysical media, notably leading to amino acids 1–3 as well as compounds relevant in RNA chemistry such as uracil itself 4 or 2-aminooxazole. 5,6 Photochemistry in the presence of ’dirty’ ice substrates was shown to be a major cause for synthetizing these compounds, through the reaction of elementary molecules such as urea and water. 7–10 Besides photochemical processes, reactions on prebiotic molecules can be triggered by particle irradiation through electron or ion impact, especially protons which are particularly abundant in 2


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Space. 7,11,12 Depending on collision energy, impinging protons may excite the biomolecular target or even ionize it, both processes being followed by a major energy redistribution and possibly fragmentation. Ionization is especially dramatic if the target is not a single molecule but lies in the vicinity of a substrate (or a solvent) it can react with. 13 The importance of the icy substrate for the formation of prebiotic compounds has been notably established in laboratory experiments in which 2,4-imidazolidinedione (hydantoin) could be produced in significant amounts under conditions expected to be similar to those found in some carbonaceous meteorites. 8,14 Hydantoin is an intermediate in cyanide acid chemistry, 15 which in itself is already of fundamental importance in prebiotic chemistry. 16,17 It has been detected first in primitive carbonaceous meteorites and new reaction sequences for its formation have been explored recently 18 as well as its alteration through photochemical reactions. 19 Hydantoin is also involved in the formation of polypeptides, 20 making this molecule of particular interest in the context of astrochemistry. To better unravel the role of the water medium on the physical and chemical properties of biological species, one natural approach consists of building the ice environment one water molecule at a time and consider so-called microhydrated compounds. This approach is useful to shed light onto the mechanisms by which the solute is affected by the solvent and even possibly transforms itself. 21,22 Even in the absence of chemical reactions altering the solute, stepwise hydration can reveal changes in the magnitude of bonding in the competition between solute-solvent and intrasolvent interactions. For instance, spontaneous reactions involving electron transfer induced by hydration have been identified in the dissociation and ionization of NaCl 23 and in the emergence of the zwitterionic form of polypeptides. 24,25 In the present contribution, we investigate the microhydration of hydantoin in the gas phase from its very most fundamental aspects of structure at zero and finite temperatures, to its behavior toward proton impact and the possibility of ionizing it. An earlier study by one of us 26 has shown that charge transfer (CT) upon proton impact on bare hydantoin is highly anisotropic and has a marked dependence on collision energy. Similar conclusions were reached for uracil and

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2-aminooxazole, but for these molecules another range of variations was obtained by placing them under microhydration environment. 27,28 In particular, we found a significant sensitivity to the arrangement of the solvent around the biomolecule, especially in the case of uracil which undergoes a structural transition between planar (ring-like) and segregated (cluster-like) hydration patterns. 27 Our theoretical investigation follows the same lines as our previous works, 27–29 and consists of combining different computational chemistry methods to locate the likely lowest-energy structures of hydantoin in contact with a limited number n = 1–10 of water molecules, to evaluate the thermal stability of these structures, and eventually to determine how the presence of the water microsolvent modifies the propensity for charge transfer upon proton impact. We generally find much similarities in microhydrated hydantoin with respect to uracil, 27 in which preferential hydration to the peripheral plane becomes disfavored once 5 water molecules are present, above which they segregate into a cluster on one side of the heterocycle. This structural transition, which was not found in 2-aminooxazole, 28 is also predicted to have relatively minor but steady influence on the proton-induced charge transfer cross sections. In addition, the global increase of charge transfer cross sections for hydrated hydantoin compounds would indicate a favored proton-induced ionization in presence of water. In the next section, we briefly describe the computational tools employed throughout this study. Section 3 presents and discusses our main results, before some concluding remarks are finally given in Sec. 4.

2 Methods 2.1

Exploration of energy landscapes

As in our earlier investigations 27,28 we use a combination of well-established computational methods to model microhydrated biomolecules, with (i) a force field exploration using extensive replicaexchange molecular dynamics (REMD) simulations combined with systematic quenching and (ii) systematic refinement of the lowest-energy structures at a more realistic level of theory, namely 4


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density-functional theory. The Amber ff99 force field 30 was chosen owing to its satisfactory performance against more refined approaches with an explicit account of electronic structure for related microhydrated compounds. 27–29 The partial charges on the atoms of hydantoin necessary to model electrostatic interactions were obtained at the equilibrium geometry using the standard RESP procedure, which is the standard method employed in the framework of the Amber force field. 30,31 Since different methods can produce different charges, 32 and in order to evaluate the robustness of the results, we have also considered natural bond orbital (NBO) charges, also extracted from the same DFT geometry. Both sets of charges are provided as Supplementary Material. Note that in both cases, water molecules are modeled using the TIP3P potential. Initial configurations for microhydrated hydantoin were generated by placing randomly desired numbers of water molecules around it, and performing replica-exchange MD simulations in the temperature range of 25–250 K, the ladder of temperatures having 32 rungs allocated in a geometric fashion. The number of water molecules was varied from n = 1 to 10 throughout this study, and for simplicity we denote the corresponding cluster by H(H2 O)n , with H refering to hydantoin. In order to prevent evaporation from occuring at high temperatures, the clusters were enclosed into a spherical container with a soft repulsive ˚ as the container radius. potential of the (r − r0 )4 form with r0 = 20 A In practice, each trajectory was thermostatted using the Nosé-Hoover method and propagated for 12 ns using the velocity Verlet algorithm 33 and a time step of 1 fs, averages being accumulated only after the first 2 ns. Electrostatic interactions were treated directly with a dielectric constant of unity and the usual screening for covalently bound atoms up to the fourth neighbors. Occasional exchanges between random pairs of trajectories were attempted every 10 ps. Configurations were saved on-the-fly every 1 ps during the REMD simulations and subject to systematic local optimization, the putative global minimum being identified from the pool of configurations. New REMD trajectories were then performed initiated from the global minimum, and quenches also carried out with the global minimum possibly improved. Such a procedure was ended once a REMD simulation no longer produced any lower-energy structure. In practice, up to 5 iterations were needed in

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the largest clusters case of n = 10 water molecules. The final iteration of REMD and systematic quenches were then deemed sufficiently ergodic to yield reliable, statistically converged data, among which the internal energy U (T ) and its temperature derivative or canonical heat capacity Cv (T ) = ∂U/∂T were primarily scrutinized. In addition to thermal properties we also considered basic geometric indicators such as the gyration radius of the distribution of water molecules around the hydantoin solute. The locally stable minima obtained by quenching the instantaneous configurations also provided information about the diversity of inherent structures {α} visited by the system as a function of temperature, which is directly connected to the fluxionality of the system in its energy landscape. More precisely, the inherent structures were enumerated according to their energy {Eα } and for each of them their occurence or probability pα was evaluated by direct counting. An inherent structure entropy SIS (T ) is then defined by similarity to the conventional information entropy as SIS (T ) = −kB

X

pα ln pα ,

(1)

α

with kB the Boltzmann constant. With this definition, a solidlike behavior associated with a single inherent structure would be such that SIS = 0, strictly positive values indicating a fluxional system.

2.2 Quantum chemical calculations For each system size, the 20 lowest energy structures obtained by quenching the REMD trajectories propagated with the Amber ff99 force field were refined using density-functional theory and the M06-2X double hybrid functional 34 shown earlier to be particularly successful for related compounds. 27,28 Using NBO charges for hydantoin, the conformations predicted by the force field are generally similar to those predicted with RESP charges, except in the case of n = 6 for which the most stable conformation differs (see Supplementary Material. For the present systems, and for all sizes considered in the range n = 1–10, the isomer with the lowest DFT energy was always among the five lowest-energy conformers at the force field

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level with RESP charges, the conformers predicted using NBO charges never being lower once reoptimized with DFT. Since we have not carried out a systematic global optimization search directly at the DFT level, we cannot exclude that even lower structures would exist (and they likely do). However, the isomers under study cover different structural families and the tendencies we obtain for the stable conformers are consistent with earlier studies. 27,28 In addition to the most stable conformer, we also selected interesting structures close in energy and displaying a contrasted hydration pattern around hydantoin. All structures were characterized in terms of their formation energy ∆Eform (n) defined by

∆Eform (n) = E[H(H2 O)n+1 ] − E[H(H2 O)n ] − E[H2 O],

(2)

where E[X] denotes the total electronic energy of system X in its locally stable minimum. We also calculated the adiabatic and vertical electron affinities and ionization energies corresponding to the addition or removal of an electron, respectively. Finally, the harmonic infrared spectra of the various low-energy conformers have also been calculated but are only reported as Supplementary Material. All quantum chemical calculations were carried out using the Gaussian09 software package. 35

2.3 Proton-transfer cross sections The charge transfer process is developed in the one-dimensional reaction coordinate approximation associated to the evolution of the ion-target quasi-molecular system along a proton approach toward the centre-of-mass of the hydantoin molecule. 36 The collision dynamics was treated by means of semi-classical methods using the EIKONXS program 37 in the framework of the sudden approximation hypothesis, which considers that vibrational and rotational motions are frozen during the collision time. Charge transfer is indeed a very fast process 38 and electronic transitions can thus be assumed to be much faster than vibrational or rotational motions. 39 As shown by both semi-classical and quantum dynamics calculations, 40,41 such approximation, usually valid in the

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keV energy range, can be extended to lower energies ranging from 10 eV to 10 keV as in the present study. 42 The CT process is highly anisotropic, 39 but consideration of all practical orientations of the impinging proton toward the different targets would not be practical. However, for DNA building blocks such as bare nucleobases 43 or sugars, 44 the reaction has been shown to be markedly enhanced in the perpendicular orientation. We thus treated, as previously in the case of microhydrated uracil 27 or aminooxazole, 28,29 an impact of the proton predominantly perpendicular to the hydantoin ring. For numerical accuracy, the calculation was performed for collisions on both sides of the ring, and the mean arithmetic value was eventually determined for bare hydantoin and quasiplanar clusters. For segregated structures, the calculation was developed also in the perpendicular orientation, toward either the hydantoin ring or the water cluster. Molecular calculations were carried out with the Molpro code 45 at the state-averaged CASSCF level of theory using the 6-311G** basis set for all atoms. ECP2sdf effective core potentials 46 were used for C, N, and O atoms in order to develop calculations at the same level of theory for bare hydantoin and water clusters. For all structures, the active space includes the five highest valence orbitals and the 1s orbital on the impinging proton, however lowest-energy orbitals were frozen in order to be able to carry similar calculations for collisions with all systems. Non-adiabatic radial coupling matrix elements gKL (R) = hΨK |∂/∂R|ΨL i were determined by the finite difference technique: 47

gKL (R) = lim hΨK (R)|ΨL (R + ∆)i, ∆−→0

(3)

with a step ∆ = 0.0012 a.u. checked to provide an accurate stability of the differentiation procedure.

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3 Results and discussion 3.1

Stable structures

The most stable structures found for microhydrated hydantoin having one to 7 water molecules are depicted in Fig. 1. In general we find two types of conformations with the water molecules near the hydantoin plane, forming acceptor hydrogen bonds with the carbonyl oxygens or donor hydrogen bonds with the peripheral imide hydrogens. Alternatively, three-dimensional water clusters forming next to the heterocycle are also obtained. While the latter pattern can be safely denoted as segregated, the former presents several positions for the lateral hydrogen bonds, the water molecules being possibly not all connected with each other if they bind more strongly with hydantoin than to themselves. We thus denote as (n + p) such planar-like conformations in which n molecules lie on one side of hydantoin and p molecules on the other side. The relative stability of these various conformers can be judged from their formation energies given in Table 1. These data show a clear predominance of hydantoin-water hydrogen bonds until the size of 4 water molecules is reached, at which stage a water cluster forming above the heterocycle is favored. In small clusters, and as was reported earlier for 2-aminooxazole, 28 the dangling OH bonds of the peripheral water molecules tend to point away from the heterocycle plane, giving rise to several isomers differing slightly in energy, sharing the same overall topology but with dangling bonds pointing toward the same side of this plane, or on opposite sides. In larger systems having up to 10 solvent molecules, the segregated pattern remains and the microhydrated compound systematically displays complete segregation with the water cluster lying above the hydantoin heterocycle. The size-induced segregation pattern predicted here for hydantoin is very similar to that reported earlier for uracil. 27 For this related molecule, the same phenomenon was found not only qualitatively with a similar set of locally stable conformers, but also quantitatively with the transition between planar and three-dimensional structures occuring exactly at n = 4 using the same DFT method. Hydantoin and uracil differ in their cycle size and in the hybridization level of hydrocarbon atoms, however the hydrophilic part is essentially the same, hence explaining the

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(1+0)

(1+1)

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(2+0)

(2+1) (3+0)

(2+2)

(4S)

(3+1)

(3+2) (5S)

(7S) (6S)

(Ice)

Figure 1: Lowest-energy structures of H@(H2 O)n for different numbers n of water molecules, n = 1–7, and selected isomers all shown with a common orientation of hydantoin. The stable structure of hydantoin deposited on a piece of ice slab is also depicted at the bottom right. similar results obtained here. In contrast with the present results, the microhydration pattern of 2-aminooxazole was found to be regular with a cluster nucleating and growing around an initial 1-molecule seed on the amino tail, reflecting the stronger segregation between hydrophilic and hydrophobic parts in this biomolecule. 28 The formation energies gradually increase from about 10.6 kcal/mol for a single molecule to about 11.8 kcal/mol at n = 10, at which stage they reach similar values as in 2-aminooxazole, 28,29 consistently with the segregation into a single growing water cluster. Significantly lower formation energies are obtained for planar structures for sizes in the crossover regime n = 3–5. The ionization energies also exhibit some dependence on the conformer, with adiabatic values that can be about 1 eV higher in planar conformers relative to the segregated minima. Such variations are

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Table 1: Formation energy ∆Eform , vertical and adiabatic electron affinities (EA), vertical and adiabatic ionization energies (IE) of microhydrated hydantoin, as obtained from quantum chemical calculations at the DFT/M06-2X/aug-cc-pVTZ level. The most stable conformer is underlined. Number of water molecules & (isomer) 0 1 (1+0) 2 (1+1) 2 (2+0) 3 (2+1) 3 (3+0) 4 (S) 4 (2+2) 4 (3+1) 5 (S) 5 (3+2) 6 (S) 7 (S) 8 (S) 9 (S) 10 (S)

∆Eform Vertical EA (kcal/mol/molecule) (eV) 0 -0.803 10.565 -0.479 10.832 -0.457 10.173 -0.461 10.508 -0.434 10.146 -0.404 11.371 -0.380 10.542 -0.409 10.068 -0.404 10.890 -0.331 10.196 -0.381 11.494 -0.328 11.636 -0.338 11.647 -0.270 11.566 -0.216 11.823 -0.248

Adiabatic EA (eV) -0.374 -0.477 -0.291 -0.456 -0.395 -0.080 -0.228 -0.397 +0.009 -0.022 +0.187 -0.215 -0.078 -0.103 -0.085 -0.063

Vertical IE Adiabatic IE (eV) (eV) 10.541 10.258 10.402 9.748 10.290 9.244 10.305 9.512 10.212 9.073 10.219 8.908 10.434 9.582 10.136 8.990 10.137 8.771 10.366 9.495 10.066 8.703 10.286 9.533 10.365 8.838 10.119 9.116 10.200 8.997 10.209 8.630

not clearly apparent on the vertical IE, which mostly shows some overall decrease from the bare hydantoin but with fluctuations amounting to 0.4 eV depending on size and conformer. Such decrease, observable also for adiabatic ionization potentials, was also valid for 2-aminooxazole, and suggests a favored ionization of prebiotic species in presence of water. The value obtained for bare hydantoin itself is higher than when calculated at the CASSCF/6-311G** level of theory by about 0.6 eV, 26 although the shift remains the same for the adiabatic value. The difference is however reduced to about 0.4 eV when considering the dynamical electron correlation effects at the MRCI level of theory, which gives vertical and adiabatic values of 10.13 eV and 9.87 eV, respectively. Similar results were also found for ionization potentials for 2-aminooxazole, 28,29 hence the data in Table 1 appear rather as upper bounds. Except for bare hydantoin, the vertical electron affinities are quite low and also display a steady decrease with increasing number of surrounding water molecules. Upon reoptimization, the adi11



abatic values are further reduced in magnitude, sometimes almost completely as in the cases of (3+0), (4S) and more generally in the largest clusters considered here. Such very low electron affinities suggest that the electron is diffuse around the complex, anionic systems being able to accomodate reasonably well with the additional electron.

3.2

Finite temperature properties

The finite temperature behavior of the various clusters was systematically explored by means of replica-exchange molecular dynamics simulations, but we focus on the most interesting case of n = 4 at which the crossover from planar to segregated conformations takes place. In Fig. 2 we have represented different properties of this system, extracted either directly from the simulations or resulting from the additional analysis of inherent structures. This figure also compares the different behaviors obtained using the RESP and NBO sets of charges on the hydantoin molecule. With RESP charges, the canonical heat capacity shows a broad increase once ˚ temperature reaches 160 K, but no strict peak even if the container radius is varied by ±5 A. This feature indicates that melting largely overlaps with the liquid-vapor transition, with melted molecules having the tendency to thermally dissociate if there were no container. The waterspecific gyration radius also shows essentially monotonic variations, and decreases initially softly at low temperatures before decreasing stronger above 160 K. The range found here for the melting temperature is very similar to earlier computational studies on pure or doped water clusters, 48 and is also comparable to available experimental data. 49 Visual depiction of the density of water molecules at the three temperatures of 25, 100, and 200 K (shown as insets in Fig. 2) illustrate the mechanisms of melting in this system. At low temperature the water cluster remains segregated on one side of hydantoin, before being able to get around it and move to the other side as it is heated up to 100 K. At this temperature, the equilibrium phase has the water molecules still connected as a cluster but flipping as a whole between the two equivalent sides of the heterocycle, with no signature on the gyration radius since the two sides are equivalent. As the temperature is raised above 160 K, the water cluster melts and the system 12


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42

Cv/kB

(a)

25 K

39 36 33

(b)

2

2

Rg (Å )

12

11 100 K

3

SIS/kB

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(c)

2 200 K

1 0 0

50

100

150

200

Temperature (K)

250

300

Figure 2: Thermodynamical properties of H@(H2 O)4 , as obtained from replica-exchange MD simulations and as a function of canonical temperature. The results are shown for the RESP and NBO charges on hydantoin using solid and dashed lines, respectively. (a) Heat capacity; (b) Average gyration radius of the water distribution surrounding hydantoin; (c) Inherent structure entropy. Three water distributions obtained for the RESP charges are depicted in each panel at 25, 100, and 200 K, respectively. 50 is able to visit the planar conformers, in a process very similar again to our earlier findings on microhydrated uracil. 27 Another tool of analysis is provided by the entropy of inherent structures SIS defined from the population of locally stable minima visited along the molecular dynamics trajectories. This quantity displays monotonically increasing variations with a stronger slope as the melting temperature is reached. The entropy is nonzero even at the lowest temperature considered here of 25 K, which shows that the system is already fluxional. Inspection of the inherent structures reveals that only a very small number of minima are indeed visited, differing in the specific orientation of a dangling hydrogen bond. This fluxionality is likely to remain so in a more realistic quantum mechanical description of nuclear motion. The strong increase in the inherent structure entropy above 160 K indicates the occurence of entire new families of structures and is consistent with an even greater extent of fluxionality

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associated with the melted state. At these temperatures, planar conformations become competitive, as was also found for microhydrated uracil near the crossover size between planar and segregated structures. 27 The planar conformers are associated with broader basins of attraction and are thus stabilized by their larger entropy. Such an effect also influences the relative ordering of isomers when including zero-point energy corrections, which similarly to the configurational entropy are primarily dependent on the vibrational frequencies. Using now NBO charges, the water cluster is thermally much more stable and isomerizes significantly only above 200 K, as seen from the inherent structure entropy. The greater stability is consistent with the higher charges predicted by the NBO method, by about 50% relative to the RESP method (see supplementary information), which leads to stronger hydrogen bonds with the water molecules. This exceptional stability of the hydrated compound is probably unrealistic with respect to the aforementioned existing literature. 48,49

3.3

Proton-induced charge transfer

The charge transfer cross sections are presented in Fig. 3(a) for bare hydantoin and quasi-planar clusters up to 5 water molecules. As previously pointed out for microhydrated uracil, 27 a clear shift is observed in the cross sections after addition of the first water molecule, but with similar variations with increasing collision energy. The CT cross sections still increase significantly when adding one more water in an opposite position, then tend to stabilize by successive addition of further molecules. Adding water molecules on the same side of the hydantoin heterocycle appears to steadily decrease the CT cross sections, as shown for example for the (1+1), (2+1), and (3+1) clusters, leading to similar orders of magnitude as for the (3+1) and (3+2) structures with a stabilized value around 10−18 cm2 . Concurrently the charge transfer is favored for symmetric structures compared to non-symmetric ones. This is emphasized in Fig. 3(a) for both (1+1) and (2+0) two-water clusters, but may be noticed also for (2+2) and (3+1) H@(H2 O)4 geometries. Besides, for clusters with an odd number of water molecules, charge transfer is less efficient when molecules are on the same lateral side of the heterocycle, as for example (3+0), compared to the less segregated (2+1) 14


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conformer. More generally, charge transfer is enhanced for symmetrically hydrated clusters, and particularly less efficient when hydration occurs on a single side of hydantoin. These results show how, at the molecular level, the detailed structural properties of the different clusters may influence the CT process. The charge transfer cross sections are in all cases about 100 times higher for quasi-planar water clusters than for bare hydantoin. Such an increase indicates a more efficient proton-induced ionization of hydantoin in the presence of water. However, since the cross sections remain low (around 10−18 cm2 ), the CT efficiency can still be considered as weak. A similar increase of CT cross sections for planar structures was already observed for uracil, 27 yet with cross sections reaching up to 10−14 –10−15 cm2 , showing for this compound that a quite efficient process could be expected to induce energy redistribution and possibly fragmentation. Such behavior may be related to the similar hydration patterns found here for both uracil and hydantoin, at variance with the segregated water clusters exhibited by 2-aminooxazole. For this biomolecule, the charge transfer cross sections indeed remain very low (about 10−20 cm2 ) in both bare and hydrated forms, concomitantly with a very low CT efficiency. 28 From this perspective, hydantoin thus appears to behave inbetween uracil and 2-aminooxazole: As a prebiotic compound, charge transfer is favored compared to 2-aminooxazole, and is more intense in the presence of water, but still weak compared to uracil, in particular in hydrated species. The behavior of hydantoin under microhydration environment is thus consistent with our previous results obtained for uracil 27 and 2-aminooxazole 28,29 in which CT was found to be enhanced mostly for planar-like hydration rings (case of uracil at low hydration numbers) but not much affected by segregated hydration on the side of the heterocycle (2-aminooxazole or uracil at larger hydration numbers). These results are likely related with the localization of the molecular orbitals mainly involved in the process also depicted in Fig. 3 for selected cases. Such orbitals correspond to the highest orbitals centered on bare or hydrated hydantoin whose electron excitations to the + colliding proton (leading to H + H@(H2 O)+ n CT levels) drive strong interactions with the entry H

+ H@(H2 O)n channel, as already depicted. 27 As was found earlier for hydrated 2-aminooxazole, 28

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the molecular orbitals obtained here for hydantoin show very weak variations upon microhydration. Such a weak polarization likewise indicates a weak interaction between the water molecules and the hydantoin heterocycle. The CT cross sections for segregated conformers are shown in Fig. 3(b) for perpendicular collisions of the proton both toward the hydantoin side and toward the opposite side against the water cluster. It can first be noticed that the CT cross sections toward the heterocycle are roughly of the same magnitude for the present segregated structures as previously noticed for quasi-planar structures. They decrease slowly with increasing number of water molecules but keep the same variations with collision energy and are around 10−18 cm2 . The CT mechanism thus appears quite similar in planar-like and segregated clusters when protons collide opposite to the water cluster. In both cases the collision proceeding toward the heterocycle is associated to a weak polarization from the water cluster. Conversely, CT cross sections are markedly lower when collisions take place toward the water side. The effect is particularly significant for four-water clusters, and, as already pointed out for planar-like structures, it is reduced with increasing number of waters. CT cross sections are thus of the same magnitude for collisions toward water in segregated clusters as in bare hydantoin. Considering the orbitals involved, two opposite effects seem to be involved: a polarization of molecular orbitals driven by hydration of the heterocycle and a direct interaction of the impinging proton with the water cluster, at variance with planar-like structures, leading to an overall lower influence on the charge transfer process. Such a result is in agreement with the previous study on 2-aminooxazole 28,29 showing that segregated water clusters do not induce a significant screening of hydantoin and thus only slightly modify the CT efficiency, which then remains very weak with cross sections around 10−19 –10−20 cm2 . The detection of prebiotic species 2,3 suspected to play a key role in the synthesis of polypeptides 20 points out to the significance of photochemistry of extraterrestrial ’dirty’ ices in the formation of organic molecules in the Solar System. This question has motivated laboratory experiments simulating the formation of such prebiotic molecules by irradiation of interstellar ice analogues, notably those undertaken by de Marcellus et al. 8 which found evidence for the presence of hydan-

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(a) Planar clusters

0

2 -16

-2

cross-section (10

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1+1 2+1 3+1 3+2 1+0

cm )

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(b) Segregated clusters

0

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cross-section (10

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


4>H 5>H

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Collision energy (eV)

Figure 3: Charge transfer cross sections upon proton impact on microhydrated hydantoin with various numbers n of water molecules, as a function of collision energy. (a) Planar structures with n + p water molecules distributed on both lateral sides of hydantoin; (b) Segregated structures with the proton hitting the cluster either toward the water cluster (>W) or toward the hydantoin plane (>H). Relevant molecular orbitals involved in the charge transfer process are also depicted for the cases of bare hydantoin, (1+1) and (2+0) conformers in (a), and for the 4>W and 4>H cases in (b). toin in organic residues. In this context, analysis of the reactivity of hydantoin deposited on ice surfaces and comparison with the behavior of microhydrated structures or the bare molecule itself are natural and fundamental issues. In order to evaluate the influence of ice substrate on charge transfer efficiency, the geometry of hydantoin on hexagonal ice surface was locally optimized using the Amber ff99 force field. The molecule was then reoptimized at the DFT level together with the 8 most nearby water molecules, keeping them fixed in the optimization process. In this optimized structure, hydantoin is mainly perpendicular to the basal plane, slightly tilted, and presents an NH side group as an hydrogen bond donor and both oxygens as hydrogen bond acceptors (see Figs.1 and 4). The CT cross sections were determined for proton impacts toward such adsorbed hydantoin, perpendicularly to the ice substrate. For a fair comparison, the process was also investigated for hydantoin under the same orientation but withdrawing the ice cluster. The CT cross sections were thus evaluated for collisions either perpendicular to the ice substrate, with or without it, and parallel to it (without ice) in order 17



to further assess the importance of tilting. The results are displayed in Fig. 4 as a function of collision energy. Unsurprisingly, the procedure with local optimization used for this cluster provides an hydantoin geometry close to the relaxed bare structure, as evidenced from the close CT cross sections perpendicular to the heterocycle found for bare and adsorbed structures. In addition, as pointed out for 2-aminooxazole, 28 the CT cross sections are increased by about one order of magnitude for the tilted structures with respect to collisions strictly perpendicular to the heterocycle. However, at variance with 2-aminooxazole, hydantoin adsorption on the ice substrate neither induces a significant change of the CT efficiency nor a different variation with collision energy; the CT cross sections increase with collision energy whatever the orientation of the colliding proton. The reactivity of hydantoin thus only weakly depends on the presence of ice, which is related with the low polarization of the molecular orbitals involved in the CT process already mentioned for microhydrated conformers. The main difference with 2-aminooxazole is that the amino NH2 group was found to induce a quite stronger hydrogen bonding with the ice substrate relative to hydantoin. These contrasted behaviors show that the influence of the ice substrate strongly depends on the molecule involved and has to be considered case by case.

4 Concluding remarks The fundamental issue of the formation of precursors of the building blocks of life and how they could survive in Space have recently lead to extensive laboratory irradiation experiments with high-energy particles 51 or UV light. 8–10 Evidence for hydantoin in organic residues formed by irradiation of interstellar ice analogues 8 has notably increased interest for this specific compound, especially its reactivity in presence of water or after deposition an icy substrates. In this contribution we have attempted a broad theoretical survey of structural and fundamental properties of hydantoin in contact with a controlled number of water molecules, at zero and finite temperatures. The effects of microhydration on collisions with an impinging proton were also scrutinized by

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cross-section (10

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-3

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parallel to ice surface

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bare relaxed hydantoin -5

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-6

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0

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1

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10

Collision energy (eV) Figure 4: Charge transfer cross sections upon proton impact on hydantoin deposited on a small ice cluster taken from hexagonal ice substrate [shown as an inset as well as in Fig. 1(Ice) under a different orientation] with the proton hitting perpendicularly to the surface (green symbols). For comparison, we show the cross sections in absence of the ice substrate, for the same collisions (orange symbols), and for collisions parallel to the ice substrate, perpendicular to the hydantoin ring (blue symbols). The cross sections for bare hydantoin perpendicularly to its plane are also depicted (black symbols). determining charge transfer cross sections under various conditions. The calculations employed well-established protocols using state-of-the-art methods including some exploration of the energy landscapes with the Amber ff99 force field with replica-exchange molecular dynamics. The most stable structures located were refined using an explicit description of electronic structure at the DFT/M06-2X level. Such replica-exchange simulations give also insight into the finite temperature behavior. Collision dynamics were developed in the semi-classical framework from ab initio CASSCF molecular potentials and couplings. The results obtained in this work may be compared to previous analyses of microhydrated uracil 27 and 2-aminooxazole 28,29 with the aim of driving some general conclusions and trends and rationalize the influence of hydration on the reactivity of prebiotic species. From a structural point of view, a peripheral hydration pattern was first found for hydantoin, leading to quasi-planar structures up to H(H2 O)n with n = 3, either symmetric with regard to the heterocycle, or conversely 19



with water molecules on the same side of hydantoin. A structural transition was identified at n = 4 with the competition between such planar-like structures with segregated cluster-like hydration patterns that become more stable in larger water clusters. This behavior makes hydantoin rather similar to uracil, 27 in which the emergence of three-dimensional structures was found to occur at a few water molecules only. Such structural features also produce similar charge transfer evolutions for both compounds from the bare molecule to planar-like hydrated structures, with at first some increase of the charge transfer cross sections as soon as one water molecule is added, followed by a further stabilization of CT efficiency for successive hydrated structures. However, polarization of the main molecular orbital involved in the charge transfer process appears much weaker in hydantoin compounds than found earlier for microhydrated uracil, 27 which we relate to an overal weaker hydration effect. Such increase of CT efficiency differs more markedly from 2aminooxazole, which exhibits a segregated water cluster bonded to the amino group already from small sizes 28 that leads to an always minor influence on charge transfer, supported also by a mechanism involving similar molecular orbitals. From a prebiotic point of view, hydantoin appears thus more likely to drive energy redistribution after charge transfer than 2-aminooxazole, even if the process remains weak, in particular for quasi-planar hydrated structures as no screening is induced by segregated water clusters. Despite the similarities reported between hydantoin and uracil under microhydrated environments, significant differences were also noted for the segregated (three-dimensional) cases at larger numbers of water molecules. Although a specific behavior with an increase of the CT cross sections at low collision energies followed by a strong decrease at higher energies was found for 3D uracil clusters, 27 an almost similar CT efficiency was predicted for segregated structures and bare hydantoin altogether. Such a result is related to the strong polarization of the main molecular orbitals for uracil, whereas almost no polarization occurs for hydantoin. Hydrogen bonding to the solvent is weak enough in hydantoin to induce very smooth hydration effects, and a poor influence of the water cluster. This also holds for hydantoin adsorbed on a model ice substrate, for which protons impinging perpendicular to the basal ice surface are about 100 times more efficient than on

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the relaxed bare molecule, even in the absence of the ice substrate itself. These results illustrate the specificities of microhydration from one organic molecule to another. The transition from planarlike to segregated-like structures is clearly an important feature, but it does not necessarily polarize the molecular orbitals to a major extent that would lead to major hydration effect on charge transfer. The adsorption on ice substrates, which reveals combined effects of orientation, relaxation and adsorption, would deserve further investigation beyond the present simplified cluster model.

Acknowledgments The authors wish to acknowledge generous computational resources from the regional Pôle Scientifique de Modélisation Numérique in Lyon, the CCIN2P3 in Villeurbanne and the CCRT/CINES/IDRIS under the allocation x20170876622 made by GENCI. The authors aknowledge also support from the COST action TD1308 Life-Origins.

Supporting Information Available Geometry and partial charges on atoms of bare hydantoin, as used with the force field calculations. Harmonic infrared spectra for lowest energy conformers of microhydrated hydantoin. Specific structure obtained using NBO charges for hydantoin in the 6-water cluster.

This material is

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

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Graphical TOC Entry segregated planar

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Size-Induced Segregation in the Stepwise Microhydration of

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