Introduction

Since the early Miller and Urey’s experiments (1959), the main concern of prebiotic chemistry has been to understand how the compounds necessary for the origin of life could be formed in the interstellar medium or on icy grains. A number of complex organic molecules have been already detected in various astrophysical environments, in the interstellar medium as well as in meteorites or comets and species which could be precursors of life may drive special interest (de Marcellus et al. 2011; Huber et al. 2003). Furthermore, since aminoacids have been discovered in the Murchison meteorite (Cooper et al. 1992), the hypothesis of an exogen origin for life has been suggested and widely discussed. In this assumption, transport of prebiotic building blocks and their survival under spatial conditions as solar UV radiations or cosmic rays are important open questions (Ehrenfreund et al. 2002).

Within a more general context, radiation damage to biological species has been shown to be driven not only by photon radiation, but also by secondary particles as low-energy electrons, radicals or ions generated along the ionizing radiation track (Michael and O’Neill 2000). Such studies may be supported by time-of-flight gas phase experiments, generally performed at keV energies (Alvarado et al. 2006; de Vries et al. 2002) but also at lower eV energies (Deng et al. 2005), combined with ab-initio theoretical treatments (Bacchus-Montabonel and Tergiman 2011a, 2012). As far as astrophysical environments are concerned, these ion-biomolecule collisions may occur in a very wide temperature range (Bacchus-Montabonel 2011), from 10 K (~meV) in the interstellar medium, to 104 K (~10 eV) or more in evolved stars, and can reach up to MeV energy for high energy bare nuclei in cosmic rays. Considering the abundance of hydrogen in space, collisions of prebiotic compounds with protons may be an important process, even fundamental in ionized clouds of the interstellar medium (H II regions) either in the gas phase or on icy grains. These reactions could drive the destruction of such species and may be considered in the reaction sequence of formation and destruction processes. We have thus investigated proton-induced collisions with a series of possible prebiotic species.

As a first step, attention may be focused on the DNA and RNA building blocks, nucleobases or sugar skeleton and even the phosphate group. Nucleobases have indeed been widely investigated in gas-phase experiments (de Vries et al. 2002) as well as in theoretical approaches (Almeida et al. 2014; Bacchus-Montabonel and Tergiman 2011b), mainly with regard to cancer treatments of hadrontherapy. A strong sensitivity to radiation has been pointed out, in particular for pyrimidine nucleobases as uracil or thymine. The deoxy-D-ribose sugar part has also been studied both experimentally (Alvarado et al. 2006; Deng et al. 2005) and theoretically (Bacchus-Montabonel 2013, 2014; Hervé du Penhoat et al. 2014) showing a strong dependence upon the conformation of the molecule. Effectively, even if the 2-deoxy-D-ribose is in the five-membered ring furanose form in DNA, the six-membered ring pyranose form is preponderant in gas phase experiments. Both forms have thus been considered. However, some more specific species would be also of crucial interest. Considering indeed the ‘RNA world’ hypothesis (Crick 1968; Orgel 1968), formation of RNA occurs from purely chemical reactions but, experimentally, the direct process from ribose and nucleobase fails (Joyce 2002). An alternative efficient and selective sequence (Powner et al. 2009) proposed the 2-aminooxazole as a potential prebiotic compound. Possible microwave spectroscopy observation of that molecule with an amino NH2 group bounded to the 5-membered oxazole ring has been checked (Møllendal and Konovalov 2010) and its formation in prebiotic conditions has been investigated theoretically (Szabla et al. 2013a, b; Bacchus-Montabonel 2015a). A synthesis of all these studies toward a comparative analysis of these different plausible prebiotic compounds, each of them corresponding to a cyclic five- or six- membered structure, could identify some qualitative trends in their behaviour in proton-induced collisions which might enlighten their possible survival in proton-rich environments.

Different processes have to be taken into account in ion-induced collisions, as a first step, excitation and ionization of the molecular target, followed by fragmentation of the ionized species. Ionization of the biomolecule may proceed directly, or by charge transfer from the incident ion to the biomolecular target. The fragmentation process has been widely investigated experimentally (Alvarado et al. 2006; Almeida et al. 2014; Deng et al. 2005; de Vries et al. 2002) providing fragmentation patterns which may be compared to theoretical analysis looking at the evolution of the ionized biomolecule considering an almost instantaneous ionization of the target (Hervé du Penhoat et al. 2014; López-Tarifa et al. 2011). However the first ionization step is quite important and has to be taken into account. In particular, charge transfer ionization is a determinant process which may be studied theoretically in the framework of the molecular representation of the collisions. We have proposed a quantum molecular treatment which has shown its efficiency for such ion-biomolecule systems (Bacchus-Montabonel et al. 2005). The potentials and non-adiabatic coupling matrix elements involving the different molecular states are determined by ab-initio quantum chemistry methods and the collision is performed semiclassically. Such approach has been developed at the same level of theory for the series of cyclic prebiotic compounds in order to exhibit some global qualitative trends.

Molecular Treatment

The charge transfer process is described by the evolution of the quasi-molecular system formed by the incident proton and the biomolecular target. In our case of polyatomic molecules, a model is defined using the one-dimensional reaction coordinate approximation (Bacchus-Montabonel et al. 2000; Bene et al. 2009) and the collision system is considered as a quasi-diatomic molecule moving along the reaction coordinate corresponding to the distance R between the projectile ion and the centre-of-mass of the target. As already pointed out, charge transfer is a very fast process and electronic transitions can be assumed to be much faster than vibrational and rotational movements of the biomolecule. The process may thus be treated in the framework of the sudden-approximation hypothesis by keeping the target geometry frozen during the collision time. Such a simple approach neglecting the internal motions of the biomolecular target has been shown indeed to provide quite reliable results for very fast processes as those considered here (Bacchus-Montabonel and Tergiman 2006).

The different prebiotic targets are presented in Fig. 1. The geometries have been optimized by means of CASSCF (Complete Active Space Self Consistent Field) and DFT (Density Functional Theory) approaches. Pyrimidine nucleobases, uracil and thymine, are constructed around a six-membered planar ring and different orientations with regard to this planar ring may be considered. The 2-deoxy-D-ribose (dR) is constructed on a five-membered ring in the furanose form and on a six-membered ring for the pyranose one. But, both structures correspond to a non-planar ring and a mean plane going through the centre-of-mass of the ring has been defined. Orientation with regard to the five-membered ring of 2-aminooxazole may also be considered. This collision system is displayed in Fig. 2 with the ring in the vertical xy plane. In order to take account of the anisotropy of the process, both perpendicular (along z), and in-the-plane geometries (along x and y) are considered.

Fig. 1
figure 1

Geometry of the different prebiotic compounds

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Fig. 2
figure 2

internal coordinates for 2-aminooxazole

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Molecular calculations have been carried out using the MOLPRO code (Werner et al. 2012) with the 6-311G** basis set. Calculations are performed in Cartesian coordinates, with no symmetries, taking account of all electrons. The potential energies and non-adiabatic coupling matrix elements (NACME) have been calculated at the CASSCF/CASPT2 (Complete Active Space Perturbation Theory 2nd order) level of theory for R values between 0.5 and 9 Å. Similar active spaces have been considered for each species, involving the six valence orbitals of highest energy, constructed on the 1 s orbital on the colliding hydrogen of course, and mainly on πC5C6 and πCO orbitals for pyrimidine nucleobases, on 2pxyz O1 and 2pxyz O3 orbitals on the oxygen of the ring and of the external chain for dR, and on 2pxyz N and πCC orbitals on nitrogen and carbons of the ring for 2-aminooxazole (see Fig. 1). The 1 s orbitals on oxygen, nitrogen and carbon have been considered as frozen cores in all cases. For numerical accuracy, NACME’s have been calculated by means of a three-point numerical finite difference technique taking the centre-of-mass of the target as origin of electronic coordinates (Fraija et al. 1994).

The mechanism of the charge transfer may be analysed from the potential energy curves of the molecular states involved in the collision process. A characteristic example is presented in Fig. 3 for the proton-induced collision on dR-furanose in the perpendicular orientation showing a strong interaction between the entrance H+ + furanose channel and the highest charge transfer level followed by successive single excitations with lower charge transfer channels.

Fig. 3
figure 3

Adiabatic potential energy curves of 1A{H+ + furanose} molecular states in the perpendicular geometry. Red {2pz O3 1sH}; green {2pz O1 1sH}; blue {2pxy O3 1sH}; black {(2pz O3)2}

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Collision Dynamics

The collision dynamics has been performed by means of semiclassical methods assuming the geometry of the biomolecule frozen in its ground state during the collision time. Such a simple approach has been shown to provide quite reliable results for energies above ~10 eV/amu (Bacchus-Montabonel 1999; Stancil et al. 1998). Recent studies have shown besides that such approach could be extended to lower collision energies down to eV (Chenel et al. 2010; Linguerri et al. 2013) providing the order of magnitude of the charge transfer cross sections in a wide impact energy range. The collision treatment was performed by means of the EIKONXS program (Allan et al. 1990) taking account of all the radial coupling transitions.

As already pointed out for collisions with carbon ions (Bacchus-Montabonel and Tergiman 2006; Bacchus-Montabonel 2015b), the process is clearly anisotropic. This may be seen on Fig. 4a for dR and 2-aminooxazole. The charge transfer process is generally preferred in the perpendicular direction where steric hindrance is reduced. In the planar approach, interaction with peripheral groups could reduce significantly the efficiency of the process, as shown for example for the furanose structure presenting a CH2OH chain bounded to the ring, or for 2-aminooxazole NH2 group. On the contrary, for molecules like pyranose, which structure is relatively regular with no peripheral chain, the anisotropic effect remains weak in the whole energy domain. Anyway, in order to take into account this orientation effect, the mean value between perpendicular and planar approaches has been calculated for every molecular target. The results are presented in Fig. 4b.

Fig. 4
figure 4

Charge transfer cross sections in proton-induced charge transfer. a Blue, furanose; red, pyranose; black, 2-aminooxazole. Dashed lines, perpendicular approach; dotted lines, in-the-plane approach; full lines, mean value. b Blue, furanose; light blue, pyranose; red, uracil; green, thymine; black, 2-aminooxazole

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Clearly, the electron capture in proton collisions appears to be more efficient for the sugar skeleton, particularly in its furanose form, than for the pyrimidine nucleobases or 2-aminooxazole. Different factors could be pointed out. First of all the composition of the species: uracil, thymine or 2-aminooxazole molecules include nitrogen atoms when the dR ring is only formed of oxygen and carbon. The different reactivity of nitrogen would certainly drive the different behaviour of dR compared to nucleobases or 2-aminooxazole. Furthermore, even if 2-aminooxazole corresponds to a five-membered ring, it is constructed on a planar ring like uracil and thymine when both dR forms are non-planar. More or less, two groups could be evidenced, nucleobases and their precursor 2-aminooxazole on a one hand, and sugar moiety on the other hand, even if pyranose appears to join a bit both groups.

These differences in charge transfer cross sections might indeed drive implication on the resistance of these potential prebiotic compounds to spatial radiation and their possible survival in space. Effectively, taking into account previous experimental and theoretical studies, an interesting correlation may be pointed out between charge transfer cross sections and fragmentation yield. Considering for example the collision of carbon ions with uracil, almost total fragmentation is observed experimentally for C2+ + uracil (de Vries et al. 2002), decreasing for increasing collision energy, although very low charge transfer cross sections increasing with energy may be calculated (Bacchus-Montabonel and Tergiman 2012). For the C4+ + uracil collision, the fragmentation yield is shown experimentally to be much lower, almost constant with energy, in correspondence to higher theoretical charge transfer cross sections, also quite constant with energy. Such qualitative correlation is also exhibited for collisions with 2-deoxy-D-ribose (Alvarado et al. 2006) showing opposite variations for experimental fragmentation yield and charge transfer cross sections. A lower charge transfer cross section could thus suggest an increased sensitivity in proton collisions with increased destruction of the molecule. In such hypothesis, 2-aminooxazole and pyrimidine nucleobases might thus be more easily disintegrated in proton collisions than furanose. This analysis is of course quite qualitative, but an enhanced fragmentation might question the resistance of such prebiotic intermediates, more specifically in proton-rich regions, and thus their role in the reaction sequence at the origin of life. Of course, we are considering here gas phase processes, even from the experimental point of view, and reactions at the surface of icy grains or in bulk aqueous medium cannot be neglected. Solvation effects have been shown to play a crucial role (Bacchus-Montabonel and Calvo 2015) and have to be considered to drive conclusions on given species at the origin of life.

Concluding Remarks

A compared study of the proton-induced charge transfer with a series of potential prebiotic compounds, nucleobases uracil and thymine, 2-deoxy-D-ribose and 2 aminooxazole has been developed by means of ab-initio quantum chemical methods followed by a semiclassical treatment in the eV to keV collision energy range. A qualitative correlation between such process and possible fragmentation of the biomolecular target in collision with protons has been pointed out. This would identify some qualitative trends suggesting an enhanced sensitivity for nucleobases and 2-aminooxazole in ionized clouds of the interstellar medium, compared to the sugar ribose, leading to a possible weakness of nucleobases in proton-rich regions. Such hypothesis concerns gas phase reactions and the present tendency could however be counterbalanced by solvation effects which have been shown to be determinant in charge transfer processes. Calculations are in progress to quantify such effect for the same series of prebiotic compounds.