Theoretical Studies on the Photochemistry of Pentose Aminooxazoline

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Theoretical Studies on the Photochemistry of Pentose Amino-oxazoline, a Hypothetical Intermediate Product in Prebiotic Synthetic Scenario of RNA Nucleotides Yuejie Ai, Shu-Hua Xia, and Rong-Zhen Liao J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.6b06061 • Publication Date (Web): 15 Aug 2016 Downloaded from http://pubs.acs.org on August 16, 2016

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The Journal of Physical Chemistry

Theoretical Studies on the Photochemistry of Pentose Amino-oxazoline, a Hypothetical Intermediate Product in Prebiotic Synthetic Scenario of RNA Nucleotides a*

b

Yuejie Ai , Shuhua Xia , Rong-Zhen Liao a

c*

School of Environmental and Chemical Engineering, North China Electric Power

University, Beijing 102206, China b

College of Life and Environmental Science, Minzu University of China,

Beijing100081, China c

Key Laboratory of Material Chemistry for Energy Conversion and Storage, Ministry

of Education, Hubei Key Laboratory of Materials Chemistry and Service Failure, School of Chemistry and Chemical Engineering, Huazhong University of Science and Technology, Wuhan 430074, China E-mail: [email protected], Phone:+86 10 61771470, [email protected]

ACS Paragon Plus Environment


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Abstract

2-Aminooxazole is generally considered as a prebiotic precursor of ribonucleotide on the early earth. Its pentose compound pentose amino-oxazoline has been suggested to be a key intermediate in the prebiotic synthetic scenario. In this contribution, detailed mechanism of the photochemistry of pentose amino-oxazoline has been studied by performing density functional theory and multi-reference CASSCF calculations. Parallel to the “ring-puckering” process which leads to ultrafast nonradiative deactivation, several other photo-dissociation channels are explored in details. In addition, the influences of the pentose structure and the solvation effects with both implicit and explicit water models have been uncovered for both the neutral and the protonated forms. The current theoretical results provide very important information not only for the photo-stability of RNA nucleotides but also for in-depth understanding of the synthesis of other prebiotic nucleotides. Keywords: 2-Aminooxazole, Prebiotic Precursor, RNA, photochemistry, CASSCF,

DFT


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1. Introduction In modern science, the origin of life has always been one of the most attractive scientific issues. Under the inclement environment of the Archean age, there is rather limited selection of prebiotic feedstock molecules for life to evolve.1-3 How these prebiotic molecules, or even more complex pan-molecules, could have been developed on our planet is one of the most challenging subjects that have attracted steadily growing attentions. 1-5 The RNA world theory

6,7

is perhaps the most central hypothesis that regarding

the function of RNA for the emergence of terrestrial life. Driven by this theory, there is an unprecedented step forward for the synthesis of ribonucleic acid building blocks under plausible prebiotically experimental conditions.8-12 Among those synthesis, perhaps the prebiotic synthesis of nucleotides is the major goal in this field since they are the basic unit of RNA and DNA, possessing decisive biological functions, involving almost all the biochemical reactions in vivo.13

NH2 OH O N NH2 2-amino-oxazole

N

N O

NH2 HO

O

OH O

N O

pentose amino-oxazoline

O O P O Oβ-ribocytidine2'-3'-cyclic phosphoate

Scheme 1. Hypothetical prebiotic precursors of RNA nucleotides. The Sutherland-synthesis,8 which was elaborated by Powner et al. recently, is proposed to be the most plausible scheme for the genesis of pyrimidine nucleotides in prelife chemistry. One of its key steps was the formation of 2-aminooxazole (Scheme 1) from glycolaldehyde and cyanamide under base catalysis. The special synthetic experimental condition, UV-light and phosphate buffer, implies significant early-earth geochemical models, and seems to play an important role in the synthesis.12 In the origin era, ultraviolet must be very crucial selection of natural



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factors influencing abiogenesis and all these main intermediates during the prebiotic synthetic routes to nucleotides must be photostable to the UV-light. 14 In the past few decades, although many efforts have been devoted into the prebiotic synthetic method using prebiotic molecules and radicals, the plausible mechanism of abiotic synthesis of RNA nucleobases and nucleotides are far from being understood. Nevertheless, beyond most of the experiments, a detailed knowledge of molecular mechanisms of the abiotic synthesis, especially their photochemical and photophysical processes under some control factors (UV radiation et. al) remain elusive. Quantum chemical calculations are a viable complement to the experiments in addressing various problems related to the origin of life.15-23 Since the accumulation of 2-aminooxazole was over long periods of time that presumed in the Sutherland’s scenario, the underlying mechanisms for the photochemical formation, photostability and other relevant properties of this compound have been studied theoretically by different groups.

15,17,21-24

Szabla et. al, features the

photochemistry of

2-aminooxazole with effective non-radiative deactivation through two relaxation pathways: “ring-puckering” and N-H bond stretching, by multi-reference quantum chemical calculations in 2013.24 Nevertheless, there has been no systematic study, as yet, on the photochemistry of the sequential intermediate products following the 2-aminooxazole synthesis suggested by Saladino et al.25 In the synthesis of Powner et al., 2-aminooxazole reacts to glyceraldehyde and giving the pentose amino-oxazolines with high overall yield in un-buffered aqueous solution.8 Starting from this compound, in this article, we report the photo-stability mechanism of pentose amino-oxazoline to further reveal the photochemistry of the suggested scenarios for prebiotic precursor. By means of high-level computational calculations, we scrutinized several possible photochemical reaction and radiationless deactivation pathways with a special emphasis on some new reaction pathways involving the pentose ring, the protonated form, and also the solvent models.

On the basis of the computational descriptions,

we herein construct a bridge interconnecting these experimental species and their intrinsic mechanisms which may bring new insight into the synthesis of other


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nucleotides.

2. Computational details In order to scrutinize possible photochemical reaction paths, the B3LYP hybrid functional of density functional theory 26-28 and the time-dependent density functional theory (TDDFT) 29-31was applied to do rigid scans of the potential-energy profiles for the ground and excited states; see details in Section 3. The B3LYP functional is moderate computational cost and predicts more accurate theoretical values of 2-aminooxazole than MP2 method as compared in the work of Møllendal and Konovalov.22 In addition, based on above potential energy surfaces, the corresponding reactants, intermediates, products, transition states, and in particular the conical intersections (CIs) were further explored by complete active space self-consistent field (CASSCF) theory.

32,33

For the active space, 8 electrons in 8 orbitals labelled as

CAS(8,8) was chosen. The CASPT2 single point energies were then obtained based on the CASSCF optimized structures with the MOLCAS 7.6 package.34,35 Such CASPT2//CASSCF approach gives better balance of computational cost and accuracy and has been successfully applied in many studies.

36-39

The 6-31G(d) basis set was

chosen in present study. Nature of local minima or first-order saddle points was confirmed by analytical frequency calculations. To explore the solvent effects, two strategies were applied─implicit and explicit water models. First, the implicit water model using the polarizable continuum model (IEF-PCM)

40-41

with water solvent (ε = 78.3553). Second, for the explicit water

models, a two-water molecule model was used to form important inter-molecular hydrogen bonds with pentose amino-oxazoline and water molecules. All the calculations (except the CASPT2 computations) were carried out with the Gaussian 09 software package. 42



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3. Results and discussions 3.1 Protonation state

Scheme 2. Structures of neutral and protonated forms of pentose amino-oxazoline.

As shown in Scheme 2, the neutral pentose amino-oxazoline molecule may get protonated depending on the pH of the solution. To compute the corresponding pKa value, we first optimized the equilibrium gas-phase geometries of neutral and protonated forms at the B3LYP/6-311G(d,p) and the B3LYP/def2-TZVP levels. Then, single-point

calculations

at

the

B3LYP/6-311++G

(2d,2p)

and

the

B3LYP/def2-TZVPPD levels in conjunction with self-consistent reaction field (SCRF) method

43-45

and SMD solvation model of Truhlar and co-workers’

46

have been

performed based on the above optimized structures. Table 1 show that pentose amino-oxazoline has a pKa of about 6-7 using the SMD solvation model (about 4 using the IEF-PCM model), suggesting that the neutral and protonated forms are most likely in equilibrium at neutral pH. Consequently, both the neutral and protonated forms are considered in the following calculations. Table 1. Calculated pKa values by SMD solvation model and IEF-PCM model at the B3LYP/6-311++G(2d,2p)//B3LYP/6-311G(d,p) and the B3LYP/def2-TZVPPD //B3LYP /def2-TZVP levels. SMD IEF-PCM 6-311++G(2d,2p) def2-TZVPPD 6-311++G(2d,2p) def2-TZVPPD pKa =6.1 pKa =7.1 pKa =3.9 pKa =4.0


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3.2 DFT results

To get a quick sketch for the possible reaction pathways, we first use density functional theory method to get the geometric and reaction information for the stationary states.

3.2.1 Stationary structures for neutral and protonated pentose amino-oxazoline

The optimized structures in vacuum for the ground state (S0) and the first excited state (S1) of neutral and protonated pentose amino-oxazoline are depicted in Figure 1. As shown in Figure 1, the furan ring is up from the plane of the oxazoline. Compared with the geometry of S0, there are alternations in bond lengths and obviously structural change of oxazoline in the S1 state. For instance, the measure of the C1-N18 bond amounts to 1.283 Å and 1.422 Å for S0 and S1 state, respectively. The C1-N6 bond is also increased to 1.382 Å in S1 state. Therefore, the excitation mainly occurs on the oxazoline. On the other hand, for the protonated model, similar alternations in bond lengths are also located in the oxazoline. This change breaks the conjugative effect and results in the out of plane structures of hydrogen H23 and also the amino group.



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Figure 1. Optimized geometrical parameters for neutral and protonated pentose amino-oxazoline, calculated at B3LYP/6-31G(d) level and TDDFT//B3LYP/6-31G(d) level for ground and excited state, respectively. 3.2.2 Possible radiationless dissociation pathways for neutral and protonated pentose amino-oxazoline by TDDFT calculations

H15 14 O 11 C 10

9

N-H bond dissociation

16

O C4 5

H O

C

2

C C 3

18

N

7

C O

1

6

H

C-O bond dissociation

N

17

H 8

pentose amino-oxazoline

C-N bond dissociation O-H bond dissociation

Figure 2. Schematic drawing for possible bond dissociation pathways. In order to investigate possible dissociation pathways, we studied several main bond dissociations as schemed in Figure 2. Based on the optimized stationary


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geometries, potential-energy profiles along different stretching coordinates are presented in Figure 3 and Figure 4, for neutral and protonated molecule, respectively.

Figure 3. Potential-energy profiles along different bond coordinates in S0 and S1 states for the neutral molecule. The profiles were draw from rigid scans at the TDDFT//B3LYP/6-31G(d) level.(energies in kcal/mol, bond length in Å )

Figure 4. Potential-energy profiles along different bond coordinates in S0 and S1 states for the protonated molecule. The profiles were draw from rigid scans at the TDDFT//B3LYP/6-31G(d) level. (energies in kcal/mol, bond length in Å ) From the scanned profiles, there are two possible cleavage pathways that may lead



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to fast deactivations: the N-H and C-N bond dissociations. Specifically, for the neutral molecule, cleavage of N-H bond leads to a S1/S0 conical intersection at approximately 1.6 Å. The N–H bond stretching mechanism has been proposed to be one primary radiationless deactivation mechanism via dark 1πσ* state that has been found in system like 2-aminooxazole

24

, pyrrole

47

, indole

48

and so on. However, for the

protonated model, from the optimized structures in rigid scans, we found when the N6-H8 bond length is increased from 1.3 Å to 1.4 Å, there is obvious turnover of the amino group and the molecular geometry has changed dramatically. Thus, along with the stretching coordinate of N-H near 1.4 Å, the molecular geometry has changed dramatically and results in a sharp drop on the energy surface. Another important radiationless pathway is the cleavage of C-N bond. Although the C-N bond is double bonded, the lone pair on N atom makes it is a good proton acceptor and the double bond is probably weakened then.

The scanned reaction potential-energy profiles of

the C1-N18 bond reveal a crossing between the S1 and S0 surface near the C-N bond distance of approximately 2.4 and 2.2 Å for neutral and protonated molecule, respectively. We also studied the cleavage energy profiles of C-O and O-H bonds as shown in Figure 3 and Figure 4. However, the parallel lines or sharp inflection points of S0 and S1 indicate that these bond cleavages may not induce possible conical intersections between the ground state and excited state.

3.3 CASSCF and CASPT2 results in the gas phase

Based on the information from the DFT calculations discussed above, we then employed CASSCF method to get more accurate details of the conical intersections. The optimized geometries for the stationary points and CIs of neutral and protonated pentose amino-oxazoline are shown in Figure 5 and Figure 6, respectively. The computed corresponding energies are summarized in Table 2. The CASPT2 energy differences at the CI structures of Table 2 have been summarized in Table S2.

Table 2. CASPT2//CAS(8,8)/6-31G(d) single point energies (kcal/mol) on top of the

optimized

structures

at

the

CAS(8,8)/6-31G(d)


level

in

vacuum.

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CAS(8,8)/6-31G(d) results have be given for comparison. neutral S0 S1-cas CI-NH CI-CN CI-bend

protonated

CASPT2

CAS

CASPT2

CAS

0 110.26 111.63 128.04 101.69

0 119.41 113.79 133.29 117.51

0 113.81 123.00 121.42 104.83

0 124.22 123.18 132.25 114.73

Figure 5. Optimized geometrical parameters for neutral pentose amino-oxazoline, computed at CAS(8,8)/6-31G(d) level. (bond length in Å )



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Figure 6. Optimized geometrical parameters for protonated pentose amino-oxazoline, computed at CAS(8,8)/6-31G(d) level. (bond length in Å )

3.3.1

Neutral molecule

Based on the optimized structure of the S0 state in Figure 5, we computed CASPT2 vertical excitation energies for the lowest-lying excited states of neutral pentose amino-oxazoline at MS-CASPT2//CASSCF(8,8)/6-31G(d) level of theory as summarized in Table S1. The corresponding transition orbitals have been drawn in Figure S1, where the lowest absorption S1 is a π to π* transition at 7.32 eV. The most intense transition is a nπ* excitation at 7.45eV, showing the oscillator strength of 0.1262. From the analysis of molecular orbitals in Figures S1, we found that these two transitions involve the C-N bond of the amino-oxazoline ring, which are the π orbital of C-N bond and the lone pair orbital of N atom. Therefore, when it is excited, the C-N bond is mainly involved in the possible transitions. The optimized structure of the S1 state in Figure 5 shows that compared to the ground state, there is a conspicuous lengthening in the C1-N18 bond (increased from 1.284 Å to 1.457Å). Such change makes the oxazoline a little bit turned up and the energy was calculated to be 110.26kcal/mol as summarized in Table 2. We have located three conical intersections for the neutral model at the CASSCF/6-31G(d) level, as presented in Figure 5. First, the geometry of the CI between the repulsive 1πσ* (N-H) state and the ground state displays a N−H distance of 1.904 Å which is longer than the one in rigid scan. The CI-NH is only 1.37 kcal/mol above the S1 state. For five-membered heterocycles, the ring-distortion deactivation mechanism has also been considered as the primary non-radiative pathway as suggested by Vazdar et al.49 First, a ring-puckered conical intersection between the S0 state and the S1 state which is of 1ππ* character stems from the twisting around the double C=N or C=C bonds in the five-membered aromatic ring. The results of such twisting motion eventually stabilize the excited 1ππ* states and finally internal conversion (IC) from the 1ππ* state to the ground state (S0) occurs. Second, a ring-opening mechanism that


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mediated by a conical intersection via πσ*(C-N) state is also suggested. We have located both two conical intersections (CI-bend and CI-CN) for the neutral model; see Figure 5. In the case of the CI-bend, the amino group is tilted out of the ring of the oxazole plane. Owing to the twisting of the amino group, it forms an intra-molecular hydrogen bonding of 2.253Å with the hydroxyl group of the pentose ring. Such characteristic hydrogen bonding can stabilize the pentose amino-oxazoline. The potential-energy profiles along the ring-puckering motion with linear interpolation in internal coordinates (LIIC) by Szabla et al. showed a barrierless manner for the ring-puckered CI. We also did linearly interpolated internal coordinate calculations for the CI-bend pathway and found there was a small barrier of 8.9 kcal/mol, see Figure S2 for details. The conical intersection responsible for the IC process from the πσ*(C-N) state to S0 state shows that the C-N length is increased to 1.866 Å. However, starting from the S1 minimum, it needs to across 17.78kcal/mol to reach the ring-opening conical intersection, see Figure S2. Meanwhile, the LIIC calculations also showed that the pathway through CI-NH conical intersection had much higher barrier (41.1kcal/mol) to reach. Therefore, in summary, for the neutral pentose amino-oxazoline, the most efficient deactivation pathway is the ring-puckered deactivation mechanism. 3.3.2

Protonated molecule

The geometries of the stationary points and the CIs for the protonated pentose amino-oxazoline model are presented in Figure 6. The calculated relative energies and corresponding transition orbitals have been summarized in Table 2 and Figure S3. Protonation at N position makes the vertical excitation of S1(ππ*) has a strong π

→ π* transition at 7.62eV with the intense oscillator strength of 0.6768. The calculated relative energy of S1 is 113.81kcal/mol. Compared to the neutral molecule, due to the protonation at N18, the protonated H23 and the amino group of S1 structure twist out of the initial planar ring and the C1-N18 and C2-N18 bonds are lengthened to 1.377Å and 1.495 Å respectively. As a result, the C1-N18 bond is weakened and the ring-opening conical intersection (CI-CN) represents a relatively lower energy compared to the neutral one (121.42kcal/mol vs 128.04kcal/mol). A longer C-N bond



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length of 1.916 Å and an intra-hydrogen bond of 2.629 Å between H23 and O14 of pentose ring is also found. On the other hand, the crossing seam via 1πσ* (N-H) state to the S0 state was computed to show the N-H length of 2.135 Å and a higher energy of 123kcal/mol. It is worth to mention that we also got a conical intersection that involved in the protonated N18-H23 bond; see optimized structure in Figure S4. However, such conical intersection has too high relative energy compared to the stationary structure of S1 and we believe this pathway is not an efficient deactivation way. In summary, due to the effect of the protonation, the C-N bond is weakened and the deactivation pathway through CI-CN has lower barrier than the neutral one. However, it still cannot compete with the decay through CI-bend. 3.4 Solvation effect

The scanned potential-energy surfaces at TDDFT//PCM/B3LYP/6-31G(d) level that provide insight into the photochemical process under the implicit PCM model can be found in Figure S5 and S6, which showed quite similar curves compared to the ones in vacuum, for both neutral and protonated molecules. It seems that there is small influence on the photochemical pathways by solution using implicit solvation models. CASPT2 single point energies based on the optimized structures in vacuum with PCM model are summarized in Table 3. One may notice that compared to the energies in vacuum (Table 2), there are different changes in the single point energies with PCM model. In general, the neutral ones have been stabilized by solvent models. In addition, as shown in Figure S2, the LIIC calculations showed that the general conclusion is similar to the situation in vacuum that is the ring-puckered mechanism is the most effective route. Table 3. CASPT2//CAS(8,8)/6-31G(d)/PCM single point energies (kcal/mol) on top of the optimized structures at the CAS(8,8)/6-31G(d) level in vacuum. neutral CASPT2(8,8)


protonated CASPT2(8,8)

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S0 S1 CI-NH CI-CN CI-bend

0 108.77 109.53 126.81 95.81

0 108.01 131.7 125.08 106.85

Further efforts are made by using the explicit solvation model with two water molecules, as shown in Figure 7 and 8. Taking comprehensive consideration of the implicit and explicit solution models, single point energy calculations by CASSCF and CASPT2 with PCM scheme for water models have been summarized in Table 4. In view of the vertical excitation energies in Table S1, with the solvent effect, the n→π* transition of neutral molecule presents a much intense f (0.6789) than the one in vacuum. Besides, in general, the vertical excitation patterns of the neutral and protonated water models are quite similar to the ones in the vacuum, see Figure S7 and S8. On closer examination on the structures in Figure 7 and 8, we found that there is strong hydrogen bond network between the waters and the molecule itself. For instance, in the ground state structure of “S0-wat-cas”, there are inter-molecular hydrogen bonds between water molecules and the amino group (2.053 Å), N18 (2.212 Å), and O14 (2.155 Å) atoms. In addition, there is also hydrogen bond of 1.914 Å between two water molecules. Such two-water cluster is quite in agreement with the work of Calvo et al. 23 In their research, the stable structures of microhydration on the 2-aminooxazole “AO(H2O)n” (AO= 2-aminooxazole, n=1~20) showed both inter- and intra- hydrogen bond network also. 23 Similar hydrogen bond network stabilizes the S1 state with only 94.94kcal/mol in energy and consequently may influence the deactivation channels. For the neutral water models, as shown in Table 4, the ring-puckered CI lie 3.81kcal/mol above the potential energy surface of S1 state. We deduce from the optimized geometries in Figure 7 that this is because of the fracture of the inter-molecular hydrogen bond from “S1” to “CI-bend”. One may see that in CI-bend, two water molecules have moved to one side of the amino group since it titled up and



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forms an intra-molecular hydrogen bond with the hydroxyl group. Overall, a small reaction barrier is induced along with the adjustment of hydrogen bond network between the molecule and the solvent for CI-bend. Another striking impact of the solution molecules can be seen in the CI-NH pathway. In the presence of water molecules, along the prolongation of the N-H bond in the amino group, to stable the N8 atom, the water molecules adjusts their orientations to form new hydrogen bonds with N8 atom. Such process not only breaks the stable water network, but also pushes the conical intersection goes up to much higher mountaintop (139.88kcal/mol) with a longer N-H bond of 3.674Å. On the other hand, although the maintenance of the hydrogen bond network in the CI-CN structure, the deactivation pathway through the C-N bond breakage still cannot compete with the ring-puckered mechanism since it needs to across energy of 16.87kcal/mol.

Figure 7. Optimized geometrical parameters for neutral pentose amino-oxazoline with water molecules, calculated at CAS(8,8)/6-31G(d) level. (bond length in Å )


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Figure 8. Optimized geometrical parameters for protonated pentose amino-oxazoline with water molecules, calculated at CAS(8,8)/6-31G(d) level. (bond length in Å )

The protonation on the N18 atom impacts the hydrogen-bond network a certain extent. The hydrogen bond N…H of N18-H2O turns into H…O of H23-H2O. This change weakened hydrogen bond with the hydroxyl group in the pentose. In the structure of “S1-wat-proton-cas”, a clear hydrogen bonded cycle network formed in the bond length of 2.227, 2.018 and 1.741 Å respectively. Along the N6-H7 bond cleavage path, the water molecule was firmly attracted by the protonated hydrogen with a bond length of 1.830 Å and when the N-H bond reaches the 2.248Å, a conical intersection of 130.10kcal/mol was found. The conical intersection CI-CN in Figure 8 shows that the C-N bond is lengthened to 2.046 Å with the relative energy of 122.75kcal/mol. Similarly, due to the protonation, the reaction barrier of CI-CN is reduced to 7.64kcal/mol. Compared to above two deactivation channels, the ring distortion CI is only 117.16kcal/mol which shows great potential in all the deactivation ways. In all, under the detailed examination of the explicit water molecules, we conclude that the water molecules may form hydrogen-bond network with the studied parent molecule and if such weak balance is interfered or even breakdown by intra-molecular



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or external environment, there will be important impacts on the deactivation pathways. For instance, a small reaction barrier is induced along with the adjustment of hydrogen bond network between the molecule and the solvent for CI-bend.

Table 4. CASPT2//CAS(8,8)/6-31G(d)/PCM single point energies (kcal/mol) on top of the optimized structures at the CAS(8,8)/6-31G(d) level in vacuum.

S0 S1 CI-NH CI-CN CI-bend

Neutral-water CASPT2(8,8) 0 94.94 139.88 111.81 98.75

Protonated-water CASPT2(8,8) 0 115.11 130.10 122.75 117.16

4. Conclusions In conclusion, in the present study, we have performed DFT and ab initio calculations of electronic structures and potential energy surfaces to elucidate possible radiationless decay mechanisms for pentose amino-oxazoline, a crucial intermediate in prebiotic synthetic scenario of RNA nucleotides. The calculated conical intersections and reaction-path revealed that the “ring-puckering” mechanism might be the most effective relaxation channel. Compared to the former theoretical work, in this work, three effects, the pentose ring structure, the protonated state and the solution environment are of considerable interest. The pentose ring structure provides new probability to form inter- and intro- molecular hydrogen bonds. The protonated state weakened the C-N bond and lowered the reaction barrier of CI-CN. In solution, the hydrogen bond network between the water molecule and the parent pentose amino-oxazoline may influence the deactivation mechanisms under different intra- or inter- molecular environment. These findings will supply important information for in-depth understanding of the synthesis of other prebiotic nucleotides.


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Electronic Supplementary Information (ESI) available: [Vertical excitation energies and transition molecular orbitals for the low-lying excited states of pentose amino-oxazoline and its protonated form have been presented in supporting information]. See DOI: 10.1039/x0xx00000x Acknowledgments This work was supported by the National Natural Science Foundation of China （21403064, 21503083).

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Theoretical Studies on the Photochemistry of Pentose Aminooxazoline

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