Mechanisms of Prebiotic Adenine Synthesis from HCN by Oligomerization in the Gas Phase

Abstract

We explored the potential energy surfaces for adenine synthesis by oligomerizations of HCN or HNC from CBS-QB3 calculations. The pathways have been obtained for the formation of the covalently bound HCN dimer, trimer, tetramer, and pentamer (adenine) by sequential additions of HCN or HNC. The activation energies of the individual oligomerization stages are a few hundred kilojoules per mole, which prevent efficient adenine synthesis in interstellar space or in the atmosphere of Titan. On the other hand, when the oligomerizations start from HCNH⁺, the activation energies of sequential HCN or HNC additions are significantly reduced. Kinetic analyses results suggest that adenine synthesis by proton-catalyzed oligomerizations cannot occur efficiently in interstellar space or in the atmosphere of Titan, even though some oligomerization stages can occur under the latter condition. Key Words: Prebiotic chemistry—Astrobiology—Chemical evolution—Titan—ISM chemistry. Astrobiology 13, 465–475.

1. Introduction

S tudies on the origin of life are as interesting as those for enhancing the quality of life. There is constant controversy about whether life developed on Earth or from extraterrestrial sources (Miller and Cleaves, 2007; Rehder, 2010). Prebiotic syntheses of nucleobases, amino acids, and carbohydrates have been extensively studied since Miller's experiment in 1953 (Miller, 1953). Oró (1960, 1961) reported that adenine (1), one of the nucleobases in RNA and DNA, could be formed by the oligomerization of hydrogen cyanide (HCN) under basic conditions. Because adenine, H₅C₅N₅, is formally a pentamer of HCN, it may be formed from HCN by oligomerization. Subsequent studies (Sanchez et al., 1966, 1967; Ferris et al., 1978; Voet and Schwartz, 1983; Levy et al., 2000; Hill and Orgel, 2002; Miyakawa et al., 2002; Borquez et al., 2005) have been performed to synthesize adenine from HCN under various different conditions, which have been well reviewed by several researchers (see, e.g., Ferris and Hagan, 1984; Orgel, 2004; Glaser et al., 2007).

Several mechanisms for prebiotic adenine synthesis have been proposed. The pathway in Scheme 1 has been accepted for the formation of adenine from five HCN molecules. It was reported that the tetramer, diaminomaleonitrile (DAMN, 12a), was readily formed and isolable at room temperature in aqueous solutions of 0.1–1.0 M HCN (Sanchez et al., 1967). However, the covalently bound dimer and trimer such as iminoacetonitrile (IAN, 2) and aminomalodinitrile (AMDN, 3) have not been isolated from aqueous HCN solutions. Theoretical investigations on the mechanisms of prebiotic adenine synthesis have been limited compared to numerous experimental studies. Partial mechanisms of the oligomerizations in Scheme 1 were investigated through quantum chemical calculations. Kikuchi et al. (2000) performed an ab initio study of the formation of 2 in aqueous solution. They demonstrated that the ammonia-catalyzed dimerization of HCN with the overall activation energy of 11.4 kcal mol⁻¹ was most efficient among their suggested pathways. Adenine synthesis from HCN may occur in the gas phase because HCN has been detected in interstellar clouds (Irvine, 1999), comets (Huebner et al., 1974; Schloerb et al., 1987), and the atmosphere of Titan (Hanel et al., 1981; Adriani et al., 2011), the largest moon of Saturn. Smith et al. (2001) located a transition state (TS) for the formation of (Z)-iminoformyl isocyanide ((Z)-HN=CHNC), an isomer of 2, which was 71 kcal mol⁻¹ above 2HCN. Kinetic estimations have indicated that the dimerization, stage I in Scheme 1, could not occur efficiently at low interstellar temperatures because of the high activation energy. Roy et al. (2007) proposed several mechanisms of the formation of 1 from 4-aminoimidazole-5-carbonitrile (AICN) and HCN (stage IV). They showed H₂O or NH₃ was needed as a catalyst to lower the reaction barriers. Glaser et al. (2007) proposed mechanisms of the pyrimidine-ring formation of isomeric monocyclic HCN pentamers with or without the aid of protons. Even though the reaction barrier was reduced by proton catalysis, it was predicted that the reaction was not efficient in interstellar space. As an alternative, they proposed that the isomerization could be accomplished with photoactivation. The latter two studies have given impetus to our examination on the mechanisms of adenine synthesis. As a first attempt, we proposed the mechanisms of the dimerization of HCN or HNC with and without the aid of protons (Yim and Choe, 2012). It was suggested that proton-catalyzed dimerizations substantially lower reaction barriers but cannot occur efficiently under interstellar conditions.

Scheme 1.

In this work, a complete theoretical mechanism of adenine synthesis (Scheme 1) from five HCN molecules in the gas phase is examined for the first time. The potential energy surfaces (PESs) for all stages in Scheme 1 were constructed from the complete basis set (CBS) QB3 (Montgomery et al., 1999) model calculations. As an alternative, a mechanism of adenine synthesis from five hydrogen isocyanide (HNC) molecules, instead of HCN, is examined because HNC is also observed in interstellar space (Wootten et al., 1978; Ohishi et al., 1992). As other alternatives, the proton-catalyzed pathway shown in Scheme 2 is examined together with the parallel pathway in which HNC is added sequentially instead of HCN. HCNH⁺ is also an interstellar gas (Ziurys and Turner, 1986; Ziurys et al., 1992) and can be produced from HCN or HNC in an acidic environment. The possibilities of adenine synthesis in interstellar space and in the atmosphere of Titan are discussed from kinetic analyses based on the obtained PESs.

Scheme 2.

2. Computational Methods

Molecular orbital calculations were performed with the Gaussian 09 suite of programs (Frisch et al., 2009). The geometries of the reactants, products, and intermediates were optimized at the B3LYP level of the density functional theory by using the 6-31G(d) basis. The TS geometries connecting the minima were examined and checked by calculating the intrinsic reaction coordinates at the same level. For better accuracy of the energies, CBS-QB3 model calculations (Montgomery et al., 1999) were performed, in which the geometries optimized at the B3LYP/6-31G(d) level were used for initial structures.

The Rice-Ramsperger-Kassel-Marcus (RRKM) (Marcus and Rice, 1951) and the quasi-equilibrium theory (Rosenstock et al., 1952) expression (Baer and Hase, 1996) was used to calculate the microcanonical rate constants for unimolecular reaction steps that were involved in selected reaction pathways: \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*}k (E) = \frac {\sigma N^{\ddag} (E - E_0)} {h \rho (E)} \tag {1} \end{align*} \end{document}

In this equation, E is the reactant internal energy, E ₀ is the activation energy of the reaction, N ^‡ is the sum of the TS states, ρ is the density of the reactant states, σ is the reaction path degeneracy, and h is Planck's constant. N^‡ and ρ were evaluated through a direct count of the states with the Beyer-Swinehart algorithm (Beyer and Swinehart, 1973). Each normal mode of vibration was treated as a harmonic oscillator. Because the geometries are optimized at the B3LYP/6-311G(2d,d,p) level in the CBS-QB3 method, the vibrational frequencies obtained at the same level were scaled down by a factor of 0.969 and were then used for the RRKM calculation. The scaling factor for the B3LYP/6-311G(2d,d,p) calculation has not been reported. Because the scaling factor reported for the B3LYP/6-311+G(2d,p) calculation is 0.9692, we used 0.969 for the B3LYP/6-311G(2d,d,p) calculation.

3. Results

The standard enthalpies and Gibbs energies of formation of selected species at 298 K, derived from CBS-QB3 calculations, are listed in Table 1 with the zero point corrected electronic energies at 0 K (see Supplementary Table S1 for all the optimized species; Supplementary Material is available at www.liebertonline.com/ast). A prerequisite for the occurrence of a bimolecular association reaction is that the reaction should be exothermic. All the examined oligomerization stages are exothermic as shown in Table 2.

Table 1.

The Zero Point Corrected Electronic Energy at 0 K, E _tot; the Standard Enthalpy of Formation at 298 K, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\Delta_{\rm f} H_{298}^{\circ}$$ \end{document} ; and the Standard Gibbs Energy of Formation at 298 K, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\Delta_{\rm f} G_{298}^{\circ}$$ \end{document} ; Derived from CBS-QB3 Calculations

Species		E_tot (hartrees)	\documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\Delta_{f} {\rm H}_{\it 298}^{\circ}$$ \end{document} (kJ mol ⁻¹)	\documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\Delta_{\it f} {\rm G}_{\it 298}^{\circ}$$ \end{document} (kJ mol ⁻¹)
HCN		−93.2875345	133	123
HNC		−93.2651185	193	181
(Z)-HN=CHCN	2a	−186.5824713	241	260
(E)-HN=CHCN	2b	−186.5813220	244	263
AMDN	3	−279.8955837	303	356
AICN(a)	4a	−373.2421706	274	371
AICN(b)	4b	−373.2462873	263	360
Adenine	1	−466.5959284	224	370
HNCH⁺		−93.5568065	950	958
(Z)-HN=CHCNH⁺	p2a	−186.8583354	1042	1078
(E)-HN=CHCNH⁺	p2b	−186.8650744	1024	1061
[AMDN]H⁺	p3	−280.1736215	1099	1168
[AICN(a)]H⁺	p4a	−373.5627634	957	1072
[AICN(b)]H⁺	p4b	−373.5623118	958	1074
N7-H⁺-adenine	p1a	−466.9374676	853	1015
N1-H⁺-adenine	p1b	−466.9504002	818	982

Table 2.

The Overall Activation Energy, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$E_{0}^{\rm OV}$$ \end{document} , and the Energy of the Product, ΔE, Relative to the Reactants Calculated from the CBS-QB3 Energies at 0 K

Reaction stage ^a	Product	\documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$E_{0}^{\rm OV}$$ \end{document}	ΔE	Reaction stage ^b	Product	\documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm E}_0^{OV}$$ \end{document}	ΔE
I	2a	295	−19	I_HNC	2a	171	−137
II	3	187	−67	II_HNC	3	125	−126
III	4a	252	−155	III_HNC	4a	197	−214
IV	1	231	−174	IV_HNC	1	199	−233
pI	p2a	13	−32	pI_HNC	p2a	0	−91
pII	p3	0	−73	pII_HNC	p3	0	−132
pIII	p4a	128	−267	pIII_HNC	p4a	69	−326
pIV	p1a	156	−229	pIV_HNC	p1b	110	−322

By HCN oligomerization.

By HNC oligomerization.

3.1. Neutral uncatalyzed pathway

3.1.1. Stage I: formation of IAN (2)

In our previous study (Yim and Choe, 2012), we found several pathways for the formation of 2 from two molecules of HCN or HNC. The lowest-energy pathway for the formation of the Z- and E-isomers of 2 (2a and 2b) by dimerization of HCN is shown in Fig. 1, which is derived from the CBS-QB3 zero point corrected electronic energies at 0 K. The highest barrier corresponds to the initial addition step 5→6 passing through a five-centered TS. The geometric structures and Cartesian coordinates of all the optimized species are provided in the Supplementary Material.

FIG. 1.

Potential energy diagram for the formation of 2 from HCN+HCN and from HNC+HNC (stages I and I_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to HNC+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

3.1.2. Stage II: formation of AMDN (3)

We found pathways for the addition of HCN to 2a or 2b. The addition to 2a is energetically more favored. After the formation of bimolecular complex 7, the H and CN moiety of HCN inserts into the HN=CH bond of 2a to form 8 (Fig. 2). A subsequent rearrangement of the C–N–C backbone to C–C–N leads to 3. The highest barrier, due to a five-centered TS (TS 7→8), lies 187 kJ mol⁻¹ above 2a+HCN. On the other hand, the addition to 2b requires passage of a four-centered TS lying at 309 kJ mol⁻¹ above 2b+HCN (not shown).

FIG. 2.

Potential energy diagram for the formation of 3 from 2a+HCN and from 2a+HNC (stages II and II_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to 2a+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

3.1.3. Stage III: formation of AICN (4)

We found several pathways for this stage but will focus on the lowest-energy pathway. It includes nine steps after the formation of bimolecular complex 9 (Fig. 3). The addition step, which is the rate-limiting step, requires passage of a five-centered TS to form a covalently bound HCN tetramer 10a. To form DAMN (12a), which is a well-characterized intermediate in prebiotic adenine synthesis, isomerization to rotamer 10b, rearrangement of the C–N–C sequence of 10b to C–C–N, and transfer of two hydrogens of 11 occur sequentially. After cis-trans isomerization to form diaminofumaronitrile (DAFN, 12b), the C–C–N backbone rearranges again to C–N–C to form 13. One may imagine an alternative route for the formation of 13 from 10a without such a rearrangement of the C–N–C sequence. We located a TS for the reaction 10a→13 through a 1,3-H shift, but it lay 113 kJ mol⁻¹ higher than the highest TS (TS 11→12a) in the pathway via 12a. A ring closure proceeds to form 4-amino-1H-imidazole-5-carbonitrile (AICN(b), 4b). Tautomerization occurs to form 5-amino-1H-imidazole-4-carbonitrile (AICN(a), 4a), 11 kJ mol⁻¹ less stable than 4b, through consecutive two 1,2-H shifts.

FIG. 3.

Potential energy diagram for the formation of 4 from 3+HCN and from 3+HNC (stages III and III_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to 3+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

3.1.4. Stage IV: formation of adenine (1)

Both the AICN tautomers, 4a and 4b, can form adenine by the addition of HCN. The formation of adenine starting from the less stable tautomer, 4a, has a lower overall reaction barrier. The HCN addition step 15→16a passing through a four-centered TS is the rate-limiting step (Fig. 4). After isomerizations to two rotamers (16b and 16c), (E)- and (Z)-5-(N′-formamidinyl)-1H-imidazole-4-carbonitrile (17a and 17b) are formed. The second ring closure occurs through a hydrogen shift from NH₂ to N of the nitrile group of 17b to lead to a tautomer of adenine with (Z)-imino form, 18a. After isomerization to its E-isomer 18b, adenine is finally formed.

FIG. 4.

Potential energy diagram for the formation of 1 from 4a+HCN and from 4a+HNC (stages IV and IV_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to 4a+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

When the reaction starts from 4b, the overall activation energy is 240 kJ mol⁻¹ (see Supplementary Fig. S1 for the PES), which is higher than that (231 kJ mol⁻¹) for the reaction starting from 4a. This suggests that its rate constant would be somewhat smaller than the reaction starting from 4a. On the other hand, 4b is 11 kJ mol⁻¹ more stable than 4a, indicating that the concentration of 4b is larger than 4a at equilibrium. Because the reaction rate is evaluated by multiplying the rate constant by the concentrations of reactants, the efficiency of both the reactions starting from 4a and 4b would be similar.

The overall activation energies of the pathways obtained for the four stages are summarized in Table 2 with the relative energies of the products. For all four stages, the rate-limiting steps are the HCN addition steps passing through four- or five-membered TSs with high energy demand.

3.1.5. By oligomerization of HNC

HNC is a potential candidate as a reactant in adenine synthesis because HNC is observed in meaningful quantities in interstellar space or in Titan's atmosphere despite HNC being less stable than HCN (see Table 1). The observed abundance ratios of HNC to HCN are generally high in cold, dark molecular clouds and in Titan's atmosphere. For example, the ratios are 1, 1.5, and 0.3 in TMC-1, L134N, and Titan, respectively (Ohishi et al., 1992; Moreno et al., 2011). Dissociative recombination of HCNH⁺ (Shiba et al., 1998; Talbi and Ellinger, 1998; Semaniak et al., 2001; Ngassam et al., 2005) and proton-assisted isomerization between HCN and HNC (Pichierri, 2002) have been proposed to explain the equal formation of the two isomers.

HNC may be used as a reactant instead of HCN at any stage in Scheme 1. We found an alternative pathway for adenine synthesis by oligomerization of five HNC molecules instead of five HCN molecules. 2a is formed from two HNC molecules via two bimolecular complexes 19 and 20 (Fig. 1). We will denote this stage as stage I_HNC and the other stages similarly. The third HNC is inserted into 2a to form 3 through a five-membered TS, TS 21→3 (Fig. 2). The fourth HNC is added to 3 through a five-membered TS to form 23, which isomerizes to 12b and then undergoes the same reaction steps to 4a as in stage III (Fig. 3). The final HNC is inserted into 4a through a four-membered TS and then isomerizes to the common intermediate 17b to eventually form adenine. The overall activation energy of each HNC oligomerization stage is lower than that of the corresponding HCN oligomerization stage, as shown in Table 2. However, the activation energies are still high for the reactions to occur efficiently in interstellar space, which will be described below.

3.2. Proton-catalyzed pathway

There are several possible pathways with proton catalysis. We chose the pathway in Scheme 2. Initially, HCN reacts with HCNH⁺ to form protonated IAN (p2), and three HCN molecules are added sequentially to eventually form N7-protonated adenine (p1a). Deprotonation of p1a may be achieved by dissociative recombination with an electron (Reaction 2) or by exothermic proton transfer to another molecule (M) (Reaction 3). \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} {\bf p1a} + {\rm e}^- \rightarrow {\bf 1} + {\rm H} \tag {2} \end{align*} \end{document} \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} {\bf p1a} + {\rm M} \rightarrow {\bf 1}+ {\rm MH}^+ \tag {3} \end{align*} \end{document}

3.2.1. Stage pI: formation of protonated IAN (p2)

Figure 5 shows the lowest-energy pathway for the formation of p2 from HCN+HCNH⁺, of which details were described previously (Yim and Choe, 2012). After the formation of ion-molecule complex p5, protonated (Z)-IAN, p2a, is formed. The overall activation energy is 13 kJ mol⁻¹, which is much lower than that (295 kJ mol⁻¹) for the formation of 2a by HCN dimerization. Further isomerization to the E-isomer, p2b, needs additional energy to overcome the barrier of 67 kJ mol⁻¹.

FIG. 5.

Potential energy diagram for the formation of p2 from HCNH⁺+HCN and from HCNH⁺+HNC (stages pI and pI_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to HCNH⁺+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

Alternatively, the covalent C–N bond may be formed between the HCNH⁺ and HCN moieties of p5, which results in protonated (E)-iminoformyl isocyanide ((E)-HN=CHNCH⁺). The TS for this step lies 17 kJ mol⁻¹ lower than that for the step p5→p2a. However, the isomerization of (E)-HN=CHNCH⁺ to p2a involves several hydrogen and skeletal rearrangements that require much higher energies (see Supplementary Fig. S2 for the PES). This pathway is much less favored than the direct pathway p5→p2a due to its high overall activation energy, 249 kJ mol⁻¹.

3.2.2. Stage pII: formation of protonated AMDN (p3)

Isomerizations to several ion-molecule complexes (p6a–p7c) occur before the formation of a C–C covalent bond between the added HCN and p2a (Fig. 6). There is no reaction barrier overall.

FIG. 6.

Potential energy diagram for the formation of p3 from p2a+HCN and from p2a+HNC (stages pII and pII_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to p2a+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

3.2.3. Stage pIII: formation of protonated AICN (p4)

We found several pathways for the formation of p4 from p3+HCN. The lowest-energy pathway is shown in Fig. 7. After the formation of ion-molecule complex p8, covalently bound pentamer p9 is formed with a barrier lying lower than the reactants. However, the subsequent reactions such as tautomerizations, rearrangements, and cyclizations, similar to those in stage III, require passage of high-lying TSs. Two protonated AICN isomers, p4a and p4b, are formed with almost the same stability.

FIG. 7.

Potential energy diagram for the formation of p4 from p3+HCN and from p3+HNC (stages pIII and pIII_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to p3+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

3.2.4. Stage pIV: formation of protonated adenine (p1)

Figure 8a shows the PES for the formation of p1a from p4a+HCN. Through three ion-molecule complexes, HCN is inserted into p4a to form p18a. This insertion step (p17b→p18a) passing through a four-centered TS that is similar to TS 15→16a is the rate-limiting step in stage pIV. The subsequent isomerizations are similar to those for stage IV. N1-protonated adenine (p1b), which is 34 kJ mol⁻¹ more stable than p1a, may be formed from p4b+HCN (see Supplementary Fig. S3), but this is less favored because the overall activation energy (216 kJ mol⁻¹) is much higher than that (156 kJ mol⁻¹) of the formation of p1a from p4a+HCN.

FIG. 8.

Potential energy diagrams (a) for the formation of p1a from p4a+HCN (stage pIV) and (b) for the formation of p1b from p4a+HNC (stage pIV_HNC), derived from CBS-QB3 calculations. The energies at 0 K are in kJ mol⁻¹, and those relative to p4a+HNC are in the brackets. Color images available online at www.liebertonline.com/ast

As summarized in Table 2, the proton catalysis substantially lowers the overall activation energies of all the oligomerization stages. In particular, those of the dimerization and trimerization are greatly lowered. The first steps in all the examined stages are the formation of bimolecular or ion-molecule complexes by association of reactants. The fact that the binding energies of the latter complexes are much larger than the former is one of the reasons for lowering of reaction barriers. The other is easier formation of covalent bonds in the proton-catalyzed pathways. The HCN addition steps in stages I and II, 5→6 and 7→8, require significant structure deformation and hence have high energy demand, while those in stages pI and pII, p5→p2a and p6a→p6b, do not. The HCN addition step in stage pIII occurs with similar ease, but the subsequent isomerizations have high energy demand. The second advantage, however, is not found in stage pIV where a four-centered TS should be passed for the addition of HCN as in stage IV.

3.2.5. By oligomerization of HNC

As in the neutral reactions, HNC may be used as a reactant instead of HCN at each stage in Scheme 2. The pathway for the formation of p2 from HCNH⁺+HNC (stage pI_HNC) was reported previously (Fig. 5) (Yim and Choe, 2012). All the TSs lie below the reactants. An alternative pathway for the formation of p2 after the initial formation of the covalent C–N bond between the HCNH⁺ and HNC moieties of p21, of which overall critical energy is 182 kJ mol⁻¹, is much less favored than the direct pathway p21→p2a (see Supplementary Fig. S2 for the PES).

The next HNC addition stage, stage pII_HNC, to form p3 is also a barrierless reaction (Fig. 6). After the formation of two ion-molecule complexes p22a and p22b, HNC is inserted into p2a to form p3 via common intermediate p7a. For the formation of p4, HNC is inserted into p3 via ion-molecule complex p23, and then p24 isomerizes to common intermediate p11 (Fig. 7). In the lowest-energy pathway obtained for the final HNC addition to p4a, similar to the pathway for stage pIV, N1-protonated adenine (p1b) is finally formed (Fig. 8b). As summarized in Table 2, the overall activation energies of all oligomerization stages pI–pIV are substantially lowered by replacing the neutral reactant with HNC.

4. Discussion

4.1. Is adenine synthesis possible in interstellar space?

We examined whether each oligomerization stage can efficiently occur in interstellar clouds such as TMC-1. For efficient thermal oligomerization of HCN or HNC in interstellar space, at least two requirements should be fulfilled. The first is that the overall activation energy should be near zero. Note that endothermic association reactions do not meet this requirement. Consider a proton-catalyzed oligomerization stage where an ion-molecule complex, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} , is initially formed by collision of the reactants A⁺ and B, and eventually forms the product P⁺: \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*}{\rm A}^+ + {\rm B} \, \mathop{\rightleftarrows}^{k_{\rm a}}_{k_d}{\rm A}^+ \cdots {\rm B} \mathop{\rightleftarrows}^{k_{\rm l}}{\rm C}^+ \rightleftarrows \rightleftarrows \rightleftarrows \,{\rm P}^+ \tag {4} \end{align*} \end{document}

Here, B is HCN or HNC; and k _a, k _d, and k ₁ are the rate constants for the reactions \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ + {\rm B} \rightarrow {\rm A}^+ \cdots {\rm B} , {\rm A}^+ \cdots {\rm B} \rightarrow {\rm A}^+ + {\rm B}$$ \end{document} and \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B} \rightarrow {\rm C}^+$$ \end{document} , respectively. Assume that the formation of P⁺ occurs by one step with the activation energy of E ₀: \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} k_{\rm f} \\ {\rm A}^+ + {\rm B} & \,\rightarrow \,{\rm P}^+ \tag{5} \end{align*} \end{document}

Then, the rate constant (k _f) would always be larger than the overall rate constant for Reaction 4 because the isomerization and dissociation steps in Reaction 4 decrease the overall reaction rate. When E ₀=0 as in stages pI_HNC, pII, and pII_HNC, a typical value of k _f for an ion-molecule reaction is 1×10⁻⁹ cm³ molecule⁻¹ s⁻¹ (Herbst, 2001). The bimolecular reaction becomes a pseudo first-order reaction for A⁺ when the number density of B, [B], is much larger than [A⁺]. The number density of HCN observed in TMC-1 is the same as that of HNC, which is 2×10⁻⁴ molecule cm⁻³ accepting [H₂]=1×10⁴ molecule cm⁻³ (Wootten et al., 1978; Ohishi et al., 1992). Then, the rate constant (k′) for the pseudo first-order reaction is k _f [HCN] or k _f [HNC]=2×10⁻¹³ s⁻¹, and the half lifetime of A⁺, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\tau_{{\rm A}^+}$$ \end{document} ln2/k′, against the formation of P⁺ is estimated to be 1×10⁵ yr, which is within the timescale of chemical revolution of typical dense interstellar clouds, 10⁶ yr. However, when E ₀ is greater than 0, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\tau_{{\rm A}^+}$$ \end{document} increases rapidly with increasing E ₀. Assuming that k _f obeys the Arrhenius law, the exponential factor becomes 6×10⁻⁶ even when E ₀=1 kJ mol⁻¹ at 10 K, a typical temperature of dense clouds such as TMC-1 (Henkel et al., 1981). An estimate of \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\tau_{{\rm A}^+}$$ \end{document} is 2×10¹⁰ yr. At 100 K, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\tau_{{\rm A}^+}$$ \end{document} is estimated to be 4×10⁵. When E ₀=10 kJ mol⁻¹, the values for \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$$\tau_{{\rm A}^+}$$ \end{document} are estimated to be 2×10⁵⁷ and 2×10¹⁰ yr at 10 and 100 K, respectively. This indicates that the overall activation energy should be smaller than a few kilojoules per mole for a proton-catalyzed HCN or HNC oligomerization to occur efficiently in interstellar space at 10–100 K even when we assume a one-step reaction. Because a typical value of k _f for a neutral-neutral reaction is 10–100 times smaller than typical k _f values for ion-molecule reactions when E ₀=0 (Herbst, 2001), this first requirement should also be fulfilled for any uncatalyzed oligomerization stage to occur. However, the overall activation energies for the uncatalyzed oligomerization stages are all a few hundred kilojoules per mole. Only three proton-catalyzed oligomerization stages, pI_HNC, pII, and pII_HNC, meet the first requirement.

The next requirement is that after the formation of \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} , the forward reactions to P⁺ in Reaction 4 should be faster than or at least compete with dissociation or reverse isomerization steps. Otherwise, no meaningful quantity of P⁺ would be formed. First of all, the vibrationally excited complex \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} , p21, p6a, or p22a in stages pI_HNC, pII, or pII_HNC, respectively, should undergo the isomerization to C⁺ efficiently (Figs. 6 and 7). We estimated k ₁ and k _d for p6a, p21, or p22a by using the RRKM formalism (Eq. 1). The calculations were performed at the zero energy of reactants (A⁺+B) because the internal energies of the reactants at 10–100 K are negligible compared to the internal energies of \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} and its isomers possessed after their formation. The k ₁/k _d ratios in stages pI_HNC, pII, and pII_HNC were calculated as 4×10⁵, 2×10⁶, and 1×10⁷, respectively. This indicates that the isomerizations ( \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B} \rightarrow {\rm C}^+$$ \end{document} ) occur much faster than the dissociations ( \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B} \rightarrow {\rm A}^+ + {\rm B}^+$$ \end{document} ) when we ignore the deactivation of \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} by collision or by radiation. The calculated k ₁ values are 9.7×10¹⁰, 2.3×10⁸, and 2.3×10⁸ for stages pI_HNC, pII, and pII_HNC, respectively. The collisional relaxation of \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} or other intermediates would be negligible compared to such isomerizations in interstellar space considering low gas densities. Assuming that the collisional rate constant of 1×10⁻⁹ cm³ molecule⁻¹ s⁻¹ and a gas density of 10⁴ to 10⁶ molecule cm⁻³ (Herbst, 2001), the collision frequency is 10⁻⁵ to 10⁻³ s⁻¹, which is much smaller than the rate constants for the isomerizations in stages pI_HNC, pII, and pII_HNC. Radiative decay of the vibrationally excited complex \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} or other intermediates would be negligible also because most of the reported IR radiative decay rate constants are smaller than 10³ s⁻¹ (Herbst, 1985; Gerlich and Horning, 1992; Dunbar et al., 1996; Petrie and Dunbar, 2000; Smith et al., 2001), also much smaller than the isomerization rate constants. This suggests that the several isomers would be interconvertible rapidly after the formation of \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} without loss of the excess energy.

Secondly, the concentration of the final product P⁺ should be enough at equilibrium to undergo a further HCN (or HNC) addition. This is well satisfied when P⁺ is the most stable among its isomers in the reaction pathway. No pathway for stages pI_HNC, pII, and pII_HNC meets this requirement. The most stable isomers in those pathways are p5, p6b, and p6b, respectively (Figs. 6 and 7). In stage pI_HNC, p5 is 53 kJ mol⁻¹ more stable than p2a. In stages pII and pII_HNC, p6b is 54 kJ mol⁻¹ more stable than p3. The relative concentration at equilibrium could be estimated from the densities of states of the isomers. At the zero energy of the reactants (HCNH⁺+HNC), the [p2a]_eq/[p5]_eq ratio is estimated to be 9.7×10⁻⁵ in stage pI_HNC. This indicates that only a tiny quantity of p2a is finally formed even though the association reaction between HCNH⁺ and HNC occurs successfully. Furthermore, p5 would dissociate to HCNH⁺+HCN rapidly before the backward isomerization to p2a. Comparing the RRKM rate constants for the dissociation and isomerization, 2.9×10⁻³ of p5 would isomerize to p2a at the same energy. Then, only 2.8×10⁻⁷ of p2a formed by the association of HCNH⁺ and HNC would survive at equilibrium even though we ignore the concentrations of p2b and p21. Then, the lifetime of HCNH⁺ against the formation of p2a along stage pI_HNC is estimated to be larger than 5×10¹¹ yr in TMC-1 with use of the k _a value (1×10⁻⁹ cm³ molecule⁻¹ s⁻¹) estimated previously (Yim and Choe, 2012). In stages pII and pII_HNC, other intermediates as well as p6b are more stable than p3 (Fig. 6). Considering all the intermediates, the quantity of p3 formed at equilibrium is 1.8×10⁻⁴ and 6.7×10⁻⁴ of the H₃C₃N₃ isomers at the zero energies of p2a+HCN and p2a+HNC, respectively. In this case, the isomerization rates are faster than the rate for back dissociations to pairs of ion and molecule. Then, the τ_p2a values against the formation of p3 along stages pII and pII_HNC are estimated to be ∼6×10⁸ and ∼2×10⁸ yr in TMC-1, respectively. Therefore, it is concluded that any oligomerization stage cannot occur efficiently in interstellar space.

4.2. Is adenine synthesis possible in Titan?

The above analysis shows that the number density of HCN or HNC is an important factor in the oligomerization kinetics. HCN is observed in high quantities in the atmosphere of Titan (Yelle and Griffith, 2003; Kim et al., 2005; Adriani et al., 2011). HNC was detected very recently (Moreno et al., 2011) in the upper thermosphere (∼1000 km) of Titan with the relative abundance [HNC]/[HCN]≈0.3. It was suggested that HNC is formed at the ionosphere levels from dissociative recombination of HCNH⁺ and other heavier nitrile ions (Moreno et al., 2011). Interestingly, Hörst et al. (2012) and Pilling et al. (2009) reported successful adenine synthesis in analogues to Titan's atmosphere. At the altitude of 1000 km, the observed number density of HCN is ∼10⁸ molecule cm⁻³ (Yelle and Griffith, 2003; Kim et al., 2005; Adriani et al., 2011), which is ∼5×10¹¹ times larger than that in TMC-1, and the temperature is ∼160 K (Lellouch et al., 1990). It is predicted that the lifetime of A⁺ in such a condition is ∼5×10¹¹ or ∼1.5×10¹¹ times shorter than that in TMC-1 when B is HCN or HNC, respectively. Because the number density of the atmospheric constituents at the altitude of 1000 km is around 10¹⁰ molecule cm⁻³ (Friedson and Yung, 1984; Adriani et al., 2011), the collisional relaxation of \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm A}^+ \cdots {\rm B}$$ \end{document} or other intermediates hardly competes with their isomerizations as in TMC-1. Thus, the estimated half lifetime of HCNH⁺ against the formation of p2a along stage pI_HNC is ∼3 yr, and those of p2a against the formation of 3 along stages pII and pII_HNC are both ∼9 h.

Stage pI has the lowest activation energy, 13 kJ mol⁻¹, among the stages with activation energy. Assuming that stage pI occurs by one step as Reaction 5, k _f is estimated to be 5.7×10⁻¹⁴ cm³ molecule⁻¹ s⁻¹ when using the Arrhenius law. Then, the half lifetime of HCNH⁺ against the formation of p2 along stage pI in the thermosphere of Titan is 3×10¹ h considering the number density of HCN, ∼10⁸ molecule cm⁻³. However, most of the formed p2 ions dissociate to HCNH⁺+HCN as in stage pI_HNC. According to the RRKM calculations at the reactants' energy of 13 kJ mol⁻¹, 1×10⁻⁸ of the \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document}$${\rm C}_2 {\rm H}_2 {\rm N}_2^+$$ \end{document} isomers would survive as p2. Then, the lifetime increases to ∼3×10⁵ yr. The reaction times for the other stages with higher activation energies were estimated to be much longer than the age of the Universe. Therefore, it is predicted that stages pI_HNC, pII, and pII_HNC can occur efficiently, and stage I can occur more slowly in the thermosphere of Titan.

5. Conclusion

The complete mechanisms of adenine synthesis by oligomerizations of HCN or HNC are proposed for the first time by construction of the PESs with CBS-QB3 calculations. The sequential HCN or HNC addition stages require high energies, so any oligomerization stage cannot occur efficiently in interstellar space or in the atmosphere of Titan. When the dimerization starts from HCNH⁺+HCN or HCNH⁺+HNC, the barriers for the dimerization and for subsequent HCN or HNC addition stages are significantly reduced. Results of kinetic analyses show that no proton-catalyzed HCN or HNC oligomerization stage can occur efficiently in interstellar space, whereas the formation of the protonated HCN trimer, p3, by sequential HCN or HNC additions to HCNH⁺ is possible in the upper atmosphere of Titan. However, even on Titan, where the concentrations of HCN and HNC are high, it is predicted that adenine synthesis with the aid of protons is not efficient due to high activation barriers for the tetramerization and pentamerization stages. This suggests that prebiotic adenine synthesis must have occurred under other conditions or by other means. Even though the proposed mechanisms are inadequate for prebiotic adenine synthesis, they can serve as the prototype for further investigations on the mechanisms of adenine synthesis with other catalysts or in other phases.

Footnotes

Acknowledgments

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2010-0008287). The authors thank Eun Ji Lee for assistance with computations.

Author Disclosure Statement

No competing financial interests exist.

Supplementary Material

Thermochemical data, geometric structures, and Cartesian coordinates of optimized species and potential energy diagrams are found in the Supplementary Material.

Abbreviations

AICN, 4-aminoimidazole-5-carbonitrile; AICN(a), 5-amino-1H-imidazole-4-carbonitrile; AICN(b), 4-amino-1H-imidazole-5-carbonitrile; AMDN, aminomalodinitrile; CBS, complete basis set; DAFN, diaminofumaronitrile; DAMN, diaminomaleonitrile; IAN, iminoacetonitrile; PES, potential energy surface; RRKM, Rice-Ramsperger-Kassel-Marcus; TS, transition state.

References

Adriani

, Dinelli

B.M.

, López-Puertas

, García-Comas

, Moriconi

M.L.

, D'Aversa

, Funke

, Coradini

2011. Distribution of HCN in Titan's upper atmosphere from Cassini/VIMS observations at 3 μm. Icarus, 214:584–595.

Baer

, Hase

W.L.

1996. Unimolecular Reaction Dynamics: Theory and Experiments. Oxford University Press: New York.

Beyer

, Swinehart

D.R.

1973. Algorithm 448: number of multiply restricted partitions. Commun ACM, 16:379.

Borquez

, Cleaves

H.J.

, Lazcano

, Miller

S.L.

2005. An investigation of prebiotic purine synthesis from the hydrolysis of HCN polymers. Orig Life Evol Biosph, 35:79–90.

Dunbar

R.C.

, Klippenstein

S.J.

, Hrušák

, Stöckigt

, Schwarz

1996. Binding energy of Al(C₆H₆)⁺ from analysis of radiative association kinetics. J Am Chem Soc, 118:5277–5283.

Ferris

J.P.

, Hagan

W.J.

Jr.

1984. HCN and chemical evolution: the possible role of cyano compounds in prebiotic synthesis. Tetrahedron, 40:1093–1120.

Ferris

J.P.

, Joshi

P.C.

, Edelson

E.H.

, Lawless

J.G.

1978. HCN: a plausible source of purines, pyrimidines and amino acids on the primitive Earth. J Mol Evol, 11:293–311.

Friedson

A.J.

, Yung

Y.L.

1984. The thermosphere of Titan. J Geophys Res, 89:85–90.

Frisch

M.J.

, Trucks

G.W.

, Schlegel

H.B.

, Scuseria

G.E.

, Robb

M.A.

, Cheeseman

J.R.

, Scalmani

, Barone

, Mennucci

, Petersson

G.A.

, Nakatsuji

, Caricato

, Li

, Hratchian

H.P.

, Izmaylov

A.F.

, Bloino

, Zheng

, Sonnenberg

J.L.

, Hada

, Ehara

, Toyota

, Fukuda

, Hasegawa

, Ishida

, Nakajima

, Honda

, Kitao

, Nakai

, Vreven

, Montgomery

J.A.

Jr. , Peralta

J.E.

, Ogliaro

, Bearpark

, Heyd

J.J.

, Brothers

, Kudin

K.N.

, Staroverov

V.N.

, Kobayashi

, Normand

, Raghavachari

, Rendell

, Burant

J.C.

, Iyengar

S.S.

, Tomasi

, Cossi

, Rega

, Millam

N.J.

, Klene

, Knox

J.E.

, Cross

J.B.

, Bakken

, Adamo

, Jaramillo

, Gomperts

, Stratmann

R.E.

, Yazyev

, Austin

A.J.

, Cammi

, Pomelli

, Ochterski

J.W.

, Martin

R.L.

, Morokuma

, Zakrzewski

V.G.

, Voth

G.A.

, Salvador

, Dannenberg

J.J.

, Dapprich

, Daniels

A.D.

, Farkas

Ö.

, Foresman

J.B.

, Ortiz

J.V.

, Cioslowski

, Fox

D.J.

2009Gaussian 09, revision A.02Gaussian, Inc.: Wallingford, CT.

10.

Gerlich

, Horning

1992. Experimental investigation of radiative association processes as related to interstellar chemistry. Chem Rev, 92:1509–1539.

11.

Glaser

, Hodgen

, Farrelly

, McKee

2007. Adenine synthesis in interstellar space: mechanisms of prebiotic pyrimidine-ring formation of monocyclic HCN-pentamers. Astrobiology, 7:455–470.

12.

Hörst

S.M.

, Yelle

R.V.

, Buch

, Carrasco

, Cernogora

, Dutuit

, Quirico

, Sciamma-O'Brien

, Smith

M.A.

, Somogyi

Á.

, Szopa

, Thissen

, Vuitton

2012. Formation of amino acids and nucleotide bases in a Titan atmosphere simulation experiment. Astrobiology, 12:809–817.

13.

Hanel

, Conrath

, Flasar

F.M.

, Kunde

, Maguire

, Pearl

, Pirraglia

, Samuelson

, Herath

, Allison

1981. Infrared observations of the saturnian system from Voyager 1. Science, 212:192–200.

14.

Henkel

, Wilson

T.L.

, Pankonin

1981. H₂CO and CO observations of TMC1. Astron Astrophys, 99:270–273.

15.

Herbst

1985. An update of and suggested increase in calculated radiative association rate coefficients. Astrophys J, 291:226–229.

16.

Herbst

2001. The chemistry of interstellar space. Chem Soc Rev, 30:168–176.

17.

Hill

, Orgel

L.E.

2002. Synthesis of adenine from HCN tetramer and ammonium formate. Orig Life Evol Biosph, 32:99–102.

18.

Huebner

W.F.

, Snyder

L.E.

, Buhl

1974. HCN radio emission from Comet Kohoutek (1973f) Icarus, 23:580–584.

19.

Irvine

W.M.

1999. The composition of interstellar molecular clouds. Space Sci Rev, 90:203–218.

20.

Kikuchi

, Watanabe

, Satoh

, Inadomi

2000. Ab initio GB study of prebiotic synthesis of purine precursors from aqueous hydrogen cyanide: dimerization reaction of HCN in aqueous solution. Theochem, 507:53–62.

21.

Kim

S.J.

, Geballe

T.R.

, Noll

K.S.

, Courtin

2005. Clouds, haze, and CH₄, CH₃D, HCN, and C₂H₂ in the atmosphere of Titan probed via 3 μm spectroscopy. Icarus, 173:522–532.

22.

Lellouch

, Hunten

D.M.

, Kockarts

, Coustenis

1990. Titan's thermosphere profile. Icarus, 83:308–324.

23.

Levy

, Miller

S.L.

, Brinton

, Bada

J.L.

2000. Prebiotic synthesis of adenine and amino acids under Europa-like conditions. Icarus, 145:609–613.

24.

Marcus

R.A.

, Rice

O.K.

1951. The kinetics of the recombination of methyl radicals and iodine atoms. J Phys Colloid Chem, 55:894–908.

25.

Miller

S.L.

1953. A production of amino acids under possible primitive Earth conditions. Science, 117:528–529.

26.

Miller

S.L.

, Cleaves

H.J.

2007. Prebiotic chemistry on the primitive Earth. Systems Biology: Vol.1: Genomics. Rigoutsos

, Stephanopouloss

Oxford University Press: New York, 3–56.

27.

Miyakawa

, Cleaves

H.J.

, Miller

S.L.

2002. The cold origin of life: B. Implications based on pyrimidines and purines produced from frozen ammonium cyanide solutions. Orig Life Evol Biosph, 32:209–218.

28.

Montgomery

J.A.

Jr. , Frisch

M.J.

, Ochterski

J.W.

, Petersson

G.A.

1999. A complete basis set model chemistry. VI. Use of density functional geometries and frequencies. J Chem Phys, 110:2822–2827.

29.

Moreno

, Lellouch

, Lara

L.M.

, Courtin

, Bockelée-Morvan

, Hartogh

, Rengel

, Biver

, Banaszkiewicz

, González

2011. First detection of hydrogen isocyanide (HNC) in Titan's atmosphere. Astron Astrophys, 536:L12.

30.

Ngassam

, Orel

A.E.

, Suzor-Weiner

2005. Ab initio study of the dissociative recombination of HCNH⁺ J Phys Conf Ser, 4:224–228.

31.

Ohishi

, Irvine

W.M.

, Kaifu

1992. Molecular abundance variations among and within cold, dark molecular clouds. Astrochemistry of Cosmic PhenomenaIAU Symposium 150 Singh

P.D.

Kluwer Academic Publishers: Dordrecht.

32.

Oró

1960. Synthesis of adenine from ammonium cyanide. Biochem Biophys Res Commun, 2:407–412.

33.

Oró

1961. Mechanism of synthesis of adenine from hydrogen cyanide under possible primitive Earth conditions. Nature, 191:1193–1194.

34.

Orgel

L.E.

2004. Prebiotic chemistry and the origin of the RNA world. Crit Rev Biochem Mol Biol, 39:99–123.

35.

Petrie

, Dunbar

R.C.

2000. Radiative association reactions of Na⁺, Mg⁺, and Al⁺ with abundant interstellar molecules. Variational transition state theory calculations. J Phys Chem A, 104:4480–4488.

36.

Pichierri

2002. Theoretical study of the proton exchange reaction: HCNH⁺+HCN↔HNC+HCNH⁺ Chem Phys Lett, 353:383–388.

37.

Pilling

, Andrade

D.P.P.

, Neto

A.C.

, Rittner

, Naves de Brito

2009. DNA nucleobase synthesis at Titan atmosphere analog by soft X-rays. J Phys Chem A, 113:11161–11166.

38.

Rehder

2010. Chemisty in Space: From Interstellar Matter to the Origin of Life. Wiley-VCH, Weinheim.

39.

Rosenstock

H.M.

, Wallenstein

M.B.

, Wahrhaftig

A.L.

, Eyring

1952. Absolute rate theory for isolated systems and the mass spectra of polyatomic molecules. Proc Natl Acad Sci USA, 38:667–678.

40.

Roy

, Najafian

, von Ragué Schleyer

2007. Chemical evolution: the mechanism of the formation of adenine under prebiotic conditions. Proc Natl Acad Sci USA, 104:17272–17277.

41.

Sanchez

, Ferris

, Orgel

L.E.

1966. Conditions for purine synthesis: did prebiotic synthesis occur at low temperatures? Science, 153:72–73.

42.

Sanchez

R.A.

, Ferbis

J.P.

, Orgel

L.E.

1967. Studies in prebiotic synthesis: II. Synthesis of purine precursors and amino acids from aqueous hydrogen cyanide. J Mol Biol, 30:223–253.

43.

Schloerb

F.P.

, Kinzel

W.M.

, Swade

D.A.

, Irvine

W.M.

1987. Observations of HCN in comet P/Halley. Astron Astrophys, 187:475–480.

44.

Semaniak

, Minaev

B.F.

, Derkatch

A.M.

, Hellberg

, Neau

, Rosén

, Thomas

, Larsson

, Danared

, Paál

, af Ugglas

2001. Dissociative recombination of HCNH⁺: absolute cross sections and branching ratios. Astrophys J Suppl Ser, 135:275–283.

45.

Shiba

, Hirano

, Nagashima

, Ishii

1998. Potential energy surfaces and branching ratio of the dissociative recombination reaction HCNH⁺+e^-: an ab initio molecular orbital study. J Chem Phys, 108:698–705.

46.

Smith

I.W.M.

, Talbi

, Herbst

2001. The production of HCN dimer and more complex oligomers in dense interstellar clouds. Astron Astrophys, 369:611–615.

47.

Talbi

, Ellinger

1998. Potential energy surfaces for the electronic dissociative recombination of HCNH⁺: astrophysical implications on the HCN/HNC abundance ratio. Chem Phys Lett, 288:155–164.

48.

Voet

A.B.

, Schwartz

A.W.

1983. Prebiotic adenine synthesis from HCN—evidence for a newly discovered major pathway. Bioorg Chem, 12:8–17.

49.

Wootten

, Evans

N.J.

, Snell

, Bout

P.V.

1978. Molecular abundance variations in interstellar clouds. Astrophys J, 225:L143–L148.

50.

Yelle

R.V.

, Griffith

C.A.

2003. HCN fluorescence on Titan. Icarus, 166:107–115.

51.

Yim

M.K.

, Choe

J.C.

2012. Dimerization of HCN in the gas phase: a theoretical mechanistic study. Chem Phys Lett, 538:24–28.

52.

Ziurys

L.M.

, Turner

B.E.

1986. HCNH⁺: a new interstellar molecular ion. Astrophys J, 302:L31–L36.

53.

Ziurys

L.M.

, Apponi

A.J.

, Yoder

J.T.

1992. Detection of the quadrupole hyperfine structure in HCNH⁺ Astrophys J, 397:L123–L126.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

3.53 MB