Gas-Phase Reactions of Deprotonated Nucleobases with H, N, and OAtomsCharles M. Nichols,‡ Zhe-Chen Wang,§ W. Carl Lineberger, and Veronica M. Bierbaum*

Department of Chemistry and JILA, University of Colorado, Boulder, Colorado 80309, United States

*S Supporting Information

ABSTRACT: Complex organic molecules, the hallmark ofterrestrial life, are increasingly detected in exotic environmentsthroughout the universe. Our studies probe the ion chemistryof these biomolecules. We report gas-phase reaction rateconstants for five deprotonated nucleobases (adenine,cytosine, guanine, thymine, and uracil) reacting with theatomic species H, N, and O. Hydrogen atoms react atmoderate rates via associative electron detachment. Oxygenatom reactions occur more rapidly, generating complexproduct distributions; reaction pathways include associativeelectron detachment, substitution of the hydrogen atom by anoxygen atom, and generation of OCN−. Nitrogen atoms donot react with the nucleobase anions. The reactionthermodynamics were investigated computationally, and reported product channels are exothermic. Many of the proposedproducts have been observed in various astrochemical environments. These reactions provide insight into chemical processesthat may occur at the boundaries between diffuse and dense interstellar clouds and in complex extraterrestrial ionospheres.

The purine nucleobases (adenine and guanine) and thepyrimidine nucleobases (cytosine, thymine, and uracil)

are essential subunits of deoxyribonucleic acid and ribonucleicacid (DNA and RNA); as such, they are critical to thechemistry of life on Earth. The origin of the nucleobases andother biomolecules remains an area of intense interest andresearch. However, the detection of nucleobases in comets1

and meteorites,2,3 as well as their extraterrestrial isotopicabundances,4 supports the hypothesis of their exogenousproduction and delivery to early Earth. Moreover, nucleobasesand their precursors may exist in other environments withinour solar system, including the atmosphere of Titan, Saturn’slargest moon. The recently concluded Cassini−Huygensmission to Titan revealed the presence of complex carbonand nitrogen-containing molecules, as well as positive andnegative ions;5,6 moreover, experimental studies of theirradiation of a simulated Titan atmosphere demonstrate theformation of nucleobases.7

The interstellar medium is home to a wide array of organicmolecules; polycyclic aromatic hydrocarbons (PAHs) andnitrogen-containing polycyclic aromatic hydrocarbons(PANHs) are the likely sources of ubiquitous infraredemissions,8,9 and C60

+ has recently been identified as the firstcarrier10,11 of the Diffuse Interstellar Bands, whose origins haveeluded astronomers for almost a century. Dark molecularclouds are especially intriguing, as the birthplace of both starsand planets but also as reservoirs of exotic species and chemicalprocesses. In these interstellar clouds, about 200 molecules,cations, and anions have been detected.12 These species rangefrom simple diatomics to complex polyatomic molecules that

represent many functional groups, including alcohols, acids,amines, ketones, aldehydes, esters, ethers, and nitriles.Although nucleobases have not yet been observed in theinterstellar medium, many complex molecules includingpossible biomolecule precursor compounds containing carbon,hydrogen, nitrogen, and oxygen are present in abundance.Our experimental studies have focused on characterizing the

structures, energies, fragmentations, and reactions of inter-stellar species with H, N, and O atoms, which are among themost abundant atomic species in the universe, in order tounderstand the synthesis and destruction mechanisms ofastrochemical processes.13 Our recent work has involvednitrogen-containing negative ions, for which laboratory resultsare lacking, including cyanoacetylene,14 cyanate,15 dicyanamideanions,16 azoles,17−19 azines,20,21 and amino acids.22 Ourrecent development16 of an electrospray ionization source(ESI)23,24 for the selected ion flow tube (SIFT) has enabledour first experimental studies of the reactions of nucleobaseanions with atomic reactants. This Letter reports our findingsthat these relatively robust ions undergo efficient andintriguing reactions with hydrogen and oxygen atoms.The SIFT technique, which has been described in detail

previously,25,26 allows quantitative kinetic measurements,including rate constants and product distributions, for a widevariety of ions reacting with neutral reagents. Figure 1 shows

Received: July 10, 2019Accepted: August 5, 2019Published: August 13, 2019

Letter

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the incorporation of a newly designed ESI source that allowsproduction of the deprotonated nucleobases: adenine,cytosine, guanine, thymine, and uracil (Figure 2). The neutral

nucleotide bases were obtained commercially as powders fromSigma-Aldrich and diluted in HPLC-grade acetonitrile to afinal concentration of ∼5 × 10−6 M. To promote solubility anddeprotonation of the nucleobases, reagent-grade sodiumhydroxide was added to the solution in a 1:1 molar ratio(nucleobase:NaOH). The acetonitrile solution was theninfused through a heated capillary at a flow rate of ∼1−10μL min−1 using a syringe pump; ions were extracted at highpotential and concentrated by an ion funnel.27 The desirednucleobase anions were mass-selected with the SIFT quadru-pole mass filter and injected into the reaction flow tube, wherethey were entrained in helium carrier gas (UHP, 99.999%,Airgas). The ions underwent thousands of collisions withhelium before undergoing reaction with added neutrals; thus,this technique provides a stable, continuous flow ofdeprotonated nucleobases for kinetic measurements at thermalenergy.The H, N, and O atoms are generated downstream using a

microwave discharge coupled to the reaction flow tube (Figure1). This technique is well described in the general literature28

and thoroughly characterized in our previous papers.20 Toform H atoms, purified molecular hydrogen is passed throughan Evenson cavity supplied with 50 W of microwave radiation;the H2 flow is regulated with a metering valve and monitoredwith a flow meter. The reaction rate constants between thedeprotonated nucleobases and H atoms are measured relative

Figure 1. Electrospray ionization-selected ion flow tube with amicrowave discharge atom source.

Figure 2. Five nucleobases deprotonated at the most acidic site.

Table 1. Reaction Rate Constants and Product Distributions for H and O Atom Reactions with the Deprotonated Nucleobases

X− + 2H X− + 3O

deprotonatednucleobasea

kexptb

(10−11 cm3/s)ΔrH theoryc

(kcal/mol)kexpt

d

(10−11 cm3/s) AEDeproduction m/z proposed productsf distributiong

ΔrH theoryc

(kcal/mol)

adenine C5H4N5−

m/z 1344.9 (1.9) −20.5 26.1 (5.2) 0.2 42 OCN− + 4HCN 0.10 −15.1

80 C3H2N3− + HNCO + HCN 0.20 −10.4

96 C3H2N3O− + 2HCN 0.10 −44.7

107 C4H3N4− + HNCO 0.10 −67.9

123 C4H3N4O− + HCN 0.35 −65.8

149 2C5H3N5O− + 2H 0.15 −30.0

cytosine C4H4N3O−

m/z 11023.6 (1.9) −23.2 39.0 (4.1) 0.7 42 OCN− + 2HCN + H2CO 0.15 −34.4

97 2C3H3N3O− + 2H + CO 0.25 −6.8

125 2C4H3N3O2− + 2H 0.60 −38.0

guanine C5H4N5O−

m/z 1504.9 (1.4) −18.9 48.1 (6.2) 0.6 26 CN− + 2HNCO + 2HCN 0.20 −19.7

42 OCN− + HNCO + 3HCN 0.15 −27.969 C2HN2O

− + HNCO + 2HCN 0.20 −46.896 C3H2N3O

− + HNCO + HCN 0.15 −69.5123 C4H3N4O

− + HNCO 0.15 −44.1165 2C5H3N5O2

− + 2H 0.15 −37.3thymine C5H5N2O2

−

m/z 1255.1 (1.6) −18.3 29.7 (5.5) 0.4 42 OCN− + HNCO + C2H4 + CO 0.45 −47.6

70 C3H4NO− + HNCO + CO 0.10 −37.3

98 C4H4NO2− + HNCO 0.25 −48.2

140 2C5H4N2O3− + 2H 0.20 −28.1

uracil C4H3N2O2−

m/z 1115.2 (1.6) −16.0 19.1 (9.1) 0.7 42 OCN− + C2H2O + HNCO 0.20 −54.9

84 C3H2NO2− + HNCO 0.15 −83.3

98 2C3H2N2O2− + 2H + CO 0.10 −12.0

126 2C4H2N2O3− + 2H 0.55 −30.3

aDeprotonation assumed to occur at the most acidic site.31 bH-atom rate constants are measured relative to the reaction Cl− + H, krxn = 9.6 × 10−10

cm3 s−1.29 The values in parentheses indicate one standard deviation of the mean (σ) of 15 or more measurements. cTheoretical energies arecomputed with the B3LYP/6-311++G(d,p) level of theory and reported at T = 298 K by including thermal corrections under the rigid rotor−harmonic oscillator approximation. dO-atom rate constants are measured using a gas-phase titration as described previously.20 The values inparentheses indicate one standard deviation of the mean (σ) of nine or more measurements. eAssociative electron detachment distribution for O-atom reactions. fThe spin state is a singlet unless indicated with a superscript 2 for a doublet. gIonic product distributions are determined bymonitoring the relative intensities of each product ion.

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to the well-characterized reaction29 between H and Cl−, whichoccurs exclusively through associative electron detachment, H+ Cl− → HCl + e−, with a rate constant of kexp = 9.6 × 10−10

cm3 s−1. For these studies, reagent-grade NaCl is added to theESI acetonitrile solution in a 1:1:1 molar ratio (nucleobase:NaOH:NaCl), and the SIFT quadrupole is set to transmit allmasses in order to simultaneously introduce Cl− and thedeprotonated nucleobase, X−, into the reaction flow tube. Thedepletions of both Cl− and X− are monitored with thedownstream triple-quadrupole mass analyzer, allowing arelative rate constant for X− + H to be determined. N atomsare generated by passing molecular nitrogen through themicrowave discharge. O atoms are formed by introducing NO(4% in He, Matheson) immediately downstream of thedischarge to initiate the reaction N + NO → N2 + O. Thistitration allows the determination of nitrogen and oxygen atomconcentrations as a function of NO flow.The deprotonated nucleobases were found to be unreactive

with H2, N2, and N atoms. However, all five nucleobase anionsreacted readily with H atoms and O atoms; the reaction rateconstants and product distributions were measured and aresummarized in Table 1.The thermochemical values, ΔrH theory, listed in Table 1,

were determined with the computational program suiteGaussian 0930 and the B3LYP/6-311++G(d,p) level of theorywith thermal corrections using the rigid rotor−harmonicoscillator approximation to provide ΔrH theory values at 298K. For these calculations, the parent nucleobases were assumedto be deprotonated at the most thermodynamically favorableposition,31 that is, N9 for adenine and guanine and N1 forcytosine, thymine, and uracil (Figure 2). Previous studiesdemonstrated that gas-phase biological ions formed by ESIgenerally retain their most stable solution structure.32

The reactions of the nucleobase anions with H-atomsproceed exclusively by associative electron detachment, inwhich a bond is formed to hydrogen and the electron isdetached. We have observed this mechanism for a wide varietyof negative ions, and indeed, we have found only two extremelystable anions (C2N3

− and C4N3−) that are unreactive with H-

atoms.14,16 Associative electron detachment processes arecritical in the interstellar medium where they play a majorrole in determining the balance between negative ions andelectrons. For the thermochemical values listed in Table 1, thehydrogen atom is assumed to bond at the original site ofdeprotonation to form the parent nucleobase molecule. Thereactions of deprotonated adenine, guanine, thymine, anduracil all occur at approximately the same rate within theprecision of the experiment. Notably, the cytosine reactionoccurs almost five times faster, perhaps because the electronbinding energy of N1 deprotonated cytosine is lower than forthe other nucleobases by ∼0.2−0.3 eV.33 Our previous studieshave demonstrated a correlation between rate constants ofassociative electron detachment processes and the electronbinding energy of the anion,14 as well as with the overallreaction thermochemistry.34

All of the deprotonated nucleobases show moderately rapidreactivity with O atoms, and they generate a variety ofremarkable products, as shown in Table 1. Previous studiescharacterized the O atoms formed by the gas-phase titration asthe triplet state, O(3P). Therefore, the spin state of thereactants and products must be considered for the reaction X−

+ 3O. To generate ΔrH theory values, two spin states wereconsidered for each of the polyatomic products in this study,

i.e., singlet and triplet (for species with an even number ofelectrons) or doublet and quartet (for species with an oddnumber of electrons). The lower-energy electronic state wasalways found to be the species of lower spin, i.e., the singlet ordoublet; in Table 1, doublets are designated with a superscript“2”, while all other species are singlets. The optimizedgeometries for all reactants and products in Table 1 areprovided in the Supporting Information (SI). In SIFTexperiments, only the mass-to-charge ratios of the ions aremeasured, and the neutral products are not observed.Therefore, the neutral products of the O-atom reactions inTable 1 were proposed assuming reasonable, stable species; inall cases, these reactions were computed to be exothermic. Theoccurrence of spin conversion, as observed in many of thesepathways, is common for reactions involving high-spin atomssuch as O(3P).22

Several trends emerge for the X− + O reactions. First,associative electron detachment occurs for all reactions,representing from 20 to 70% of the reaction pathways. Second,a product ion 15 amu higher than the mass of X− is observedfor each reaction. This ion corresponds to addition of O andloss of H [X− + 3O → 2X(+O−H)− + 2H]. Our previous studythat investigated deprotonated organic heterocycles + Oobserved similar product channels.19 This substitution processconserves spin and is exothermic for each reaction systeminvestigated. For the +15 amu anionic products, two or moreisomer geometries are optimized to determine ΔrH theory.The lowest-energy isomer is formed when O replaces H on anunsaturated ring carbon atom, suggesting that O preferentiallyattacks the nucleophilic regions of the molecule. Fordeprotonated adenine, cytosine, guanine, thymine, and uracil,these lowest-energy isomers correspond to replacement of Hby an O-atom at positions 2, 6, 8, 6, and 5, respectively.A third process common to all X− + O reactions is the

formation of the cyanate anion, OCN−, at m/z 42. Thisresonance stabilized anion possesses high thermodynamicstability and was the first anion detected in the interstellarmedium.35,36 While OCN− is readily generated for each X− +O reaction, the mechanisms of formation may differ becauseeach system contains multiple O−C−N structural motifs.When O binds to a molecule, the newly formed adduct can beexcited by 75−150 kcal/mol. These highly excited transientspecies can undergo complex reaction mechanisms to generatethe rich product distributions that are observed. Several ofthese additional pathways are discussed below.Neutral adenine, a purine nucleobase, is a hydrogen cyanide

pentamer (HCN)5. Our recent study of the fragmentation ofdeprotonated adenine by collision-induced dissociationrevealed sequential loss of HCN moieties.37 In analogy withthis decomposition pattern, the formation of OCN− may beaccompanied by loss of four HCN molecules. Other productchannels correspond to loss of fewer HCN molecules and/orloss of isocyanic acid (HNCO) in which OCN− has beenprotonated before fragmentation. Guanine, also a purinenucleobase, shows similar product pathways with loss ofmultiple HCN and HNCO molecules. Both deprotonatedadenine and guanine have six ionic product channels andexhibit extensive decomposition upon reaction with O-atoms.In contrast to the purine nucleobases, the reactions of the

deprotonated pyrimidine nucleobases with O-atoms generatecarbonyl products. Carbon monoxide is produced by all of thepyrimidine reactions; in addition, formaldehyde is formed fromcytosine, and ketene is formed from uracil. Extrusion of HCN

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and HNCO molecules occurs in several of the productchannels. Quantum mechanical calculations to explore thedetailed mechanisms of these processes would be extremelyvaluable; however, these computational studies will bechallenging due to the relatively large size of the nucleobases,their structural complexity, and the occurrence of multiplereactions pathways.In summary, the anions formed by deprotonation of the

nucleobases (adenine, cytosine, guanine, thymine, and uracil)react readily with H-atoms by associative electron detachment.The anions are unreactive with N-atoms but exhibit a richchemistry in reactions with O-atoms; associative electrondetachment, exchange of hydrogen by oxygen, and formationof the cyanate anion are exhibited by all nucleobases. Many ofthe proposed neutral molecule products, including HCN,HNCO, H2CO, and CO, have been detected in the interstellarmedium, as have been the product anions OCN− and CN−. Inaddition to providing fundamental understanding of thereactivity of nucleobase ions, these studies provide insightinto astrochemical environments where biomolecules, theirions, and their prebiotic building blocks exist. In particular,these studies reveal the chemical reactions that may occur atthe boundaries between diffuse clouds, where atomic speciesare abundant, and the dense molecular clouds, where complexions and molecules have been detected.

■ ASSOCIATED CONTENT

*S Supporting InformationThe Supporting Information is available free of charge on theACS Publications website at DOI: 10.1021/acs.jp-clett.9b01997.

Optimized geometries for the neutral and negativelycharged molecules used in Table 1 to generate thethermochemical ΔrH theory values (PDF)

■ AUTHOR INFORMATION

Corresponding Author*E-mail: veronica.bierbaum@colorado.edu.

ORCIDCharles M. Nichols: 0000-0001-9398-3410Zhe-Chen Wang: 0000-0002-0887-6619W. Carl Lineberger: 0000-0001-5896-6009Veronica M. Bierbaum: 0000-0002-8828-1171Present Addresses‡Agilent Technologies, Santa Clara, CA 95051, United States.§Wadsworth Center, New York State Department of Health,Department of Environmental Health Sciences, SUNYAlbany, Albany, NY 12201, United States.

NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTS

We gratefully acknowledge support of this research by theNational Science Foundation (Grants CHE-1300886, PHY-1734006, and CHE-1213862). This work used the ExtremeScience and Engineering Discovery Environment (XSEDE)Comet at the San Diego Supercomputer Center at UC SanDiego through Allocation AST110040.

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