Fragmentation Pathways in the Uracil Radical Cation - The Journal of

Article pubs.acs.org/JPCA

Fragmentation Pathways in the Uracil Radical Cation Congyi Zhou,† Spiridoula Matsika,*,† Marija Kotur,‡ and Thomas C. Weinacht‡ †

Department of Chemistry, Temple University, Philadelphia, Pennsylvania 19122, United States Department of Physics, Stony Brook University, Stony Brook, New York 11794, United States

‡

S Supporting Information *

ABSTRACT: We investigate pathways for fragmentation in the uracil radical cation using ab initio electronic structure calculations. We focus on the main fragments produced in pump−probe dissociative ionization experiments. These are fragments with mass to charge ratios (m/z) of 69, 28, 41, and 42. Barriers to dissociation along the ground ionic surface are reported, which provide an estimate of the energetic requirements for the production of the main fragments. Direct and sequential fragmentation mechanisms have been analyzed, and it is concluded that sequential fragmentation after production of fragment with m/z 69 is the dominant mechanism for the production of the smaller fragments.

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INTRODUCTION One of the most important consequences of radiation damage in DNA is the formation of radical cations, and specifically radical cations of the nucleobases.1−5 These cations are also important in many experimental pump−probe techniques, where a probe pulse ionizes the molecules, and subsequently the ions further break up.6−10 Radical cations of nucleobases can break into smaller fragments when enough energy is provided through electrons or photons, leading to the production of various fragments. The mechanisms that lead to the production of these fragments are not well understood. Our interest in the fragmentation of radical cations stems from our interest in following excited-state dynamics in molecules using pump probe spectroscopy.6−8 In this technique a UV pump excites gas-phase neutral molecules from the ground state to the first bright excited state, and then a timedelayed intense IR probe ionizes and dissociates the molecules. Time-of-flight mass spectrometry (TOFMS) is used to identify the fragments. These fragments carry information about the neutral excited-state dynamics. However, to interpret the timedependent fragment ion yields and associate the observed fragments with the different photophysical pathways in the molecule, we need to understand the fragmentation process of the molecules upon ionization. This technique has been used to study the pyrimidine nucleobases cytosine and uracil. However, the mechanisms for fragmentation of the radical cations of the pyrimidine nucleobases are not well understood.7,11−19 Early work proposed schemes for the production of the fragments seen in mass spectra of the pyrimidine bases, and isotope substitution was used to demonstrate these schemes.11 Rice at al.13 reported mass spectra of uracil and other methylated species, along with deuterated ones. They used deuteration and metastable peaks20 to investigate the origin of the fragments, and they concluded that sequential fragmentation is leading to © 2012 American Chemical Society

the main small fragments with mass to charge ratios (m/z) of 28, 41, and 42. Experimental mass spectrometry studies show a similar fragmentation pattern for uracil and thymine,13,16 which is expected because they differ by only a methyl group. The experimental and theoretical studies have shown that the ejection of neutral HNCO or NCO species is a common feature of the main dissociation pathway for all of the radical cations of the DNA/RNA bases.7,12−17 For thymine and cytosine radical cations, theoretical studies have been carried out to describe the main fragmentation pathways in detail.7,14,17 DFT studies of the uracil radical cation fragmentation have also been reported very recently.21 These studies give a wide range of possible fragmentation pathways applicable to various ionization techniques, but they do not address all of the fragments observed in our work. There has also been some recent work on doubly charged uracil cations.22 Here, we examine the fragmentation decay pathways for uracil in detail using ab initio electronic structure methods. Experimental TOFMS are also shown and interpreted using the theoretical predictions. Furthermore, the time dependence of the ion yields as a function of pump−probe delay gives further insight into the fragmentation pathways, and we use this information to augment our analysis.

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COMPUTATIONAL METHODS Optimizations of minima and transition states for the parent ion and the various fragments produced were carried out using the second-order perturbative many-body Møller−Plesset approach (MP2 or UMP2 for open-shell systems)23,24 with two different basis sets: 6-31G(d) and 6-311++G(d,p).25,26 The Received: September 23, 2011 Revised: August 17, 2012 Published: August 24, 2012 9217

dx.doi.org/10.1021/jp209213e | J. Phys. Chem. A 2012, 116, 9217−9227

The Journal of Physical Chemistry A

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pump and probe pulses are combined on a dichroic beam splitter and focused into an effusive molecular beam inside our TOFMS. The energies of our pump and probe pulses were about 1 μJ and between 5 and 60 μJ, respectively. To compensate for the different focal length of the lens at the two frequencies, the probe pulses are sent through a pair of lenses to prepare a slightly convergent beam, which can then be focused to the same position and spot size as the pump pulses. The peak intensities of the pulses were about 0.3 TW/cm2 for the UV and about 10 TW/cm2 for the IR. The experimental setup is described in more detail elsewhere.7 We prepare an effusive beam of uracil by gently heating a powder sample. Care was taken to work at the lowest temperature that provides a useful molecular density at the focus of the lasers, and the lasers were focused near the nozzle of our molecular beam to achieve a relatively high number of molecules in the focal volume.

energies of the MP2/6-311++G(d,p) geometries are further improved using single-point calculations with the CoupledCluster with Single, Double and perturbative Triple excitations (CCSD(T))27 with the 6-311++G(d,p) basis set. For species that have an unpaired electron, the CCSD(T) calculations were carried out using the restricted open-shell Hartree−Fock (ROHF) wave functions. The energies discussed in the text are the CCSD(T)/6-311++G(d,p) ones, and they are given with respect to the energy of the ground state of the parent ion at its minimum (denoted D0(112)), unless otherwise stated. All of the optimized geometries were verified to be energy minima or transition states by computing the harmonic frequencies. Because the uracil cation and most of the fragmented species are radicals, some spin-contamination is present in our MP2 calculations. Although the exact expectation value for S2 (where S is the spin operator) is 0.75 for an ionic molecule with multiplicity of 2, our MP2 calculations give S2 closer to 0.8. This value does not depend much on the basis set used. Furthermore, values for S2 vary a bit according to the fragments calculated. For example, for a minimum of fragment with m/z 42, S2 is 0.79 and 0.81 at the levels of MP2/6-31G(d) and MP2/6-311++G(d,p), respectively, while for a transition state of fragment with m/z 69 S2 is 0.85 for both levels. Although we do not report any results with the UMP2 energies corrected by spin projection, we have tested how the results are altered if we included the spin correction, and it was found that they are not affected much. In general, the differences are around 0.1 eV or less. The CCSD(T) results are expected to have negligible spincontamination because they are based on ROHF orbitals.28,29 Constrained optimizations stretching a single bond while optimizing the remaining coordinates of the molecule were performed in certain cases using MP2 with the 6-31G(d) basis set.30−32 Dissociation is not expected to be described accurately with single reference methods, such as MP2, although the problem is less severe for radicals. Our main aim with these calculations was to obtain relative estimates of the energetic requirement to break bonds. For dissociation energies, we rely on the calculations of the separate fragments, rather than the dissociation limit obtained from the constrained optimizations. The constrained optimizations provide estimated barriers along pathways, which when appropriate are refined by locating the transition states. An intrinsic reaction coordinate (IRC) calculation is also performed for the transition state that is involved in the main fragmentation path of the uracil cation to produce fragment 69. This calculation was done at the MP2/6-31G(d) level using the Gonzalez−Schlegel approach, 3 3 as implemented in GAMESS.34,35 The computational packages Gaussian 03,36 NWChem,37 and GAMESS34,35 were used for all calculations. Molecular visualization was rendered with MacMolPlt38 and MOLDEN.39

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RESULTS AND DISCUSSION Strong Field Dissociative Ionization. Figure 1 shows a TOFMS spectrum obtained with our pump−probe setup. A

Figure 1. TOFMS spectrum of uracil when (i) a pump pulse interacts with the sample before the probe pulse (shown in red), or (ii) the probe pulse interacts with the sample before the pump pulse (shown in blue). Both spectra are normalized to the parent ion yield.

UV pump (4.74 eV) excites the uracil molecules to the first bright state (which is S2), and then an IR intense laser pulse ionizes and fragments them. The generated fragments are detected in the TOFMS (shown in red in Figure 1). Superimposed to this spectrum is a spectrum taken with the IR pulse applied before the pump pulse. The main peaks in the spectrum are at m/z 112, corresponding to the parent ion, and at m/z 69, 41, 42, and 28 . These peaks also appear in electron impact mass spectra13 or photoionization mass spectra,16 although the relative intensities differ. The relative intensity of the peaks also depends on whether the pump pulse is applied before or after the probe pulse, as seen in Figure 1. The fragmentation pattern seen in the mass spectra depends on the energy deposited in the molecule. The energy deposited in the molecule via ionization is mostly electronic, although it can be rapidly converted to vibrational motion through evolution on the ionic potential energy surfaces (PESs) and radiationless decay. This leads to bond breaking. Alternatively, dissociation can occur on the excited electronic state PESs. For negative delays, when the probe pulse arrives first, mostly low-lying ionic states are excited, because ionization from S0 already requires the absorption of at least six probe photons

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EXPERIMENTAL METHODS Our measurements make use of an amplified ultrafast titanium sapphire laser system, which produces 30 fs laser pulses with a central wavelength of 780 nm and an energy of 1 mJ at a repetition rate of 1 kHz. These laser pulses are directed into a Mach−Zehnder interferometer, which is used for our pump− probe measurements. One arm of the interferometer has a third harmonic generation apparatus, which we use to generate pump pulses at a wavelength of 260 nm. The other arm of our interferometer is used to generate the probe pulses (at 780 nm) and contains a translation stage under computer control. The 9218



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Figure 2. Schematic diagram showing which bonds need to be broken to produce the observed fragments. The numbers in parentheses indicate the two fragments that will be produced in each case. The dashed lines correspond to the different bonds that need to be broken to produce a given fragment. The color of each line matches the color of the pair of fragments in parentheses that will be produced from this breaking. (I) Direct fragmentation from the parent uracil cation; (II) stepwise fragmentation with fragment 69 being the intermediate. If tautomerization is needed before fragmentation (see I(C) and II for fragment 42+), breaking of the NH bond is also indicated. The exact pathways will be discussed in the appropriate sections.

out the original model proposed in 1965 is the most energetically favorable, according to our results. Our studies focus on dissociation from the ground ionic state; that is, we restrict our studies to the PES of D0. Barriers on D0 provide the minimum energy required to produce the fragments. Although ionization may lead to higher ionic states, it is very likely that radiationless decay to the ground state will be fast and dissociation will follow from D0. This idea is similar to Kasha’s rule,42 which describes relaxation of higher excited electronic states to the lowest excited state in a neutral molecule, and is based on the high density of states characterizing the excited states of neutrals. According to Kasha’s rule, fluorescence is expected from the lowest excited state of a molecule. Because the ions are also characterized by a high density of states, one would expect similarly fast radiationless decay to D0 before dissociation occurs. Even if rapid dissociation in an excited state of the ion is competing with radiationless decay, many of the dissociation energies we calculate are comparable to the difference in energy between the excited and ground states, implying that dissociation on the excited states is not energetically favorable. Furthermore, experiments that we have carried out on other molecules with a velocity map imaging apparatus indicate that ionization to excited states of the ion is followed by dissociation on the ground state of the cation, where fragments are ejected with the maximum possible kinetic energy.43 Finally, we note that if the molecule does not relax all of the way to the ground state prior to dissociation, we expect the barrier to dissociation to be comparable to the ground-state dissociation barrier to avoid curve crossings that would facilitate relaxation to the ground state prior to dissociation. On the basis of these arguments, we focus on dissociation on D0 to find the energetic requirements for the fragments we observe. Open-Ring Structures. For fragmentation to occur, two bonds need to be broken in the ring structure of the molecule. There are, however, stable structures where only one bond is broken. For the uracil radical cation, we found two minima where the N3−C4 bond is partially broken. These structures are shown in Figure 3a. In one of them, D0(112)-o1, the N3−C4 bond has been stretched to 2.49 Å, and the energy of the cation is 1.44 eV above the D0 minimum D0(112). If the N1−C2 bond is further rotated, a second minimum is found, D0(112)-o2, with energy 1.10 eV above D0(112). The N3−C4 bond length in this second minimum is 4.33 Å. To establish the barrier that could lead to D0(112)-o1, we carried out constrained

(the experimental vertical ionization potential (VIP) and adiabatic ionization potential (AIP) are 9.60 and 9.32 eV, respectively;40,41 the calculated values at the CCSD(T)/6-311+ +G(d,p) level are 9.34 and 9.13 eV, respectively), and higherlying states would require the absorption of even more photons, which is less likely at the intensities used in the experiment. Thus, one expects mostly the parent ion and large fragments (formed from low-lying cationic states) for negative delays. For positive delays, when the UV pump is applied first, the molecules are excited to S2. The intense IR probe then moves the population from S2 to the ionic states. The effective IP is the difference between the VIP and the excitation energy to S2, which is 4.9 eV (9.6 − 4.7 eV). Ionization can be accomplished with the absorption of roughly three IR photons, and the absorption of six photons (as required for ionization from the ground state) can lead to excited cationic states, which have more energy for dissociation. Thus, one expects lighter fragments to be more prominent for positive delays. This is the case as shown in Figure 1. The measurements show that for negative delays, the TOFMS is dominated by the parent ion with some signal at m/z 69 but almost no smaller fragments. However, for positive delays, the peak at m/z 69 dominates the TOFMS, and smaller fragments become prominent. These observations are consistent with our calculations, and with experimentally determined appearance energies for the various fragments,15,16 as will be shown below. Fragmentation Pathways. The dominant fragments in the TOFMS in the dissociative ionization experiments (excluding the parent ion) are at m/z 69, 28, 41, and 42, so we will focus our following discussion on how these fragments can be generated. Figure 2 shows the bonds that have to be broken in uracil to generate these fragments. Figure 2(I) shows how direct fragmentation from uracil can produce the desired fragments, while Figure 2(II) indicates how further fragmentation of m/z 69 can generate the smaller fragments. Although direct fragmentation seems to be more straightforward, previous studies on nucleobases have proposed sequential fragmentation with fragment 69 being the intermediate.11,13,14,16 The sequential scheme has been proposed as early as 196513 and has been tested by others experimentally. However, there has been no theoretical verification that this model is indeed the predominant one. In this work, we investigate both direct and sequential possibilities and draw conclusions about which is expected to be dominant. It turns 9219



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closer to 1.3 eV, although some uncertainty in this value remains. Ejection of neutral fragment 43, which is what is needed to obtain the cation of 69, is common in the fragmentation of nucleobase radical cations in general,7,12−14,16,17 so the mechanism for this process may be important for the other bases as well. Figure 2(I(A)) shows that there are three possibilities to produce this fragment just by looking at the appropriate combination of atoms. Previous theoretical and experimental work on thymine and uracil, however, indicates that the predominant pathway is the one where the N1−C2 and N3−C4 bonds are broken.11,13,14,21 According to theoretical calculations on thymine, this path generates the lowest ion with structure HNCHCHCO+. According to our calculations as well, the N1−C2 bond in the cation has weakened considerably as compared to the neutral molecule, making this bond easier to break. Constrained optimizations where we stretch the N1−C2 bond show that about 1.8 eV are needed to stretch the bond by 2.4 Å. Optimizing the two fragments 69 and 43 separately shows that the energy of the final products, 69 cation (denoted min1(69)) plus 43 neutral fragment (denoted neu(43)), is 1.93 eV above D0(112). The energies at all levels of theory used are shown in Table 1. The energy to produce a cation of 43 and neutral 69 fragment is 4.49 eV (shown as min1(43) + neu(69) in Table 1), much higher than the alternative pair. This difference depends on the IP of each species and is a consequence of the fact that the IP of HNCHCHCO (fragment

Figure 3. (a) Minima on the D0 PES of uracil radical cation that have an open structure. (b) Transition states important for the fragmentation pathways in uracil cation. For the hydrogen bonds’ lengths, only those of the symmetric geometries and those involving H transfer are shown.The imaginary frequencies for the transition states are 157i, 1954i, 1629i, 382i, 804i, and 1415i for ts1(112), ts1(69), ts2(69), ts3(69), ts4(69), and ts5(69), respectively. The numbers shown next to bonds represent bond lengths in angstroms. All geometries are calculated at the UMP2/6-311++G(d,p) level.

optimizations from D0(112) stretching the N3−C4 (see Figure S1). These calculations cannot clearly demonstrate the barrier, however, because it appears that a curve crossing occurs along the pathway, and the process involves more than one electronic diabatic state. The open-ring structures indicate that the parent ion signal observed in the TOFMS could come not only from the cyclic parent ion but from these open structures as well, if there is at least 1.5 eV extra energy in the system. It is, however, not possible experimentally to distinguish an open from a closed ring structure. Furthermore, the exact energy of the barrier is not established yet, so the energy required could be higher. Finally, if the system has this additional energy, it may be very easy for it to continue breaking making smaller fragments. This will depend on the additional energy needed to break one more bond in the ring. It turns out that the energy required to make the energetically most accessible fragment 69 is about 2 eV or less, close to the energy required to break just one bond, so it is likely that this fragment will be produced rather than the openring structures. Fragment m/z = 69. The peak at m/z 69 is the largest peak in the TOFMS, so we start our studies with this fragment. We compare our results with experimental data on the energy needed to produce the fragments. The experimental energy is taken as the difference between the appearance energy of the fragment minus the appearance energy of the parent ion, and will be denoted appearance energy difference (AED). Two previous studies have found that the AED for fragment 69 is the lowest, although the AED varied between 1.3 and 1.8 eV depending on the experimental study.15,16 Actually, both studies find about the same appearance energy for fragment 69, between 10.9 and 11 eV. However, the discrepancy comes because the appearance energy of the parent ion is different between the two studies. Reference 16 gives 9.1 eV, whereas ref 15 gives 9.5 eV. Because the second value is closer to the accepted value for the VIP of uracil, the AED for 69 is probably

Table 1. Energies ΔE in eV of Important Transition States and Minima Relative to D0(112)a species (m/z) D0(112)-o1 D0(112)-o2 min1(112) min2(112) min1(69)b min2(69)b min3(69)b min4(69)b min1(28) + min1(28) + min1(41) + min2(41) + min3(41) + min1(42) + min1(42) + min2(42) + min3(42) + min1(43) + ts1(112) ts1(69)b ts2(69)b ts3(69)b ts4(69)b ts5(69)b

neu(41)b neu(84) neu(28)b neu(28)b neu(28)b neu1(27)b neu2(27)b neu2(27)b neu Hb neu(69)

ΔE (a)

ΔE (b)

ΔE (c)

1.42 0.95 0.36 0.61 2.22 1.95 2.68 2.63 4.37 2.97 2.14 3.77 5.30 2.78 3.69 5.94 11.15 4.88 1.85 4.35 4.45 2.36 3.49 4.32

1.30 0.95 0.27 0.45 2.03 1.75 2.49 2.33 4.06 3.15 1.88 3.53 5.13 2.55 3.35 6.06 11.02 4.48 1.69 4.01 4.08 2.12 3.26 3.95

1.44 1.10 0.11 0.45 1.93 2.09 2.47 2.65 4.30 3.06 2.12 3.87 4.72 2.88 3.54 5.60 10.88 4.49 1.63 4.04 4.30 2.28 3.16 4.31

a

(a), (b), and (c) correspond to the theoretical levels of MP2/631G(d), MP2/6-311++G(d,p), and CCSD(T)/6-311++G(d,p), where the CCSD(T) energies are from single-point calculations using the MP2/6-311++G(d,p) optimized geometries. bFor these species, the energy of neu(43) is added to their energy, and the sum is subtracted from D0(112) to obtain the relative energies.

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transition states below the dissociation limit is uncommon, it can occur. In this case, there is a local minimum very close to ts1(112) with an energy just 0.1 eV below the transition state. At ts1(112) and the neighboring local minimum, the two fragments still interact with each other. As the fragments move further away, the attractive interactions vanish, and the energy rises slowly to the dissociation limit. We performed an IRC calculation, that is, a steepest descent path in mass weighted coordinates, that connects the saddle point to reactants and products, starting from ts1(112). This calculation showed that the transition state is connected to the equilibrium structure of the cation D0(112) in one direction of the reaction coordinate, and to the local minimum mentioned above on the other side. Figure S2 in the Supporting Information shows the path produced from the IRC calculations. We checked that there are no additional barriers to dissociation by carrying out constrained optimizations starting from the local minimum next to ts1(112) and stretching the N1−C2 bond further (also seen in Supporting Information, Figure S2). Overall, these calculations establish a minimum energy path starting from D0(112) and leading to min1(69) + neu(43) through ts1(112). A transition state similar to the one we report here was also found for thymine in previous studies.14 In that work, however, a second transition state is reported, which shows that the N1−C2 bond is broken first. Cytosine radical cation, on the other hand, has been reported to have a single transition state for the pathway leading to a loss of neutral HNCO, similar to our current calculations.17 Fragment m/z = 28. A fragment with m/z 28 can be produced directly from the parent ion in three possible ways, as shown in Figure 2. In two of these ways, the product will be CO+. However, the IP for CO is very high, calculated to be 13.65 eV, so the overall energy to produce 28+/84, where 28+ is CO+, is very high. For example, MP2/6-31G(d) calculations show that it takes about 8.33 eV to form 28+/84, with the N1− C2 and C2−N3 bonds being broken. Although we did not calculate the other possibility of breaking N3−C4 and C4−C5, we expect this to be high as well. We conclude that the two pathways that produce CO+ are energetically inaccessible, and therefore the pathways leading to those final products are disregarded. The third pathway to form 28+, shown in I(B) in Figure 2, involves breaking the bonds N1−C2 and C5−C6, producing HCNH+ and CHCONHCO. As compared to the product of CO+, the energy of the final products involving HCNH+ is much lower. The energy of the pair of fragments that include HCNH+ (denoted min1(28)) and its corresponding neutral 84 fragment (denoted neu(84)) is 3.06 eV, while the energy of the final products when HCNH is neutral is 4.00 eV. HCNH has

69) is much lower than the IP of HNCO (fragment 43). Figure 4 shows the final geometries for fragment 69 and its neutral partner, along with all of the other important final fragments found in this work.

Figure 4. Final optimized geometries of the fragments obtained at the MP2/6-311++G(d,p) level of theory. Bond lengths shown in angstroms. All of the cations are within the black frames, while their corresponding neutral fragment pairs are in the red frames. For the lengths of the hydrogen bonds, only those of the symmetric geometries are shown.

Calculating the energy of the final products is not sufficient. We also need to determine whether there are any additional barriers leading to these products. We have located a transition state that is involved in the production of fragment 69, denoted ts1(112). The structure is shown in Figure 3. This transition state achieves simultaneous breaking of the N3−C4 and N1−C2 bonds through a retro Diels−Alder (RDA) reaction44 leading to the loss of the HNCO group. The involvement of RDA reactions in fragmentation of ions is well-known.45 In RDA reactions, cyclohexene-like molecules fragment into an ethylene-like fragment with one double bond, and a butadiene-like fragment with two double bonds. The imaginary frequency of ts1(112) is low, 157 cm−1, and the mode involves simultaneous stretching of both bonds. The energy of ts1(112) is given in Table 1, and it is 1.63 eV above the D0 minimum, which is lower than the dissociation limit. Although the presence of

Figure 5. Possible fragmentation pathways leading to m/z 28. The neutral pair is omitted when it can be implied. 9221



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Figure 6. Possible fragmentation pathways leading to fragment m/z 41. The most energetically favorable pathways are indicated by the green arrows, and the transition states involved are shown in green letters next to the arrows. For each pathway, its corresponding dominant barrier is indicated by the asterisk on the right top of a path number. The neutral pair is omitted when it can be implied. Estimated energy barriers are shown in Table 2.

final products here are different from what we expected by just dividing the molecule into two species (shown as path I in Figure 5). In contrast to what we found by just calculating the final products, the constrained optimizations show that the neutral fragment 84 species further breaks into two fragments: HCCO and HNCO. Even though the neutral cyclic fragment 84 is 1.24 eV lower than the two separate products HNCO + HCCO, the barrier for dissociation is higher. Going over this barrier along the dissociation pathway is likely that it drives the molecules to move toward further breakup of 84 into smaller fragments rather than go to the more thermodynamically stable cyclic minimum of 84. Another possibility for the production of fragment 28 is sequential fragmentation from fragment 69 by breaking the C5−C6 bond, shown as path III in Figure 5. This leads to the production of HCNH+ and HCCO. A constrained optimization starting from min1(69) and stretching the C5−C6 bond is shown in Figure S4, where it is shown that there are no additional barriers higher than the dissociation limit of 4.30 eV to reach the final products. The overall final products in this case are exactly the same as seen in the direct fragmentation, HCNH+ + HNCO + HCCO, and the energy required for fragmentation is also the same. In both cases, the dissociation energy is the same as the final products’ energy; that is, there are no additional barriers along the dissociation. In summary, m/z 28 can be produced both directly and sequentially, as shown in Figure 5, with the same energy requirements and forming the same products. Fragment m/z = 41. Another significant peak in the TOFMS is at m/z 41. For the direct fragmentation mechanism shown in Figure 2I(C), there are two ways to produce fragment 41 directly from the cation. One possibility is to have the N3− C4 and C5−C6 bonds broken leading to HCCO+. The energy needed to break C5−C6 however will be high given that it is a

an IP of 6.78 eV, which is much lower than the IP of CO. HCNH+ is the protonated form of hydrogen cyanide, and a stable known molecular ion of astrophysical interest.46 This ion is linear, while the neutral species is bent. Fragment 84 has a calculated IP of 7.72 eV with the neutral species forming a cyclic structure, while the cation has an open structure. The higher IP for 84 shows that the cation 28 will be formed easier in our experiments. Figure 5 shows the structure of these two species as one of the pathways (pathway I) for the production of fragment 28, with final products min1(28) + neu(84). More detailed calculations have also been performed to search for barriers along the dissociation for the direct fragmentation pathway. However, we were not able to find pathways leading to the above final products. Instead, our calculations of pathways lead to different products. To the left of the parent ion in Figure 5 is the calculated direct dissociation pathway. To produce HCNH+ from uracil, two bonds need to be broken, N1−C2 and C5−C6. It is easy to break the N1−C2 bond of D0(112) as was discussed earlier, but it is hard to break the C5−C6 bond as this has substantial double bond character. As the N1−C2 bond is being broken though, the C5−C6 bond is weakened and it becomes easier to break. We confirmed this by performing two constrained optimizations. Initially, we stretch the N1−C2 bond until it reaches 2.735 Å. This geometry is shown in Figure 5 as int1(112). The energy of int1(112) is 1.8 eV above the D0 minimum at the MP2/631G(d) level. Starting from int1(112), we then keep the N1−C2 bond fixed while we start stretching the C5−C6 bond (see Figure S3). We do not imply that this is the actual pathway that this breaking will occur, but this procedure gives us an estimate of the energy requirements needed to break the bonds. This calculation leads to the fragmentation of the uracil cation into three fragments, shown as int2(112) in Figure 5, HCNH+ + HNCO + HCCO. The overall dissociation energy is 4.30 eV. Interestingly, the 9222



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Three isomers with m/z 41 can be obtained on the basis of the sequential fragmentation mechanism. Their structures can be seen in Figure 6, denoted as min1(41), min2(41), and min3(41), and their energies are listed in Table 2. min1(41) is proven to be the most thermodynamically stable, being 1.75 eV lower than min2(41) and 2.60 eV lower than min3(41). For min1(41), two sequential fragmentation pathways were found. First, we discuss pathway II, involving steps II(a), II(b), II(c), and II(d). Our calculations predict the stepwise fragmentation pathway II is characterized by three transition states with geometries shown in Figure 3. Two of these transition states facilitate isomerization of fragment 69. The first saddle point ts1(69) corresponds to the H1 atom moving between N1 and C5, describing the energy barrier along path II(b). H1 is located between the two atoms C5 and N1, with the distance of H1−N1 being 1.343 Å and H1−C5 being 1.367 Å. ts1(69) is 4.04 eV above the D0(112) (see Table 1). After this rearrangement of fragment 69, a second rearrangement is occurring (step II(c)). This is facilitated by another transition state, ts2(69), which is characterized by H6 being transferred from C6 to N1, and has energy 4.30 eV higher than D0(112) (see Table 1). The last transition state along path II is ts3(69), corresponding to the breaking of the C5−C6 bond via path II(d). The energy barrier is 2.28 eV higher than the D0(112), lower than all of the previous barriers. One can observe that the hydrogen rearrangements, H1 moving from N1 to C5 for path II(b), and H6 moving from C6 to N1 for path II(c), define the energetic requirements for the overall path II. This will be seen in the fragmentation pathways for m/z 42 as well. The highest barrier is 4.30 eV, and this is the overall requirement for path II. Alternatively, min1(41) can be obtained via pathway III where the previous two rearrangements in 69 are performed in one step, by H6 transferred to C5 directly to produce min2(69). The transition state facilitating this migration is denoted ts5(69) and it is 4.31 eV above D0(112). So, it appears that pathway III is isoenergetic to pathway II, and it requires less steps. Path IV shows that a three-member cyclic product min2(41) can be produced from min1(69) by breaking the C4−C5 bond and removing a CO group from min1(69). This pathway involves a high energy step as discussed above for direct fragmentation, because breaking the C4−C5 bond in min1(69) leads first to HC−CH−NH, which has high energy before it forms the cyclic product. The constrained optimizations are shown in Figure S6. A transition state has been located near the top of the pathway, and it has energy 5.38 eV. Clearly, this energy is much higher than the energetic requirements of all previous pathways, so path IV is less important. Path V requires breaking the C4−C5 bond and removing a CO group from min3(69) to produce min3(41). The final product has an energy of 5 eV or more, so this path is not favored. In summary, pathways II and III seem to be the energetically favorable ones, while the remaining paths are less likely to occur. Sequential fragmentation is involved in the production of fragment 41, and min1(41) is both the thermodynamically and the kinetically favorable product. Fragment m/z = 42. A fragment with m/z 42 cannot be produced from fragmentation of uracil cation by merely breaking bonds. A hydrogen transfer has to occur at some point as well. The most obvious way for this to occur is directly by tautomerization of the parent ion first forming one of the enol tautomers. The energetic requirements for tautomerization

partially double bond. Thus, it is unlikely that this bond will be broken first. There is still the possibility that N3−C4 is broken first, and this may reduce the strength of the C5−C6 double bond, leading to an easier dissociation along C5−C6. To examine whether this is feasible, we checked whether the C5− C6 bond is weakened when the N3−C4 bond is being stretched by performing constrained optimizations along N3−C4, and we found that the C5−C6 bond length changes very little during the N3−C4 dissociation. On the basis of this information, this bond-breaking scenario to produce fragment 41 seems energetically unfavorable. The remaining possibilities that have been investigated are shown in Figure 6. Energetic requirements along the various paths are summarized in Table 2. Detailed energies of the transition states and final products are reported in Table 1. Table 2. Energy Barriers and Energies of the Final Products along Each Pathway Shown in Figure 6 To Produce Fragment m/z 41a path

final product

estimated barrier

I II III IV V

min1(41) min1(41) min1(41) min2(41) min3(41)

4.72 4.45 (4.30) 4.32 (4.31) 5.38 ≥5.30 (≥4.72)

ΔE 2.14 2.14 2.14 3.77 5.30

(2.12) (2.12) (2.12) (3.87) (4.72)

a

All energies are given in eV relative to D0(112). Energies correspond to the theoretical level MP2/6-31G(d), while the numbers in parentheses correspond to CCSD(T)/6-311++G(d,p).

Another possibility to produce fragment 41 directly is by breaking the N1−C2 and C4−C5 bonds producing HCCHNH, which is shown as path I in Figure 6. The starting point, uracil parent ion D0(112), is located at the center. The N1−C2 bond is easier to break, as already discussed. We used again the structure int1(112), which is one of the structures along the constrained optimization where the N1−C2 bond is partially broken (N1−C2 = 2.735 Å), shown in path I in Figure 6, and did a second constrained optimization stretching the C4−C5 bond while keeping the N1−C2 bond length fixed at 2.735 Å. This plot is shown in Figure S5. We do not suggest that this is the exact path the molecule takes to break these two bonds, but it can give us an estimate of the energy required to break the bonds. A transition state was found starting from the highest point on the constrained optimization path. The energy of this transition state is 4.72 eV above D0(112). The main difficulty with this path is that as the C4−C5 bond is stretched, the remaining fragment has the structure HC−CH−NH. This structure however is not stable, and rearrangement of the hydrogen atoms will take place to stabilize it. The rearrangement involves moving a H from C6 to C5, which drops the energy by more than 3 eV. The final cation product min1(41), known as ketenimine, is finally obtained. Fragment 71, which is the neutral pair of cationic fragment 41, is also not stable, and it further fragments according to our calculations into neutral CO and HNCO (see path I in Figure 6). Sequential fragmentation has been proposed experimentally for the production of m/z 41.11,13,16 In this case, fragment 69 can dissociate further into smaller fragments. This requires a single bond breaking to produce fragment 41. Except for path I, the remaining four paths in Figure 6 show how sequential fragmentation can occur. 9223



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C4 bond is much shorter so it would be even more difficult to break that bond. The C5−C6 is longer, which would probably make it easier to break the bond, but overall it will likely be energetically unfavorable to produce fragment 42 directly from an enol form of the parent ion. As seen in the other fragments, sequential fragmentation is a possible alternative. Even in this case, in addition to two bonds being broken, a H transfer is also required to form fragment 42. It is necessary to consider at which step the H transfer occurs. Below, we will show how it makes an obvious difference whether and when H rearrangements occur. Figure 8 shows the five possible pathways to produce fragment 42 sequentially. The initial point, the uracil parent ion D0(112), is at the center, to the left are the pathways leading to ketene cation min1(42), to the right are the pathways leading to its enol tautomer min2(42), and on top is the pathway that can produce cation min3(42). Tables 1 and 3 show the final energies of the

depend on the barriers for going from one tautomer to the other. We calculated 13 cationic uracil enol products. The lowest energy tautomer that can participate in the production of fragment 42, min2(112), is shown in Figure 7, and lies 0.45

Figure 7. Tautomerization between the keto minimum and enol minima in uracil cation. Energies are at the CCSD(T)/6-311++G(d,p) level using MP2/6-311++G(d,p) geometries. Listed beside each vertical arrow are the energy barriers in eV for the corresponding pathway.

Table 3. Estimated Energy Barriers and Energies of the Final Products along Each Pathway Shown in Figure 8 To Produce Fragment m/z 42a

eV higher than the keto cation minimum D0(112). To investigate the energy requirements for cationic keto to be tautomerized, two transition states were located between the reactant keto D0(112) and the enol product min2(112), as shown in Figure 7. It turns out that two steps of hydrogen rearrangements occur to generate min2(112), and the overall barrier for the tautomerization is 2.07 eV. The barriers for tautomerization in neutral uracil have been calculated previously,47 and they were found to be higher than those of the cation. For example, the equivalent barriers to those shown in Figure 7 for the neutral are 1.85 and 3.42 eV, for ts3(112) and ts4(112), respectively. The tautomerization energies are lower than other barriers involved in fragmentation, so it is possible that tautomerization occurs first followed by fragmentation. We did not explore all of these possibilities, but we use min2(112) as an example of the energetic requirements involved in this process. Direct fragmentation of the enol tautomer min2(112) would require breaking the C5−C6 and N3−C4 bonds. This breaking pattern is the same as what we discussed for making fragment 41 from the keto tautomer, and there we argued that it would be difficult to break these bonds. In the enol tautomer, the N3−

path

final product

I II III IV V

min3(42) min2(42) min2(42) min1(42) + HCN min1(42) + HNC

estimated barrier ≥11.15 ≥5.94 ≥5.94 4.35 4.45

(≥10.88) (≥5.60) (≥5.60) (4.04) (4.30)

ΔE 11.15 5.94 5.94 2.78 3.69

(10.88) (5.60) (5.60) (2.88) (3.54)

a

All energies are given in eV relative to D0(112) at the MP2/6-31G(d) level. Energies in parentheses are at the CCSD(T)/6-311++G(d,p) level.

products involving the isomers of 42. min1(42) can be produced from 69 with the neutral pair being HCN or HNC. min1(42) plus neutral HCN is the most thermodynamically stable product pair, being 0.66 eV lower than min1(42) plus neutral HNC, 2.72 eV lower than min2(42), and 8.00 eV lower than min3(42). From these energies, it is immediately clear that min3(42) is not expected to occur, so we further examine only the other pathways. The high energy for the production of min3(42) as compared to D0(112) is due to the fact that the dissociation energy to break the NH bond from HNCO+ (path I(b)) is very high.

Figure 8. Possible fragmentation pathways leading to fragment m/z 42. The most energetically favorable pathway is indicated by the green arrows, and the transition states involved are indicated next to the arrows. The asterisk on the right top of each path number corresponds to the dominant barrier along that pathway. The neutral pair is omitted when it can be implied. Estimated energy barriers are shown in Table 3. 9224



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measurements for m/z 28, 41, and 42 are very similar, but different from those of m/z 69 and 112.48 Table 4 summarizes the energetic requirements found in this work to produce the various fragments. The experimental AED are shown as well for comparison. According to the fragmentation energies we calculated, ca. 2 eV is needed to produce fragment 69, while 4 eV or higher is needed to produce the other fragments 28, 41, and 42. The calculated CCSD(T) AED values differ from the experimental ones by 0.06−0.6 eV. One should however take into account that there is some uncertainty in experimental values, as discussed earlier for fragment 69. There is also some uncertainty in the theoretical values, but we believe the CCSD(T)/6-311+ +G(d,p) values are quite accurate. Regardless of these small discrepancies, it seems that at least 4 eV needs to be deposited in the cation for the smaller fragments to be produced. This implies that higher ionic states need to be populated for these fragments to be produced. At vertical ionization, the first five ionic states of uracil are less than 3 eV above D0 and are single hole states.8 The sixth state, D5, is at 4.01 eV, and it has significant contributions from configurations with three holes in π orbitals (π1π1π1). The seventh state, D6, is at 4.18 eV, and it also has significant contributions from configurations with one hole on a lone pair and two more holes in π orbitals (n1π1π1). The eighth state is at 4.64 eV, and it can be qualitatively represented as π1π1π1. This indicates that ionization to states below D5 can only produce fragment 69, while ionization to states D5 and higher is needed to produce the lighter fragments. The fact that all of the lighter fragments have the same time dependence, as seen in Figure 9, indicates that they all come from the same ionic state(s). This is reinforced by the fact that they all have the same angle dependence in their yields.48 Furthermore, the fact that the m/z 28, 41, and 42 yields remain constant relative to one another as a function of pump−probe delay suggests that branching to form these three separate fragments does not occur immediately upon ionization. If this were the case, it would be very surprising to see a constant branching ratio for many different locations on the excited ionic state (D5 or D6) surface as the wave packet moves on the neutral S2 PES following the pump pulse. Rather, the measurements are more consistent with first the formation of an intermediate fragment, that is, 69, followed by branching to the three smaller fragments. This is in agreement with the calculation results discussed above.

For the enol product min2(42), two pathways are proposed (II and III). One of them involves steps II(a), II(b), and II(c), where tautomerization of min1(69) to min4(69) is followed by breaking the bond C5−C6(II(c)). The second pathway involves tautomerization of the parent ion (III(a)), which is the same process as in Figure 7, followed by paths III(b) and II(c). However, the energy of the final products of min2(42) plus HNC is 5.60 eV, which is higher than the overall requirements to produce min1(41). So regardless of the barriers involved in the paths, the energy required will be at least 5.60 eV, possibly higher because of any barriers involved. To generate min1(42), two possible pathways (IV and V) are shown in Figure 8. These paths involve H rearrangements of min1(69) similar to the ones we saw for fragment 41 in the previous section. The transition states and barriers for these rearrangements have already been discussed. Path IV is characterized by three saddle points with all of the geometries shown in Figure 3 and energies listed in Table 1. After production of min1(69), this can isomerize according to step IV(b), which has a transition state (ts1(69)) with energy 4.04 eV. The C5−C6 bond is then broken through the transition state ts4(69) with energy 3.16 eV (energies are always given with respect to D0(112)). So ts1(69) determines the overall energetic requirement for path (VI) to be 4.04 eV. min3(69) can further isomerize to min2(69) before dissociation through ts2(69), as seen in path V. The energy of ts2(69) is 0.26 eV higher than ts1(69), so path V is overall less favorable kinetically and thermodynamically as compared to path IV. The energies of all of the paths are summarized in Table 3 . According to the discussion above, we conclude that the favorable path for producing fragment 42 is via steps II(a), IV(b), and IV(c), ending at fragments min1(42) and HCN. Again, sequential fragmentation proved to be the preferred pathway, and the most thermodynamically favorable product is reached. Comparison with Experiment. Figure 9 shows ion yields as a function of time for a deep UV pump pulse, followed by an

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CONCLUSIONS We have performed detailed ab initio calculations to determine the fragmentation pathways in the uracil radical cation. Although these pathways are present in the cation regardless of the way it is formed, here we focus on the fragments produced in a pump−probe experimental approach where the pump pulse excites neutral molecules to the first bright neutral excited state, and the intense probe ionizes and fragments them. The main fragments observed in a TOFMS are at m/z 69, 28, 41, and 42. We mainly discuss the pathways that we believe require the lowest energy. More energetically demanding ones are possible and have been explored by other workers,21 but we do not focus on them here. All of the fragmentation patterns that we found in the uracil radical cation involve breaking the N1−C2 and N3−C4 bonds, which are the weakest bonds in the ion, followed by removal of the HNCO neutral species. Removal of HNCO is in agreement with previous studies on fragmentation of pyrimidine

Figure 9. Ion yield signals from m/z 28, 41, and 42 fragments as a function of pump−probe delay. The signal for each fragment is normalized.

intense IR probe pulse. The intensities of both pulses were chosen such that there were no ions produced by either pulse alone. The ion yields have been normalized to their maximum values. Fragments with m/z 28, 41, and 42 show similar dynamics as a function of pump−probe delay, whereas m/z 69 and 112 (the parent molecular ion) show different dynamics. Measurements of ion yields as a function of the angle between the UV and IR pulse polarization vectors show the same trend: 9225



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Table 4. Summary of the Barriers (Δ†E) and Energy of the Final Products (ΔE) for the Prominent Pathway To Produce Each Fragmenta species (m/z) +

(C3H3NO) (69) (CH2N)+(28) (C2H3N)+(41) (C2H2O)+(42)

AED15,16

Δ†E (a)

Δ†E (b)

Δ†E (c)

ΔE (a)

ΔE (b)

ΔE (c)

1.30−1.80 4.60 3.80 4.10

2.22 4.37 4.32−4.45 4.35

2.03 4.06 3.95−4.08 4.01

1.93 4.30 4.31−4.30 4.04

2.22 4.37 2.14 2.78

2.03 4.06 1.88 2.55

1.93 4.30 2.12 2.88

a

Experimental AEDs (the experimental energy difference between the fragment cation and the parent cation) are also shown. (a), (b), and (c) correspond to the theoretical levels of MP2/6-31G(d), MP2/6-311++G(d,p), and CCSD(T)/6-311++G(d,p), respectively. The zero has been set to the energy of D0(112) at the corresponding theoretical level. All energies are given in eV.

cations.7,11−14,16,17 In fact, even when we tried to form the products in a different way, these two bonds broke spontaneously. Further fragmentation occurs by breaking the C5−C6 (to produce m/z 28 and 42) or C4−C5 (to produce m/z 41) bonds. Fragment 69 is the dominant intermediate, and often the rate-determining step (highest barrier) in the fragmentation pathways is rearrangement of this fragment to its isomers. On the basis of our calculations, m/z 69 can easily be formed when at least 2 eV of energy is deposited in the cation, which implies that it is formed when ionization leads to ionic states above D1. The lighter fragments require at least 4 eV of energy to be produced, and this energy will be obtained only when ionization leads to the higher ionic states, D5 and higher. Rapid radiationless decay from the high ionic states to D0 can transform the electronic energy to vibrational energy on the ground-state D0, which is then used for dissociation. Our calculations indicate that fragment 28 can be produced directly or sequentially with the same energy requirements, whereas fragments 41 and 42 are produced in a stepwise mechanism, with fragment 69 being first formed and then dissociating further to the lighter fragments. Measurements of ion yields as a function of pump−probe delay show very similar dynamics for the smaller cationic fragments 28, 41, and 42. This is consistent with the idea that sequential fragmentation is the dominant mechanism leading to all three fragments.

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(2) Becker, D.; Sevilla, M. D. The Chemical Consequences of Radiation Damage to DNA. Advances in Radiation Biology; Academic Press: San Diego, CA, 1993; Vol. 17, pp 121−180. (3) Núnez, M. E.; Hall, D. B.; Barton, J. K. Chem. Biol. 1999, 6, 85− 97. (4) Lewis, F. D.; Liu, X.; Jianqin Liu, S. E.; Miller, R. T. H.; Wasielewski, M. R. Nature 2000, 406, 51−53. (5) Kanvah, S.; Joseph, J.; Schuster, G. B.; Barnett, R. N.; Cleveland, C. L.; Landman, U. Acc. Chem. Res. 2010, 43, 280−287. (6) Kotur, M.; Weinacht, T. C.; Zhou, C.; Matsika, S. IEEE J. Sel. Top. Quantum Electron. 2011, 1−8. (7) Kotur, M.; Weinacht, T. C.; Zhou, C.; Kistler, K.; Matsika, S. J. Chem. Phys. 2011, 134, 184309. (8) Matsika, S.; Zhou, C.; Kotur, M.; Weinacht, T. C. Faraday Discuss. 2011, 153, 247−260. (9) van Tilborg, J.; Allison, T. K.; Wright, T. W.; Hertlein, M. P.; Falcone, R. W.; Liu, Y.; Merdji, H.; Belkacem, A. J. Phys. B: At. Mol. Phys. 2009, 42, 081002. (10) Kosma, K.; Schröter, C.; Samoylova, E.; Hertel, I. V.; Schultz, T. J. Am. Chem. Soc. 2009, 131, 16939−16943. (11) McCloskey, J. A. In Basic Principles in Nucleic Acid Chemistry; Ts’o, P. O. P., Ed.; Academic Press: New York and London, 1974; Vol. 1, pp 209−309. (12) Jolibois, F.; Cadet, J.; Grand, A.; Subra, R.; Rega, N.; Barone, V. J. Am. Chem. Soc. 1998, 120, 1864−1871. (13) Rice, J. M.; Dudek, G. O.; Barber, M. J. Am. Chem. Soc. 1965, 87, 4569−4576. (14) Improta, R.; Scalmani, G.; Barone, V. Int. J. Mass Spectrom. 2000, 201, 321−336. (15) Denifl, S.; Sonnweber, B.; Hanel, G.; Scheier, P.; Mark, T. Int. J. Mass Spectrom. 2004, 238, 47−53. (16) Jochims, H.-W.; Schwell, M.; Baumgartel, H.; Leach, S. Chem. Phys. 2005, 314, 263−282. (17) Wolken, J. K.; Yao, C.; Tureček, F.; Polce, M. J.; Wesdemiotis, C. Int. J. Mass Spectrom. 2007, 267, 30−42. (18) Tabet, J.; Eden, S.; Feil, S.; Abdoul-Carime, H.; Farizon, B.; Farizon, M.; Ouaskit, S.; Märk, T. Int. J. Mass Spectrom. 2010, 292, 53− 63. (19) Tabet, J.; Eden, S.; Feil, S.; Abdoul-Carime, H.; Farizon, B.; Farizon, M.; Ouaskit, S.; Märk, T. D. Phys. Rev. A 2010, 81, 012711. (20) McLafferty, F. W., Ed. Mass Spectrometry of Organic Ions; Academic Press: New York and London, 1963. (21) Arani, L. S.; Mignon, P.; Abdoul-Carime, H.; Farizon, B.; Farizon, M.; Chermette, H. Phys. Chem. Chem. Phys. 2012, 14, 9855− 9870. (22) López-Tarifa, P.; Hervé du Penhoat, M.-A.; Vuilleumier, R.; Gaigeot, M.-P.; Tavernelli, I.; Le Padellec, A.; Champeaux, J.-P.; Alcam, M.; Moretto-Capelle, P.; Martin, F.; et al. Phys. Rev. Lett. 2011, 107, 023202. (23) Møller, C.; Plesset, M. S. Phys. Rev. 1934, 46, 618−622. (24) Head-Gordon, M.; Pople, J. A.; Frisch, M. J. Chem. Phys. Lett. 1988, 153, 503−506. (25) Krishnan, R.; Binkley, J. S.; Seeger, R.; Pople, J. A. J. Chem. Phys. 1980, 72, 650−654. (26) Clark, T.; Chandrasekhar, J.; Spitznagel, G. W.; Schleyer, P. V. R. J. Comput. Chem. 1983, 4, 294−301.

ASSOCIATED CONTENT

S Supporting Information *

The minimum energy path (IRC and constrained optimizations) that shows fragmentation to min1(69) + neu(43) via ts1(112) is shown. Other constrained optimizations used in this work are also shown. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We gratefully acknowledge support from the Department of Energy under award numbers DE-FG02-08ER15983 and DEFG02-08ER15984. Most of the calculations were conducted using EMSL, a national scientific user facility sponsored by the Department of Energy Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory.

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REFERENCES

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