Low energy (1–19 eV) electron scattering from condensed thymidine (dT) II: comparison of vibrational excitation cross sections with those of tetrahydrofuran and the recalibrated values of thymine

V. Lemelin*, A. D. Bass, P. Cloutier and L. Sanche
Groupe en Sciences des Radiations, Département de Médecine Nucléaire et Radiobiologie, Faculté de Médecine et Sciences des radiations, Université de Sherbrooke, Québec J1H 5N4, Canada. E-mail: Vincent.Lemelin@usherbrooke.ca

Received 18th June 2019 , Accepted 3rd September 2019

First published on 3rd September 2019


Recent measurements of absolute vibrational cross sections (CSs) for low-energy electron (LEE) scattering from condensed thymidine (dT) allows comparison with CSs of its constituents; thymine and tetrahydrofuran (THF). To facilitate this comparison, the vibrational CSs of condensed thymine were remeasured at six electron incident energies and a correction was applied to the earlier thymine CS values measured by Lévesque et al. [Nucl. Instrum. Methods Phys. Res., Sect. B, 2003, 208, 225]. The incident energy dependence of the CS of each vibrational mode of dT is compared with the corresponding modes in thymine and/or THF. It is found that the magnitude of the CSs of the thymine breathing mode and the C–C stretch mode of THF are greatly attenuated in dT. Finally, the magnitudes of the total vibrational CSs of each molecule are compared. Below 4 eV, the total vibrational CSs of dT is greater than each of its two constituents. Interestingly, at higher energy (>6 eV), the magnitude of the total vibrational CS of dT is roughly equal to that of THF and is greater than thymine by only 15% at 10 eV, showing that the CSs of dT cannot be approximated by the addition of the CSs of its constituents over the entire energy range. These comparisons are discussed in terms of the basic principles involved in the formation and decay of shape resonances, which are known to be responsible for major enhancements of LEE-induced vibrational excitation at low electron energies.


I. Introduction

Studies into the interactions of low-energy electrons (LEEs) with biomolecules are of considerable relevance to radiobiology, since they are one of the most abundant secondary species produced by ionizing radiation.1 The interaction probabilities or cross sections (CSs) of LEE scattering from molecular components of the biological medium are necessary input parameters for the Monte Carlo simulations needed to produce precise calculations of radiation dose imparted to biological matter at a nanoscopic level.2–6 Such nanodosimetric models should be particularly useful for future “highly-localized” radiotherapies such as radiotherapy with gold nanoparticles or targeted radionuclide therapy.7–10 Since LEE scattering CSs are difficult to calculate from theory, experimental measurements of such CSs from relevant biomolecules are required for these radiobiological models and simulations.

In paper I (V. Lemelin, A. D. Bass, P. Cloutier and L. Sanche, DOI: 10.1039/c9cp03447a), we presented the measurements of absolute vibrational CSs for LEE (1–19 eV) scattering from condensed thymidine (dT). dT is a nucleoside composed of the DNA base thymine and the deoxyribose from the backbone of the DNA (see Fig. 1(C)). dT is the most complex component of the DNA molecule to be studied with high-resolution electron energy loss spectroscopy (HREELS), which can provide absolute LEE CSs. Our previous studies on CS measurements always focused on an isolated DNA basic constituent; i.e., a DNA base or analog (pyrimidine, cytosine, thymine, adenine)11–17 or a molecule from its backbone (tetrahydrofuran (THF) (a model for deoxyribose) and dimethyl phosphate (model for the phosphate group)).18–21 Furthermore, both calculations and experiments have shown that LEE-biomolecule interactions are directly affected by the molecular environment, particularly neighboring water molecules.22–30 Hence, it becomes necessary to measure CSs in more complex environments and/or with more complex molecules, as we did with dT in paper I, to obtain reliable CSs that better represent the biological reality.


image file: c9cp03448j-f1.tif
Fig. 1 Chemical structure of tetrahydrofuran (THF) (A), thymine (B) and thymidine (dT) (C).

Here we compare the absolute vibrational CSs of condensed dT and those of its constituents: thymine13 and THF18 (Fig. 1(A) and (B)), which we have previously measured. Firstly, we measure the absolute vibrational CS values of condensed thymine so as to apply a correction to those previously obtained by Lévesque et al.13 in 2003. This renormalization, along with the higher resolution and better signal of the present experiments, permits a direct comparison of these data with those of dT of paper I. Secondly, the HREEL spectra of condensed thymine, THF and dT are compared with each other. Thirdly, the incident energy dependence of the CSs for each vibrational mode of dT and the corresponding ones for each constituent are compared. Finally, the magnitude of the total vibrational CSs of dT, thymine and THF are compared. The ultimate objective of this paper is to verify if the CSs of dT are close to the sum of the CSs of its constituents and to study the variations in the CS values when the two molecules are chemically bonded together.

II. Experiment and scattering model

In this work, multiple EEL spectra of condensed thymine were recorded using HREELS. The apparatus has been described in previous studies31 and the technique is the same as described in paper I. Thymine (powder, Sigma-Aldrich, 99%) was sublimated using the double-stage oven described in paper I. Here however, the sublimation temperature was changed to 90 °C, for thymine, as in the experiment of Imhoff et al.32 The thymine molecule was condensed onto a 3 monolayers (ML) Ar spacer11–21 to physically isolate the molecule from the Pt substrate and avoid potential interactions with this latter.12,14,16,33 From measurement of the attenuation of the specular reflectivity of the Ar substrate,34 we deduced a thickness of 1.5 monolayers (ML) of thymine for each spectrum recorded in the present study. To extract absolute vibrational CSs of thymine, each spectrum is fitted using the sum of Gaussian functions that represent a vibrational mode of thymine.11–18,20,21 The absolute CS values for each vibrational mode is calculated using the area under the corresponding Gaussian with the single scattering model (eqn (1) in paper I). The surface number density (ns) used in the calculations of the CSs values is 2.1 × 1014 molecules cm−2 (±10%) for a disordered film of thymine.13,35 More details on the scattering model and the experimental method are given in paper I and ref. 13.

Regarding the absolute vibrational CS values of condensed THF, they were measured recently in 2016.18 The deoxyribose cannot be injected into our system due to its degradation during the sublimation process. THF was used in 2016 as an analogue of the deoxyribose.18 These measurements provide the best data set, representative of the sugar group, readily available for comparison with our new CS results for thymidine.

III. Results and discussion

A. Correction of absolute CSs values of thymine

Lévesque et al.13 measured the vibrational CSs of condensed thymine in 2003. Since then, changes have been made to the apparatus and the CS measurement procedure. Because of the potential for systematic error in the earlier measurements/calculations of CS values and to allow for a more precise and significant comparison, it was decided to remeasure the CSs for thymine with the same updated apparatus that served to record the dT and the THF data. Accordingly, the new HREEL spectra for thymine recorded using the present system can also be compared with those of Lévesque et al.13 Fig. 2 shows the EEL spectrum for 1 ML of thymine as measured by Lévesque et al.13 and the new one measured for 1.5 ML of thymine, both at an incident energy of 8.5 eV. It is clearly seen that the upgraded apparatus exhibits superior resolution (i.e., 23 meV compared to 28 meV FWHM for the measurements of Lévesque et al.) and signal-to-noise ratio. These differences can be attributed to incremental upgrades made to the apparatus, since the publication of the work of Lévesque et al., as well as to refinements in the experimental protocol (e.g., the deposition method). Hence, in the present EEL spectrum, the vibrational structures are more easily observable, particularly the breathing mode, around 98 meV, which is almost completely lost within the elastic peak in the EEL spectrum of Lévesque et al. Nonetheless, it is possible to correlate all the structures observed here to the ones identified in the previous work.
image file: c9cp03448j-f2.tif
Fig. 2 Comparison of electron energy loss (EEL) spectra measured by Lévesque et al.13 (top panel) and in the present study at an incident electron energy of 8.5 eV. Lévesque et al. used 1 ML of thymine on Ar, while 1.5 ML of thymine was deposited onto Ar in our study.

In the present study, six new EEL spectra of thymine were measured at incident electron energies of 2, 3, 4, 8.5, 12 and 16 eV. The spectra were fitted by assigning a Gaussian function to each of the vibrational modes of Lévesque et al. The CS values are then obtained for each vibrational mode as a function of incident energy (see method and eqn (1) in paper I). Thereafter, these vibrational CSs are summed for each incident energy and the same procedure is applied to the data of Lévesque et al., to compare both total absolute vibrational CSs. These total vibrational CS values are shown in Fig. 3 and it is seen that the magnitude of the total CS values of Lévesque et al. is much larger than that of the present measurements. It should be noted that the absolute CSs are independent of the experimental parameters (i.e., incident current used and the number of layers deposited) since these are considered by the single scattering model. Thus, the large discrepancies likely derive from an error in the measurement/estimation of experimental parameters (i.e., incident current, number of molecules on the surface) or simply in the calculation of the CSs using the scattering model. It is possible that an error of calculation and/or number of condensed molecules occurred, since it was the first time in 2003 that this model was applied and the oven operated. By multiplying the data of Lévesque et al. with a factor 1/3, their values fit almost exactly the ones measured in this present work, as we can see in Fig. 3. The divided values show the exact same trend as the new data, which suggests that their CSs can be corrected by this coefficient alone. When comparing the order of magnitude of the CSs of Lévesque et al. for thymine to those of subsequent works on similar bases (cytosine and pyrimidine),11–16 it is clear that their values are considerably larger. The order of magnitude that is obtained in these present measurements (when dividing the values of Lévesque et al. by 3) correlates well with the one obtained in the studies of the other bases.11–17 Hence, the corrected absolute values are used for the rest of this paper and referred to as “corrected CS values of Lévesque et al.”. Using the two sets of data (the new measurements and the corrected ones of Lévesque et al.), the uncertainties of the corrected data values of thymine are estimated to be about ±16%.


image file: c9cp03448j-f3.tif
Fig. 3 Total absolute vibrational cross sections as a function of incident electron energy for thymine. These values correspond to the sum of the CSs of each vibrational mode identified in the electron energy spectra of thymine. Lévesque et al.13 (●); present study (○); data of Lévesque et al.13 multiplied by a factor 1/3 (+).

B. Comparison of interactions of LEEs with dT, thymine and THF

a. Vibrational spectra comparison. Fig. 4 and Fig. S1 in ESI compare EEL spectra for thymine, THF and dT measured with 4 and 8.5 eV incident electrons, respectively. Each observable vibrational mode of dT is related to a mode found in one or both constituents. The assignments for each of these vibrational excitations are explained in paper I. The only vibrational mode observed in dT not present in the EEL spectra of either constituent (thymine and THF) is the stretch mode of the OH group contained in the deoxyribose of dT, which is not present in THF. The latter only represents the ring of deoxyribose. When comparing the three molecules, it is interesting to note that the EEL spectra of dT most closely resembles those of thymine. Previously, it was shown from Raman data that dT vibrations are dominated by thymine modes.36 Nevertheless, the vibrational spectrum of dT contains contributions from the vibrational modes of both deoxyribose and thymine. The structure found around 375 meV in dT (related to the stretching of CH groups) is similar in terms of shape and intensity to the one found in thymine. On the other hand, the structure at 131 meV clearly relates to the C–O–C stretch of THF. Hence, since each structure observed in the EEL spectrum of dT is related to a vibrational mode of THF and/or thymine, it is possible to compare their absolute CSs in order to investigate the variations induced when two constituents are united by chemical bonds. This quantitative comparison is the subject of the next subsection.
image file: c9cp03448j-f4.tif
Fig. 4 EEL spectra recorded with incident electrons of 4 eV for thymidine (dT), thymine and tetrahydrofuran (THF). Vertical dashed lines represent the position of vibrational modes found in thymine (black lines) and THF (red lines). The EEL spectrum of THF is reproduced from Lemelin et al. 2016.18
b. Vibrational CSs of dT, thymine and THF. Fig. 5 shows the incident energy dependence of the CSs for each vibrational mode identified in dT, thymine and THF. The error bars for the vibrational CSs of each molecule showed in Fig. 5 correspond to the total absolute uncertainties of ±28% for dT, ±28% for THF18 and ±16% for thymine. Generally, these yield functions resemble broad structures that exhibit maxima in the 2–6 eV region and decrease in intensity with increasing incident energy. These broad features are probably composed of overlapping short-lived resonances, which control the magnitude of the CSs between 1 and 14 eV. The CS values of thymine are the corrected ones of Lévesque et al.,13 the CSs of THF comes from our previous work18 and those of dT are presented in paper I. Similarities are observed between the incident energy dependence of the CSs of several vibrational modes. Effectively, multiple vibrational CSs of THF or thymine show roughly the same incident energy dependence for the corresponding vibrational excitation of dT, as well as the same magnitude. It is the case for the vibrational modes at 131, 210, 357 and 417 meV. This result suggests that even if thymine and THF are paired to form dT, the LEE has the same probability to excite these vibrational modes in dT as if the constituents were isolated. Hence, for these vibrational excitations, it seems that no difference is produced by the presence of the other constituent.
image file: c9cp03448j-f5.tif
Fig. 5 Variation with electron impact energy of the cross sections (CSs) for various vibrational modes of thymidine (dT), thymine and tetrahydrofuran (THF). CSs of vibrational modes of thymine and THF are always compared to the corresponding modes of dT. CSs values of dT are reproduced from paper I; those of thymine are the corrected CSs of Lévesque et al.13 and those of THF are reproduce from ref. 18.

In other cases, some vibrational modes of dT relate to modes found in both molecules. It is the case for the mode around 150 meV of dT (related to the modes at 146 and 150 meV of THF and thymine respectively), the vibrational mode of dT at 182 meV (related to the modes at 181 and 180 meV of THF and thymine respectively) and the vibrational mode of dT at 375 meV, which is found at 371 meV in THF and 375 meV in thymine. It is interesting to observe that the CSs of these three modes of dT never correspond to the sum of the CSs of its two constituents. On the contrary, above 6 eV, the CSs of dT is generally equal to the CSs of the corresponding modes of THF and thymine, except for the mode at 375 meV, where surprisingly the CSs of dT is lower than the CSs of its two constituents. Two other surprising results are observed for the modes found at 98 meV and 114 meV. The magnitude of the CS values for these vibrational modes is greatly attenuated in dT reaching only 25% of the magnitude of thymine and THF at the resonance around 4 eV. Since these modes are two adjacent losses in the EEL spectra of dT, the weakness of their CSs is not induced by the fitting process, which can sometimes cause the overestimation of one mode over another with slightly different energy. This suggests that these two modes are quenched in dT; when the two constituents are linked together. By studying the assignments of each of these modes, we can attempt to explain these results.

The mode at 98 meV is related to the breathing mode of thymine; the simultaneous contraction and relaxation of the bonds of the thymine ring. The other mode at 114 meV, which corresponds to the C–C stretch of the ring of THF is similar to a ring breathing mode, but not necessarily in phase. Hence, these two correspond to collective excitations of the links between a large number of atoms of the molecules. One possible explanation of this result is that the symmetry of each isolated molecule may be altered by the presence of the other, which causes the collective modes to be weakened in intensity. The collective modes are probably more sensitive to bonding with another molecule than the other vibrational modes involving two atoms. Similarly, Regeta et al.37 studied the C[double bond, length as m-dash]C vibrational mode of cis- and trans-cyclooctene by HREELS and they observed quenching of this vibration for the trans configuration. They explained this result by the modified symmetry between the two configurations which supports our present result.

The energies of resonances or transient anions (TAs) observed in each set of CSs can also be compared. Firstly, the resonance found in thymine13 at 4 eV is probably related to the same one found in the CSs of dT for the modes expressed in these two molecules (the modes at 150, 181, 210, 375 and 417 meV). However, the strongest resonance in THF18 around 4.5 eV seems to be slightly downshifted in dT by 0.5–1 eV for the corresponding vibrational modes (131, 146, 181, 357 and 371 meV). The resonance of THF could be affected in dT by the presence of the thymine moiety. Also, THF only represents the ring of the deoxyribose contained in dT, which can alter the energy position of the resonances. Antic et al.38 studied the dissociative electron attachment (DEA) of three deoxyribose analogs of different complexity: THF, 3-hydroxytetrahydrofuran and α-tetrahydrofurfuryl alcohol and they observed shifts in the energy of the resonances. The strongest resonance found was around 10.4, 10.2 and 10 eV for THF, 3-hydroxytetrahydrofuran and α-tetrahydrofurfuryl alcohol, respectively. The downshifts of 0.2 and 0.4 eV observed for the molecules with the added OH (3-hydroxytetrahydrofuran) and the added CH2OH (α-tetrahydrofurfuryl alcohol) demonstrate that the energy of resonances does vary according to supplementary molecular groups. Hence, the downshifts observed in the present work between the resonances of dT and THF could be, at least partially, due to the complete deoxyribose moiety contained in dT.

c. Comparison of total vibrational CSs values. Each set of absolute vibrational CSs have been summed for comparison and they are presented as a function of incident electron energy in Fig. 6. Below 4 eV, the total vibrational CS of dT is greater than each of its two constituents, and around 2 eV, it corresponds roughly to the sum of the CSs of THF and thymine. This result is anticipated due to the geometrical molecular size of thymidine, which is roughly two-fold larger than that of THF and thymine and because CSs are expected to increase with increasing molecular size.39–44 For incident electron energies of 2 to 4 eV, the total vibrational CSs of dT increase, but not as rapidly. In this energy range, the total CSs of dT do not correspond to the sum of the total CSs of the constituents; only accounting for about 85% of the sum of the CS values of thymine and THF at 3.5 eV. Around the resonance at 4.5 eV, this percentage drops to ∼60%. More surprising, above 6 eV, the magnitude of the total vibrational CSs of dT becomes almost comparable to the magnitude of the CSs of THF and about 15% higher than the total vibrational CSs of thymine at 10 eV. Hence, the total CS values of dT are clearly not the sum of its two constituents above 4 eV.
image file: c9cp03448j-f6.tif
Fig. 6 Total absolute vibrational cross sections (CSs) as a function of incident electron energy for thymidine (dT) (●), thymine (red ▲) and tetrahydrofuran (THF) (blue ■). These values correspond to the sum of the CSs of each vibrational mode identified in the electron energy spectra of each molecule, showed in Fig. 5. The sum of the total vibrational CSs of THF and thymine is represented by ⊕ (green). The uncertainties related to the CSs values for dT, THF, thymine and the sum (thymine + THF) are ±28, ±28, ±16 and ±18% respectively.

Winstead et al.45 compared the calculated integral elastic CSs (ICSs) for LEEs (0–20 eV) scattering from thymine and dT. The magnitude of the ICSs of dT are roughly 80% higher than the ICSs of thymine; supporting the idea that CSs increase according to the molecular size. This result is similar to the trend observed in the present results for incident energies under 4 eV. However, it does not explain the behavior that we observe at higher energies. On the other hand, it was shown in previous experimental and theoretical studies that the magnitude of the electron CSs does not only depend on the molecular size. Makochekanwa et al.44 measured the total CSs for electrons of 0.4 to 1000 eV scattering from benzene (C6H6) and the geometrically bigger molecules related to benzene, i.e., 1,4-C6H4F2, 1,3-C6H4F2, C6H5Cl and C6H5F. It was shown that the total CSs for electron scattering from benzene molecules are greater than any of the other larger molecules. This surprising result was not explained by the authors and no mechanism nor hypothesis was proposed. Since they observed this kind of behavior by only swapping one or two hydrogens of benzene (a fairly simple molecule) by bigger atoms, it is perhaps not too surprising to observe counterintuitive results, when studying complex molecules such as THF, thymine and dT. Moreover, in their theoretical work, Mozejko and Sanche46 compared the sum of calculated ionization CSs of H3PO4 and C5H10O2 (models of phosphate and sugar group respectively) to the calculated ionization CSs of the entire sugar–phosphate unit of the backbone of DNA for 10–4000 eV electrons. Interestingly, the magnitude of the summed CSs is distinctively greater than the sugar–phosphate unit reaching 27% higher at 20 eV.

The behavior observed in our results at high energy is not easily explained, since many factors can be responsible for the variations of the magnitude of vibrational CSs. When a supplementary electron is temporarily captured by a molecule, it creates a TA (i.e., a compound state or resonance).47–50 As explained in paper I, shape resonances are highly effective in causing vibrational excitation. In such a resonant process, the incoming electron wave tunnels through the electron-molecule potential to occupy quasi-bond energy level.51 The repulsive part of this potential is the centripetal barrier constructed from the partial wave content of the scattering electron.52 Usually at low energy (0–5 eV), this barrier arises from low-momentum (l = 1 and 2) partial waves, whereas at higher energy, higher ones also contribute to the potential that retains the additional electron within the target molecule for a time much larger than its non-resonant scattering time.52 When two molecules are bound together, the scattering waves of the individual components are necessarily perturbed, particularly the larger-momentum partial waves due to overlap of the individual wave functions. In other words, higher-energy resonances may have their repulsive barrier weakened and hence the retention of faster electrons may be more difficult. The effect of such resonances on vibrational excitation may therefore be more easily suppressed in the bonded configuration, as observed experimentally (Fig. 6). During the lifetime of a shape resonance, motion of the atoms forming the molecule is initiated to reach the inter-nuclear equilibrium distances of the TA.53 Since in shape resonances the extra-electron orbital is usually antibonding, the latter distances are different than those of the ground state neutral.54 After the autodetachment of the additional electron, the nuclei return to their initial positions of the ground molecular state. This process amplifies vibration of the nuclei.53,54 However, due to the symmetries of the orbitals involved, some selection rules apply, and only certain vibrational modes become excited via the autoionization channel. Chemically bonding thymine and THF is likely to lower the symmetry of the TA states of the individual components and thus change their electron capture CSs and lifetimes as it was shown by Allan and Andric55 when studying the resonances of cyclic and linear alkanes. The net effect should be a reduction in the amplitude of the stretching of the nuclear coordinates and therefore the magnitude of the vibrational CSs.52 Finally, these amplitudes would be modulated by the modified Franck–Condon factors.

When studying the full width at half maximum (FWHM) of the main resonance in each set of total vibrational CSs in Fig. 6, it is possible to observe an enlargement of the main resonance for dT relative to that in thymine or THF. Indeed, the FWHM for the resonance of dT is about 5.1 eV compared to 4.5 and 4 eV for thymine and THF respectively. This resonance enlargement by 0.6 to 1.1 eV suggests that in the case of dT, the linking of two molecules to form one can effectively reduce TA symmetry, which reduces the lifetime and the magnitude of the CSs. Hence, the CSs of this complex molecule will not be equal to the sum of the CSs of its constituents.

As discussed above, experimental and theoretical studies seem to contradict themselves, demonstrating that more studies are required to elucidate the types of behavior we observe here. It seems that the naive concept of CSs depending exclusively on the molecular size is not always applicable and that the problem of predicting CS for large polyatomic molecules is certainly more complex than a simple addition of the CSs of each unit to model a complex molecule. These results show that when modelling such complex molecules (as a nucleoside or a DNA chain), the sum of the CSs of its constituents may not be as reliable as a directly measured experimental CSs of the entire molecule. Monte Carlo simulations that employ the sum of CSs of various fundamental units to model a complex molecule such as DNA are ultimately introducing errors in their calculations. Nevertheless, at this moment, the CSs of each isolated constituent are still the best available values to model interactions of LEEs with DNA and its fundamental units. New theoretical studies could tackle this problem to help modelling more precisely the variations induced when two or more molecules are paired. Also, more experimental investigations are needed to produce absolute CSs for molecules of increasing complexity in order to represent as close as possible the biological reality.

IV. Summary

We have conducted the first quantitative and comparative study of the absolute vibrational CSs for LEE scattering from condensed dT and its two constituents: thymine and THF. Firstly, the CSs of thymine previously measured in 2003 by Lévesque et al. have been remeasured with our current HREELS system and corrected by a factor 1/3. In any simulations of radiation dose or radiobiological damage entering as input parameters the CS values for thymine of Lévesque et al.,13 it would be important to apply this correction factor.

Secondly, the EEL spectra for each molecule were compared and all the vibrational excitations of dT were identified and related to the vibrational modes of thymine and/or THF. The incident electron energy dependence of the CSs of each vibrational mode of dT were compared to the corresponding vibrational CSs of thymine and/or THF. It was found that the incident energy dependence of the vibrational CSs of dT closely resemble, in terms of magnitude and features, those of its constituents for the modes at 131, 210, 357, 417 meV. Surprisingly, the modes responsible for ring breathing of thymine and the C–C stretch of THF are strongly attenuated in dT. This result indicates that collective modes are selectively weakened, by the possible alteration of the symmetry of the molecules, when they are paired to form dT. When comparing the total CSs of each molecule, it was shown that the total CSs of dT is roughly equal to the sum of the total CSs of each constituent at 2 eV and about 80% of the sum at 3.5 eV. However, at higher energy, the magnitude of the total CSs of dT becomes similar to those of its constituents. Obviously, more work is needed at experimental and theoretical levels to elucidate this behavior. To improve the present comparison, it is desirable to measure the vibrational CSs of a better model of the deoxyribose (contained in dT), such as the 3-hydroxytetrahydrofuran and α-tetrahydrofurfuryl alcohol. It would also be instructive to investigate the electronic excitation CSs of the three molecules, make the same comparisons as we did in this present work and study CS variation when a OH and/or CH2OH group is added on THF.

The present study demonstrates that the addition of absolute vibrational CSs of basic units to model a complex molecule (i.e., nucleoside or short DNA strand) is not as reliable as measuring the CSs of the entire molecule. The absolute CS values for each isolated constituent are still the best data available, but this present study shows that the experimental limits restraining measurements of CSs for complex molecules need to be surpassed. Our analysis also suggests that once the symmetries of the TAs and vibrational modes of simple molecular units of a large biomolecule are identified, it should be possible to estimate theoretically the vibrational CSs of larger one from the experimental CSs of the smaller basic units. In fact, Caron et al.56 have shown that by incorporating in a quantum mechanical calculation, the scattering matrix elements of basic units of DNA, LEE elastic scattering CSs from this molecule can be calculated. Thus, considering the difficulties in generating experimentally LEE-CS values for large biomolecules, these suggested approaches may be promising for modelling applications. Measurements of LEE CSs for scattering from DNA and its various constituents, such as we present in these papers, are most pertinent to modeling direct processes occurring within the DNA of the nucleus. However, in the nucleus DNA is bound to histone proteins, that pack and support the DNA and to the water molecules of the hydration shell. Since the local molecular environment can significantly modulate electron scattering there is increasing interest to know how water, proteins and other molecules affect LEE induced processes in DNA.57,58 For example measurements of the electron stimulated desorption of anions from short oligonucleotides onto which 3 ML of water molecules had been added indicated the formation of DNA-H2O complex TAs.28 Moreover the DEA process occurring on DNA hydrated bases has been studied theoretically by molecular dynamical simulation59 and in micro-solvation cluster phase experiments.24,60 Hence in the future, measurements that include water molecules in close proximity to biomolecules will be undertaken to produce CSs one step closer to the cellular environment.

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

V. Lemelin gratefully acknowledges the financial support from the Fonds de Recherche du Québec – Santé (FRQS) in the form of a doctoral research award. This research is supported by CIHR grant PJT-162325.

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Footnote

Electronic supplementary information (ESI) available. See DOI: 10.1039/c9cp03448j

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