J. Phys. Chem. B 2005, 109, 7749-7757
7749
Electronic Structure of the Nucleobases
J. MacNaughton* and A. Moewes
Department of Physics and Engineering Physics, UniVersity of Saskatchewan, 116 Science Place, Saskatoon,
Saskatchewan S7N 5E2, Canada
E. Z. Kurmaev
Institute of Metal Physics, Russian Academy of Sciences Ural DiVision, 620219 Yekaterinburg GSP-170, Russia
ReceiVed: August 16, 2004; In Final Form: February 11, 2005
We present a comparison between experimental and calculated soft X-ray spectra of DNA’s nucleobases,
adenine (A), guanine (G), cytosine (C), and thymine (T) using X-ray absorption spectroscopy (XAS) and soft
X-ray emission spectroscopy (XES). Spectra of the 1s thresholds of carbon, nitrogen, and oxygen give a
complete picture of the occupied and unoccupied partial density of states of the nucleobases. A combination
of both Hartree-Fock and density functional theory calculations are used in the comparison to experimental
results. Most experimental results agree well with our theoretical calculations for the XAS and XES of all
bases. All spectral features are assigned. A comparison of the experimental highest occupied molecular orbitallowest unoccupied molecular orbital energy gaps is made to the diverse values predicted in the literature.
1. Introduction
The desire to build devices on the nanoscale has led to an
interest in molecular electronics research. DNA may be a
suitable candidate for nanowires because of its ability to selfassemble, its molecular recognition abilities, and the fact that
it is widely available.1 Currently, the main limiting factor seems
to be controversy regarding the efficiency of DNA as an
electrical conductor. Heavily debated in the literature, contradictory results have been reported indicating insulating,2-5
semiconducting,6-8 highly conductive,9 or even superconducting10 behavior for the molecule. The complexities involved with
interactions of DNA and its surrounding environment as well
as the large number of atoms involved in the molecular system
create significant challenges in designing experiments and the
theoretical models required to gain understanding about its
electronic structure.
The physical structure of the DNA molecule consists of a
right-handed helical stack of complementary pairs of nitrogenous
bases supported by a sugar (deoxyribose) and phosphate
backbone. The four nucleobases are aromatic ring-type structures
and are adenine (A), guanine (G), cytosine (C), and thymine
(T). The molecular structures of the bases are displayed in Figure
1. The atoms in the structures are numbered for identification
purposes in the theoretical results.
A systematic approach to understanding the complicated
electronic structure of DNA is to first examine the electronic
structures of its main components. Several recent theoretical
attempts have been made to study electronic properties of
isolated nucleobases and homonucleotide base stacks11-17 but
do not include predictions of spectroscopic results. While the
majority of these studies utilize the density functional theory
(DFT) methodology, Hartree-Fock and AM1 techniques were
also investigated. The calculated highest occupied molecular
orbital (HOMO)-lowest unoccupied molecular orbital (LUMO)
* Author to whom correspondence should be addressed. Phone: (306)
966-6380. Fax: (306) 966-6400. E-mail:
[email protected].
Figure 1. Molecular structures of the four DNA bases, (a) adenine,
(b) guanine, (c) cytosine, and (d) thymine.
gaps for these types of systems is found to vary (see, for
example, refs 11 and 13).
In this study, the experimental soft X-ray absorption spectra
(XAS) and X-ray emission spectra (XES) for all C, N, and O
are compared to calculated spectra for the four nucleobases of
DNA. Some previous experimental work has been done
primarily with energy loss spectroscopy18 and X-ray absorption
of the nucleobases.19-21 This is the first comprehensive study
including detailed experimental and theoretical results for both
absorption and emission spectroscopy for all three edges (C,
N, and O). The main transitions in the XAS and XES spectra
are identified. Our experimental values of the HOMO-LUMO
energy gaps are related to our calculated values as well as
compared to the very different values given in the literature.
10.1021/jp0463058 CCC: $30.25 © 2005 American Chemical Society
Published on Web 04/02/2005
MacNaughton et al.
7750 J. Phys. Chem. B, Vol. 109, No. 16, 2005
TABLE 1: Nucleobase Geometry Optimized by StoBe
bond lengtha (Å)
CsC
CdC
CsN large ring
CsN small ring
CdN large ring
CdN small ring
CsNH2
CsH (ring)
NsH (ring)
NsH (amino)
CdO
CsCH3
CsH (methyl)
a
adenine
guanine
cytosine
thymine
1.418
1.405
1.350
1.387
1.351
1.323
1.358
1.094
1.020
1.015
1.442
1.405
1.396
1.386
1.325
1.318
1.369
1.091
1.021
1.014
1.231
1.442
1.365
1.392
1.468
1.360
1.397
1.331
1.365
1.093
1.020
1.016
1.232
1.094
1.022
1.233
1.502
1.103
Bond length is averaged when there are multiple occurrences.
the ionization potentials for the samples. Good agreement with
theoretical predictions is another indicator that the measured
spectra do not have significant contributions from carbon
contamination.
3. Calculations
Figure 2. Experimental and theoretical carbon 1s soft X-ray absorption
(XAS) spectra for (a) adenine, (b) guanine, (c) cytosine, and (d)
thymine. Experimental spectra are displayed with black lines, and
calculated spectra are shown with gray lines. The offset used for the
y-scale is 35%.
2. Experimental Section
The soft X-ray spectroscopic measurements were performed
at beamline 8.0.1 at the Advanced Light Source synchrotron
located at the Lawrence Berkeley National Laboratory. The
X-ray absorption spectra were measured in total fluorescence
yield (TFY) mode for the nucleobases. The resolving power
E/∆E for the absorption spectra is about 5000 for the carbon,
nitrogen, and oxygen edges. For the fluorescence spectra, the
emitted radiation is partially collected in a Rowland circle-type
spectrometer with spherical gratings and recorded with an areasensitive multichannel detector. The details of this endstation
are described elsewhere.22 Total experimental resolution in the
KR X-ray emission region is 0.4 eV full width at half-maximum
(FWHM) for carbon, 0.75 eV FWHM for nitrogen, and 1.2 eV
FWHM for oxygen. All absorption and emission spectra are
normalized to the number of photons falling on the sample,
monitored by a highly transparent gold mesh in front of the
sample. Samples of the four nucleobases were purchased from
Sigma and measured in powder form. Energy calibration was
completed by using measurements of reference samples and by
shifting the energy using literature values. For these calibrations,
highly oriented pyrolytic graphite23 was used for the carbon
edge, hexagonal boron nitride (h-BN)24 was used for the nitrogen
edge, and TiO2 25 was used for the oxygen edge.
The carbon edge is often affected by contamination of the
optical beamline components. When the experimental data were
obtained, the Au mesh had been refreshed by evaporating a fresh
layer of Au on it. To ensure features in the spectra are real and
not introduced by the normalization process, the mesh current
(Io) was examined. The XAS spectra before normalization
contain the same features as the final spectra displayed in Figure
2. The main contribution that normalization to Io has for the
spectra displayed is a slight change in slope in the features after
Results from two different calculation programs are used to
model the experimental spectra. The program GSCF326 was used
for X-ray absorption calculations and involves an ab initio selfconsistent field (SCF) calculation of the core-excited and coreionized states with explicit consideration of the core-hole.27
The improved virtual orbital method involving the relaxed
Hartree-Fock potential was used to obtain the core-excited
states.28 The transitions to the unoccupied molecular orbitals
were determined and correspond especially well to the transitions to the π* orbitals in the experimental XAS spectra for the
four nitrogenous bases. A separate calculation was performed
for each atom of interest with nonequivalent symmetry, and the
results are summed into a final spectrum. Huzinaga-type basis
sets29 were used for the calculations, with the contraction
schemes (411121/3111) with a polarization function being used
for heavy atoms with the core-hole, (621/41) being used for
heavy atoms without the core-hole and (41) being used for
the hydrogen atoms. Gaussian line widths used in the production
of the simulated spectra from the calculated oscillator strengths
were 0.7 eV FWHM up to the ionization potential and 4.0 eV
FWHM beyond. These line widths were chosen to correspond
to the experimentally observed results.
The second calculation program used to calculate spectra is
StoBe30 and is software designed to analyze electronic structure
of molecules, with a focus on inner-shell spectroscopies. This
approach uses a linear combination of Gaussian-type orbitals
approach to form self-consistent solutions of the Kohn-Sham
DFT equations. All calculations using StoBe used the gradientcorrected Becke (BE88)31 exchange functional and the Perdew
(PD86)32 correlation functional. The orbital basis set used for
the nitrogen, carbon, and oxygen atoms was a triple-ζ valence
plus polarization and had the following form (7111/411/1*).
Hydrogen atoms were represented by the double-ζ valence plus
polarization scheme (311/1).
The StoBe program calculated the X-ray absorption spectra
using a combination of the transition potential method and a
double basis set technique incorporated into density functional
theory.33 To more accurately define the core-hole state, the
non-core-excited atoms were represented by effective core
potentials.34 For better representation of relaxation effects, the
atom with the core-hole was described by the IGLO-III basis
Electronic Structure of Nucleobases
J. Phys. Chem. B, Vol. 109, No. 16, 2005 7751
TABLE 2: Assignment of Spectral Features for the C 1s Absorption Data
A
1
2
3
4
a
G
transitiona
oscillator
strength
(× 10-3)
C2 f 7a′′
C2 f 8a′′
C3 f 7a′′
C5 f 7a′′
C1 f 7a′′
C2 f 9a′′
C2 f 26a′
C4 f 7a′′
C4 f 8a′′
C5 f 8a′′
C1 f 8a′′
C2 f 27a′
C3 f 8a′′
C5 f 9a′′
C5 f 26a′
C1 f 9a′′
C1 f 26a′
C2 f 28a′
C2 f 29a′
C2 f 30a′
C3 f 26a′
C3 f 9a′′
C4 f 9a′′
C4 f 26a′
C5 f 27a′
0.611
3.876
9.357
9.526
9.106
1.313
0.062
3.463
6.043
0.847
0.743
0.151
0.003
0.771
0.070
1.203
0.048
0.024
0.003
0.084
1.243
1.117
0.784
0.208
0.179
1
2
3
4
C
transitiona
oscillator
strength
(× 10-3)
C2 f 8a′′
C2 f 9a′′
C2 f 29a′
C3 f 8a′′
C2 f 30a′
C2 f 10a′′
C3 f 9a′′
C4 f 8a′′
C1 f 8a′′
C2 f 32a′
C2 f 33a′
C3 f 30a′
C3 f 10a′′
C4 f 29a′
C4 f 30a′
C5 f 8a′′
C1 f 9a′′
C1 f 29a′
C3 f 31a′
C3 f 32a′
C4 f 10a′′
C4 f 31a′
C5 f 29a′
C5 f 9a′′
3.046
0.202
0.150
9.119
0.145
1.830
0.020
8.511
11.35
0.050
0.021
0.993
0.794
0.022
0.207
12.37
0.046
0.207
0.194
0.527
1.215
0.127
0.023
0.015
1
2
3
4
5
T
transitiona
oscillator
strength
(× 10-3)
C1 f 6a′′
C2 f 6a′′
C1 f 22a′
C1 f 23a′
C3 f 6a′′
C1 f 25a′
C1 f 26a′
C1 f 8a′′
C2 f 22a′
C2 f 7a′′
C3 f 7a′′
C4 f 6a′′
C2 f 24a′
C3 f 22a′
C3 f 23a′
C4 f 7a′′
4.996
10.80
1.705
0.160
8.418
1.042
0.318
0.334
2.356
0.026
4.053
11.06
0.327
0.170
0.082
2.798
1
2
3
4
5
transitiona
oscillator
strength
(× 10-3)
C1 f 7a′′
C2 f 7a′′
C1 f 24a′
C1 f 25a′
C3 f 7a′′
C5 f 24a′
C5 f 8a′′
C1 f 9a′′
C1 f 27a′
C2 f 25a′
C3 f 8a′′
C4 f 7a′′
C5 f 26a′
C5 f 9a′′
C2 f 9a′′
C2 f 28a′
C3 f 24a′
C4 f 8a′′
C5 f 10a′′
4.667
9.358
0.031
0.215
10.01
1.178
0.068
2.092
0.682
0.020
2.772
12.54
3.049
3.550
0.363
0.683
0.206
2.479
1.813
Transitions are from the core level in the labeled atom (labels from Figure 1) to the given unoccupied state.
set.35 The StoBe calculations for the XAS were completed using
the Cs symmetry group. This allows the main features of the
absorption to be labeled with the specific transitions that are
occurring. These theoretical spectra have been broadened in the
same way as the GSCF3 results for comparison purposes.
All nonresonant X-ray emission spectra for the nucleobases
were calculated using the StoBe code. The valence-core level
transitions in these calculations are based on the calculated
ground-state Kohn-Sham orbitals.36 Similar to the XAS
calculations, the StoBe XES calculations were completed using
the Cs symmetry group. This allows the main features of the
emission to be labeled. The theoretical discrete emission rates
for each constituent were Gaussian-broadened with a constant
line width of 0.7 eV FWHM for the N and O edges and a line
width of 1.0 eV FWHM for the C edge. The broadened results
from the individual atoms were summed into a final spectrum
for each element that is compared to the experimental results.
Information regarding geometry for these planar molecules,
optimized by the StoBe program, is found in Table 1. For all
cases, the theoretical spectra have been shifted in energy to align
with the experimental data. For the XAS data, the calculated
spectra were shifted to line up with the first low-energy π*
feature. In the case of the XES, the theoretical data were moved
to align with the high-energy edge. The minimum has been set
to zero for all spectra. The labeling for the XAS and XES
features corresponds to the two separate absorption and emission
calculations done with the StoBe program. In the absorption
calculation, the core-hole effects are included and therefore
have a shifting effect on the orbital energies. This results in a
slight overlap in the orbital naming scheme between the two
techniques. (For example, in the case of the carbon edge for
guanine, the orbital 31a′ shows up as an unoccupied state and
occupied state depending on if you look at the labeling for the
XAS or XES). This is not considered a large concern since the
symmetry of the orbitals is still accurate (a′ or a′′), the oscillator
Figure 3. Experimental and theoretical nonresonant carbon KR
emission spectra for (a) adenine, (b) guanine, (c) cytosine, and (d)
thymine. Experimental spectra are displayed with black lines, and
calculated spectra are shown with gray lines.
strengths are precise and comparisons can still be made
successfully within the XAS or the XES results.
4. Results and Discussion
Figure 2 shows the carbon 1s XAS spectra for two doublering purines, (a) adenine and (b) guanine, and the two single-
MacNaughton et al.
7752 J. Phys. Chem. B, Vol. 109, No. 16, 2005
ring pyrimidines, (c) cytosine and (d) thymine. These experimental results agree with previously published electron energy
loss spectra for adenine and thymine.18 Calculations were
completed using both the GSCF3 and the StoBe program. The
agreement between theoretical and experimental data is good
in the region of the lower-energy features that result from the
excitation of the carbon 1s core electron to the π* unoccupied
orbitals. The broader feature, located at higher energy, is a result
of several excitations to σ* unoccupied states. By calculating
each carbon site individually using GSCF3, theoretical results
indicate that for the relatively simple pyrimidine molecules each
sharp peak is a result of a π* feature that corresponds to a
specific nonequivalent carbon site. These features in the GSCF3
spectra are numbered C1 through C4 to correspond to the carbon
sites labeled in Figure 1. The nonequivalent sites are not as
obvious in the spectra of the purines in Figure 2, parts a and b,
because of peak overlap. These results and comparisons to
resonant inelastic X-ray emission spectra have been shown
previously.19 The results from the StoBe calculations allow
greater detail in labeling the features corresponding to bound
transitions in the spectra. The numbered features in the StoBe
spectra are described in detail in Table 2. Each arrow is labeled
with the transitions that are occurring in the region (0.3 eV
from the arrows energy location. In more common terms, the
a′ orbital has σ-like symmetry, and the a′′ orbital has π-like
symmetry. Although the spacings of the peaks in the GSCF3
calculations seem to correspond better to experiment than the
StoBe results, the details for the transitions that are occurring
agree in both theoretical methods. The results in Table 2 for
cytosine and thymine confirm the prediction from the GSCF3
Figure 4. Experimental and theoretical nitrogen 1s XAS spectra for
(a) adenine, (b) guanine, (c) cytosine, and (d) thymine. Experimental
spectra are displayed with black lines, and calculated spectra are shown
with gray lines. The offset used for the y-scale is 35%.
TABLE 3: Assignment of Spectral Features for the C Kr Emission Data
A
1
2
3
4
5
6
G
transition
oscillator
strength
14a′ f 6a′
15a′ f 7a′
15a′ f 9a′
17a′ f 6a′
18a′ f 7a′
19a′ f 10a′
20a′ f 7a′
21a′ f 7a′
20a′ f 8a′
21a′ f 8a′
22a′ f 10a′
22a′ f 6a′
23a′ f 7a′
23a′ f 8a′
23a′ f 9a′
24a′ f 10a′
25a′ f 10a′
25a′ f 6a′
2a′′ f 7a′
26a′ f 8a′
26a′ f 9a′
5a′′ f 6a′
28a′ f 7a′
5a′′ f 8a′
28a′ f 8a′
5a′′ f 9a′
6a′′ f 10a′
0.154
0.168
0.181
0.100
0.185
0.192
0.194
0.197
0.144
0.161
0.209
0.417
0.269
0.181
0.325
0.379
0.510
0.408
0.520
0.113
0.830
0.252
0.108
0.358
0.128
0.183
0.321
1
2
3
4
5
6
7
8
C
transition
oscillator
strength
15a′ f 7a′
16a′ f 7a′
16a′ f 8a′
17a′ f 10a′
19a′ f 8a′
20a′ f 9a′
22a′ f 11a′
19a′ f 7a′
20a′ f 8a′
21a′ f 9a′
22a′ f 9a′
23a′ f 7a′
24a′ f 7a′
25a′ f 8a′
1a′′ f 9a′
26a′ f 9a′
26a′ f 10a′
27a′ f 11a′
2a′′ f 11a′
1a′′ f 7a′
27a′ f 8a′
27a′ f 9a′
28a′ f 10a′
29a′ f 11a′
3a′′ f 7a′
3a′′ f 8a′
29a′ f 8a′
4a′′ f 9a′
4a′′ f 10a′
5a′′ f 11a′
31a′ f 9a′
32a′ f 11a′
7a′′ f 11a′
7a′′ f 9a′
7a′′ f 10a′
0.300
0.230
0.152
0.165
0.156
0.155
0.230
0.150
0.172
0.178
0.162
0.295
0.468
0.110
0.156
0.279
0.469
0.460
0.133
0.530
0.234
0.517
0.778
0.142
0.120
0.665
0.624
0.316
0.285
0.296
0.144
0.193
0.429
0.232
0.441
1
2
3
4
5
6
7
T
transition
oscillator
strength
12a′ f 6a′
14a′ f 5a′
14a′ f 6a′
14a′ f 7a′
16a′ f 8a′
17a′ f 8a′
19a′ f 6a′
19a′ f 7a′
1a′′ f 7a′
20a′ f 8a′
21a′ f 8a′
19a′ f 5a′
1a′′ f 5a′
1a′′ f 6a′
20a′ f 6a′
21a′ f 6a′
2a′′ f 6a′
21a′ f 7a′
3a′′ f 8a′
2a′′ f 5a′
22a′ f 5a′
3a′′ f 7a′
3a′′ f 5a′
23a′ f 8a′
4a′′ f 8a′
5a′′ f 8a′
23a′ f 6a′
5a′′ f 7a′
0.335
0.196
0.228
0.130
0.129
0.136
0.213
0.131
0.174
0.768
0.603
0.281
0.362
0.291
0.152
0.300
0.535
0.753
0.201
0.171
0.561
0.518
0.381
0.151
0.276
0.450
0.159
0.144
1
2
3
4
5
6
7
transition
oscillator
strength
12a′ f 5a′
13a′ f 6a′
16a′ f 7a′
16a′ f 8a′
15a′ f 5a′
17a′ f 6a′
18a′ f 8a′
17a′ f 5a′
18a′ f 7a′
1a′′ f 5a′
1a′′ f 6a′
21a′ f 6a′
21a′ f 7a′
22a′ f 7a′
2a′′ f 8a′
24a′ f 8a′
2a′′ f 9a′
24a′ f 9a′
25a′ f 9a′
22a′ f 5a′
2a′′ f 5a′
23a′ f 6a′
3a′′ f 6a′
25a′ f 7a′
4a′′ f 7a′
4a′′ f 5a′
27a′ f 8a′
6a′′ f 8a′
0.264
0.196
0.100
0.176
0.185
0.190
0.340
0.258
0.421
0.499
0.194
0.105
0.523
0.103
0.173
0.629
0.562
0.757
0.757
0.449
0.208
0.380
0.448
0.165
0.431
0.193
0.145
0.654
Electronic Structure of Nucleobases
J. Phys. Chem. B, Vol. 109, No. 16, 2005 7753
TABLE 4: Assignment of Spectral Features for the N 1s Absorption Data
A
1
2
3
4
a
G
transitiona
oscillator
strength
(× 10-3)
N2 f 7a′′
N4 f 7a′′
N5 f 7a′′
N5 f 8a′′
N1 f 7a′′
N2 f 8a′′
N2 f 26a′
N2 f 9a′′
N4 f 26a′
N4 f 9a′′
N4 f 27a′
N5 f 9a′′
N5 f 27a′
N1 f 8a′′
N1 f 26a′
N2 f 27a′
N3 f 7a′′
N4 f 28a′
N4 f 29a′
N4 f 30a′
N5 f 28a′
N5 f 29a′
N5 f 30a′
N1 f 27a′
N1 f 9a′′
N1 f 28a′
N2 f 29a′
N2 f 30a′
N3 f 26a′
N3 f 9a′′
5.890
4.318
1.689
4.581
1.427
1.423
0.151
1.508
0.017
2.443
0.189
0.211
0.054
0.262
1.371
0.179
3.501
0.054
0.006
0.050
0.017
0.193
0.075
0.321
0.392
4.702
0.047
0.004
3.167
1.043
1
2
3
4
5
C
transitiona
oscillator
strength
(× 10-3)
N2 f 8a′′
N2 f 9a′′
N2 f 29a′
N4 f 8a′′
N4 f 29a′
N4 f 9a′′
N1 f 29a′
N1 f 8a′′
N2 f 10a′′
N2 f 31a′
N3 f 8a′′
N4 f 10a′′
N4 f 31a′
N4 f 32a′
N5 f 29a′
N1 f 30a′
N1 f 31a′
N3 f 29a′
N3 f 30a′
N5 f 9a′′
N5 f 30a′
N1 f 10a′′
N1 f 32a′
N1 f 33a′
N3 f 32a′
N3 f 33a′
N5 f 32a′
N5 f 10a′′
N5 f 33a′
7.231
0.162
0.074
1.509
0.134
0.887
1.742
3.020
1.813
0.006
4.204
2.514
0.602
0.057
2.124
1.767
0.459
0.114
3.356
0.017
4.636
0.016
0.125
0.317
0.526
0.131
1.064
0.006
0.496
1
2
3
4
5
6
T
transitiona
oscillator
strength
(× 10-3)
N2 f 6a′′
N2 f 7a′′
N2 f 23a′
N2 f 24a′
N1 f 6a′′
N2 f 25a′
N3 f 6a′′
N1 f 23a′
N1 f 7a′′
N2 f 8a′′
N3 f 7a′′
N3 f 23a′
N1 f 24a′
N1 f 25a′
N3 f 24a′
3.415
0.001
0.049
0.779
1.146
0.572
2.056
2.047
0.801
3.273
1.361
1.547
1.171
3.763
0.994
1
2
3
4
5
transitiona
oscillator
strength
(× 10-3)
N1 f 7a′′
N2 f 7a′′
N1 f 8a′′
N2 f 8a′′
N1 f 27a′
N2 f 27a′
N1 f 28a′
N2 f 28a′
N1 f 29a′
N1 f 9a′′
N2 f 29a′
N2 f 9a′′
2.317
1.375
0.271
1.630
0.634
2.394
2.421
0.905
1.224
2.039
0.234
1.178
Transitions are from the core level in the labeled atom (labels from Figure 1) to the given unoccupied state.
results that the main transitions occurring in each of the main
four prepeaks corresponds to a specific nonequivalent carbon
site. The sites that these features are resulting from are in
agreement for the two techniques.
Nonresonant carbon KR X-ray emission spectra of the bases
are displayed in Figure 3. The excitation energy used for
measuring these spectra was at 320 eV, well above the 1s carbon
absorption edge. The calculations were completed with the
StoBe program. Small differences exist in the spectra, resulting
from differences in the occupied density of states for the four
molecules. Experimental and theoretical agreement is quite good.
The carbon emission is one large feature resulting from a
multitude of transitions occurring from occupied states with
p-symmetry to the open K-shells in the various carbon atoms.
The main transitions and oscillator strengths associated with
the numbered features in Figure 3 are identified in Table 3 for
the carbon edge.
Figure 4 displays the nitrogen 1s X-ray absorption spectra
for the four bases. For the nitrogen edge, both StoBe and GSCF3
were used to calculate the spectra. Although many of the main
features are represented in the theory, some variations in peak
intensity and location occur between experimental and calculated
results in both theoretical sets of spectra. A possible source of
deviation is that the calculations were performed for gas-phase
molecules and measurements are for powdered samples. The
two spectra with the largest variations seem to be guanine and
cytosine, which likely are results of the solid-state structures.
The crystal structure of guanine monohydrate (a comparable
structure to guanine) forms a layered graphite-type structure
hydrogen bonded together with N-H‚‚‚N-type bonds.37 In the
case of cytosine, the structure is held together with N-H‚‚‚O
Figure 5. Experimental and theoretical nonresonant nitrogen KR
emission spectra for (a) adenine, (b) guanine, (c) cytosine, and (d)
thymine. Experimental spectra are displayed with black lines, and
calculated spectra are shown with gray lines.
and N-H‚‚‚N bonds.38 In both cases, the nitrogen atoms are
heavily involved in the hydrogen bond network in the crystal
MacNaughton et al.
7754 J. Phys. Chem. B, Vol. 109, No. 16, 2005
TABLE 5: Assignment of Spectral Features for the N Kr Emission Data
A
1
2
3
4
5
6
7
G
transition
oscillator
strength
16a′ f 1a′
18a′ f 4a′
18a′ f 5a′
19a′ f 1a′
21a′ f 2a′
21a′ f 3a′
22a′ f 5a′
21a′ f 1a′
23a′ f 2a′
24a′ f 4a′
22a′ f 1a′
24a′ f 2a′
25a′ f 3a′
26a′ f 4a′
2a′′ f 5a′
1a′′ f 1a′
2a′′ f 2a′
3a′′ f 4a′
3a′′ f 5a′
4a′′ f 2a′
27a′ f 3a′
4a′′ f 3a′
28a′ f 4a′
28a′ f 5a′
4a′′ f 1a′
29a′ f 3a′
29a′ f 4a′
6a′′ f 4a′
29a′ f 5a′
0.228
0.241
0.563
1.274
1.461
0.203
0.116
0.472
0.636
0.160
0.606
0.424
0.415
0.484
0.515
0.733
0.834
1.145
0.145
0.710
1.719
1.323
0.422
1.593
1.344
0.339
1.791
0.713
1.155
1
2
3
4
5
6
7
C
transition
oscillator
strength
19a′ f 2a′
19a′ f 3a′
20a′ f 4a′
22a′ f 5a′
21a′ f 2a′
22a′ f 2a′
21a′ f 3a′
25a′ f 6a′
23a′ f 2a′
23a′ f 3a′
24a′ f 4a′
26a′ f 5a′
26a′ f 6a′
26a′ f 2a′
1a′′ f 3a′
1a′′ f 4a′
28a′ f 5a′
3a′′ f 6a′
3a′′ f 3a′
30a′ f 5a′
4a′′ f 6a′
30a′ f 6a′
4a′′ f 4a′
31a′ f 5a′
31a′ f 6a′
5a′′ f 2a′
5a′′ f 3a′
6a′′ f 4a′
7a′′ f 6a′
0.197
0.691
0.610
0.145
0.366
1.478
0.472
0.254
0.382
1.281
1.217
0.559
0.674
0.851
0.633
0.415
1.035
0.284
0.457
0.999
1.081
1.667
1.024
1.592
1.017
1.181
1.224
0.638
0.622
1
2
3
4
5
6
T
transition
oscillator
strength
14a′ f 2a′
15a′ f 3a′
16a′ f 4a′
16a′ f 2a′
17a′ f 2a′
18a′ f 3a′
19a′ f 4a′
1a′′ f 4a′
1a′′ f 2a′
20a′ f 2a′
2a′′ f 3a′
3a′′ f 4a′
3a′′ f 2a′
23a′ f 4a′
4a′′ f 4a′
4a′′ f 3a′
4a′′ f 2a′
24a′ f 2a′
5a′′ f 2a′
1.030
0.768
0.271
0.574
1.542
1.193
0.725
0.391
0.796
0.464
1.182
0.212
0.392
2.584
0.934
1.835
0.617
0.250
0.687
1
2
3
4
5
6
7
transition
oscillator
strength
15a′ f 3a′
16a′ f 3a′
16a′ f 4a′
17a′ f 4a′
18a′ f 3a′
19a′ f 3a′
20a′ f 3a′
18a′ f 4a′
19a′ f 4a′
20a′ f 4a′
1a′′ f 3a′
1a′′ f 4a′
3a′′ f 3a′
3a′′ f 4a′
4a′′ f 3a′
4a′′ f 4a′
26a′ f 3a′
5a′′ f 4a′
6a′′ f 3a′
27a′ f 4a′
0.882
0.419
0.420
1.302
0.890
0.901
0.702
0.560
0.654
1.177
0.650
0.652
0.552
0.504
0.803
0.159
0.231
1.925
1.125
0.378
TABLE 6: Assignment of Spectral Features for the O 1s Absorption Data
cytosine
1
2
3
a
guanine
transitiona
oscillator
strength
O1 f 6a′′
O1 f 7a′′
O1 f 25a′
O1 f 26a′
O1 f 29a′
O1 f 8a′′
0.001519
0.003455
0.000019
0.000043
0.000089
0.000524
1
2
3
thymine
transitiona
oscillator
strength
O1 f 8a′′
O1 f 9a′′
O1 f 33a′
O1 f 10a′′
O1 f 34a′
0.004250
0.000026
0.000090
0.000706
0.000043
1
2
3
4
5
transitiona
oscillator
strength
O1 f 7a′′
O2 f 7a′′
O1 f 8a′′
O2 f 8a′′
O1 f 27a′
O2 f 27a′
O1 f 9a′′
O1 f 30a′
O1 f 10a′′
O2 f 29a′
O2 f 30a′
0.003862
0.002417
0.001169
0.002569
0.000096
0.000077
0.000655
0.000235
0.000075
0.000052
0.000431
Transitions are from the core level in the labeled atom (labels from Figure 1) to the given unoccupied state.
structure and could cause intermolecular effects on the measured
spectra. The experimental results agree with previously published results for the nitrogen edge XAS of the bases.20-21 The
multiple prepeak features result mainly from transitions to the
π* unoccupied levels in the different nitrogen sites. The
transitions to the multiple σ* states dominate the broader feature
at higher energy. The main transitions corresponding to the
regions ((0.3 eV) under the numbered arrows in Figure 4 are
labeled along with their oscillator strengths given from the StoBe
program and can be found in Table 4.
Figure 5 shows the nonresonant N KR X-ray emission spectra
for adenine, guanine, cytosine, and thymine with the corresponding theoretical spectra calculated using StoBe. The excitation energy used for this emission data was 420 eV. All features
in the experimental data are reasonably seen in the theoretical
predictions. Like the carbon emission, the nitrogen XES involves
many different transitions from occupied levels occurring in the
multiple nitrogen atoms in the molecules. The most prominent
transitions, along with oscillator strengths corresponding to the
numbered peaks in Figure 5, are shown in Table 5.
The oxygen 1s X-ray absorption data are displayed in Figure
6. This study involves the three bases that contain oxygen,
guanine, cytosine, and thymine. Experimental XAS data are
compared to theoretical calculations performed with StoBe and
GSCF3. The sharper peaks (lower energy) are mainly from the
transitions to the π* states, while the broader features (higher
energy) are the results of transitions to σ* states. These
experimental results are in agreement with previously published
experimental results for the nucleobases.21 Guanine and cytosine
have one main π* feature due to the single oxygen atom in
their respective structures, while thymine has a double peak π*
feature, resulting from the excitation of the two oxygen sites in
its molecular structure. The main transitions corresponding to
the regions ((0.3 eV) under the numbered arrows in Figure 6
are labeled along with their oscillator strengths given from the
StoBe program, which can be found in Table 6. For the oxygen,
Electronic Structure of Nucleobases
Figure 6. Experimental and theoretical oxygen 1s XAS spectra for
(a) guanine, (b) cytosine, and (c) thymine. Experimental spectra are
displayed with black lines, and calculated spectra are shown with gray
lines. The offset used for the y-scale is 35%.
StoBe seems to provide better results, particularly in the case
of thymine. When the two sites were calculated in GSCF3, they
had significant overlap in the first peak, and the defined twopeak structure occurring in the experimental results was not
properly modeled.
Figure 7 includes the results from nonresonant O KR X-ray
emission measurements for guanine, cytosine, and thymine.
These emission spectra were measured with the excitation
energy set at 560 eV. This emission is more discrete than the
carbon and nitrogen edges because there are less sites contributing to the emission process. Table 7 displays the labels for the
most prominent transitions occurring in the oxygen emission
process, corresponding to the numbered peaks in Figure 7. By
comparison of the number of main transitions in a molecule
with one oxygen atom (cytosine and guanine) to a molecule
with two oxygen atoms (thymine), the number of transitions
involved in the emission process has roughly doubled.
By combination of XES and XAS experimental data onto a
common energy axis, it is possible to determine an energy gap
measurement.39-41 This procedure of determining the HOMOLUMO gap is displayed in Figure 8 for the adenine molecule,
using the nitrogen data carefully calibrated with known spectral
peak locations of h-BN.24 By extension of a line along the
J. Phys. Chem. B, Vol. 109, No. 16, 2005 7755
Figure 7. Experimental and theoretical nonresonant oxygen KR
emission spectra for (a) guanine, (b) cytosine, and (c) thymine.
Experimental spectra are displayed with black lines, and calculated
spectra are shown with gray lines.
TABLE 7: Assignment of Spectral Features for the O Kr
Emission Data
cytosine
1
2
3
4
transition
oscillator
strength
21a′ f 1a′
22a′ f 1a′
3a′′ f 1a′
24a′ f 1a′
5a′′ f 1a′
0.422982
4.531453
2.117876
6.382281
2.556386
guanine
transition
1 27a′ f 1a′
2 3a′′ f 1a′
29a′ f 1a′
3 6a′′ f 1a′
4 31a′ f 1a′
32a′ f1a′
7a′′ f1a′
oscillator
strength
thymine
transition
oscillator
strength
0.572670 1 1a′′ f 1a′ 0.605986
1.623532
21a′′ f 2a′ 0.952401
4.450748 2 22a′ f 1a′ 3.868707
2.328636
23a′ f 2a′ 3.300495
0.759807
3a′′ f 2a′ 1.404307
5.830437 3 4a′′ f 1a′ 1.509710
1.097151
25a′ f 2a′ 0.824462
4 5a′′ f 1a′ 1.925977
26a′ f 1a′ 5.621324
5a′′ f 2a′ 2.369543
26a′ f 2a′ 0.851319
5 27a′ f 1a′ 0.990141
6a′′ f 1a′ 0.979252
27a′ f 2a′ 5.660287
6a′′ f 2a′ 0.792720
spectral slope and identification of the intersection with the slope
of the noise floor, the barriers of the gap were determined. The
linear extrapolation method was used to remove the “tail”
MacNaughton et al.
7756 J. Phys. Chem. B, Vol. 109, No. 16, 2005
associated with it, but it is important that each gap was measured
in the same way for each sample, making comparisons possible.
Calibrating the energy involves shifting both emission and
absorption data according to measurements done on a reference
sample. This is an essential step to correct the experimental
energy scale but is only as accurate as the known values for
the peaks in the reference spectra. To summarize, these both
can have a direct influence on the experimental gap measurement and are likely to add a larger error to the (0.2 eV of our
method. Other methods of measuring HOMO-LUMO gaps
exist (for example, using a combination of photoelectron
spectroscopy and electron transmission spectroscopy in the gas
phase), but this method as presented gives a reasonable
estimation for the solid phase of these molecules. However, the
gas-phase measurements may correspond better to some of the
theoretical results.
Figure 8. Nitrogen edge XES and XAS spectra for adenine used for
demonstration of experimental HOMO-LUMO gap measurement.
TABLE 8: Nucleobase HOMO-LUMO Gap Comparison
e
bases
∆Eexp
(eV)
∆Ecalc (eV)
(StoBe)
∆Ecalc (eV)
(isolated bases)
∆Ecalc (eV)
(base stacks)
adenine
4.7
3.71
12.1a
8.6b
3.73c
7.22d
thymine
5.2
3.85
12.7a
9.3b
3.12c
6.91d
guanine
2.6
3.66
12.2a
8.4b
4.8e
3.19c
6.44d
2.97e
2.5f
3.5g
cytosine
3.6
4.02
12.5a
9.3b
3.34c
6.60d
a
Reference 13. b Reference 16. c Reference 11. d Reference 17.
Reference 12. f Reference 14. g Reference 15.
caused by experimental (Gaussian) and lifetime (Lorentzian)
broadening. The down slope of the emission spectrum was used
to determine the first intersection (HOMO), and the onset slope
of the π* feature in the absorption spectrum was used for the
second intersection (LUMO). The energy difference between
the two intersections gives the gap value. This is a relatively
simple procedure and is easily reproduced; therefore, the error
in completing this method is no more than 0.1 eV for each of
the boundaries or (0.2 eV for the total experimental gap value.
The results for all four bases using this method are displayed
in Table 8, where they are compared to results from our StoBe
calculations and other various theoretical results for isolated
bases and homonucleotide base stacks. The experimental gap
measurements differ between the nucleobases as a result of their
unique electronic structures. The experimental values for the
gap do not correspond directly to any of the theoretical
predictions. However, the theoretical predictions do not seem
to be in agreement either and differ substantially depending on
the method of calculation applied. While it provides an estimate
for comparison, this experimental method is not always
straightforward to determine an absolute value for the gap since
core-hole interactions, and calibrating the energy to a reference
sample has effects on the final results. Core-hole effects can
cause the onset of the absorption spectrum to shift to lower
energy due to the influence of the core-hole on the final state
in the absorption process. The presence of the core-hole tends
to shift the emission spectrum to lower energy as well but has
minimal impact. The linear extrapolation will also have error
5. Conclusions
X-ray absorption spectroscopy and X-ray emission spectroscopy are used to study the electronic structures of the four DNA
nucleobases, adenine, guanine, cytosine, and thymine and are
compared to our calculations. Spectral features are assigned in
the XAS and XES spectra according to the Cs symmetry used
in the calculations. The experimental and theoretical results for
the four nucleobases show each has a unique partial density of
states for the carbon, nitrogen, and oxygen sites. For the XAS
results, comparisons are made to both GSCF3 and StoBe
calculations. Although producing quite similar results, GSCF3
seems better suited to calculating the carbon spectra while StoBe
provides improved results for the oxygen edge. Both types of
calculations have similar difficulties modeling some features
in the nitrogen edge spectra. While there is good agreement
between many of the experimental and theoretical spectra, a
challenge remains with determining absolute values of the
HOMO-LUMO gaps. The origin of the gap challenge is
twofold; discrepancies in the values of the gap exist among
theoretical results, and obtaining experimental values is complicated due to influences of energy calibration procedures and
to a lesser extent due to the presence of core-hole effects. These
experimental techniques have proven useful at probing the
electronic density of states and in combination with the
theoretical results have helped provide a description of the
electronic structure of the nucleobases.
Acknowledgment. Funding by the Natural Sciences and
Engineering Research Council of Canada, the Research Council
of the President of the Russian Federation (Grant No. NSH1026.2003.2), and the Saskatchewan Synchrotron Institute is
gratefully acknowledged. A.M. is a Canada Research Chair. The
work at the Advanced Light Source at the Lawrence Berkeley
National Laboratory was supported by the U. S. Department of
Energy (Contract No. DE-AC03-76SF00098).
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