Dissociation Pathways in the Cysteine Dication after Site-Selective

Sep 18, 2014 - A photoelectron–ion–ion coincidence experiment has been carried out on the amino acid molecule cysteine after core-ionization of th...
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Dissociation Pathways in the Cysteine Dication after Site-Selective Core Ionization J. Laksman,*,†,∥ K. Kooser,‡ H. Levola,‡ E. Ital̈ a,̈ ‡ D. T. Ha,‡ E. Rachlew,§ and E. Kukk‡ †

Department of Physics, University of Oulu, P.O. Box 3000, FIN-90014 Oulu, Finland Department of Physics and Astronomy, University of Turku, FIN-20014 Turku, Finland § Atomic and Molecular Physics, Royal Institute of Technology KTH, S-20691 Stockholm, Sweden ‡

ABSTRACT: A photoelectron−ion−ion coincidence experiment has been carried out on the amino acid molecule cysteine after coreionization of the O 1s, N 1s, C 1s, and S 2p orbitals. A number of different dissociation channels have been identified. Some of them show strong site-selective dependence that can be attributed to a combination of nuclear motion in the core-ionized state and Auger processes that populate different final electronic states in the dication.



on adsorption of cysteine on surfaces.13−17 Figure 1 shows the geometric structure of the cysteine molecule. It has two oxygen

INTRODUCTION Proteins that are responsible for the biochemical processes in living organisms are formed when amino acid molecules are linked together by peptide bonds between their carboxyl acid, COOH, and amine, CNH2, functional groups. Knowledge regarding the electronic states, nuclear dynamics and decay in the amino acids is therefore interesting from the fundamental scientific point of view, but can also be of value to the life sciences and for medical applications. Indeed due to their importance, during the past decade the inner shell electronic structure of various amino acids have gained considerable interest and many studies have been made. Photoionization and NEXAFS studies have been made by Plekan et al.1 and Feyer et al.2 Relevant studies that also consider fragmentation are made by Marinho et al.,3 Itälä et al.,4 and Ha et al.5 Ultrafast charge migration in an amino acid was observed by Belshaw et al.6 Maclot et al. studied fragmentation of isolated amino acid molecules compared with that of the chemical environment of clusters.7 Peptide bonds have been studied by Gordon et al.8 Li et al.9 studied K-edge NEXAFS spectra of an amino acid in the solid phase compared with that in the gas phase. In this study we investigate fragmentation patterns of the amino acid cysteine after core ionization. Photoionization of an atomic inner shell electron from a molecule leads to a highenergy ionized state and the subsequent relaxation by Auger decay populates states in the dication that are predominantly dissociative. Fragmentation of cysteine and other amino acid cations have been studied theoretically by Gil et al.10 who found loss of the carboxyl group to be the most favorable pathway. Cysteine has the thiol group, CH2−SH, as a side chain. In the 1980s ab initio calculations were made on the neutral ground state and its ionization potential,11 while photoelectron spectra were obtained by He(II) ionization.12 To the best of our knowledge, very few publications exist on the inner shell spectra of gas-phase cysteine, although studies have been made © 2014 American Chemical Society

Figure 1. Geometric structure of the cysteine molecule. The nuclei C and O are labeled with numerical indexes for identification of identical atomic constituents in different chemical environments.

atoms and three carbon atoms in different chemical environments which provides the possibility to distinguish them based on the electron binding energy.18



EXPERIMENT AND DATA ANALYSIS METHODS The experiments were performed on the undulator beamline I411 at MAX-lab, Lund, Sweden.19 The soft X-ray radiation was monochromatized by a Zeiss SX-700 plane-grating monochromator. The equipment and data acquisition software used in this experiment were developed by Kukk et al.20 It has proven to be a useful tool to study the nuclear dynamics in molecules and clusters after photoionization by detecting photo- or Auger-electrons in coincidence with multiple produced cationic fragments.5,21,22 The setup is a Scienta SES-100 hemispherical electron analyzer and a Wiley−McLaren type ion time-of-flight spectrometer mounted perpendicular to the light propagation. The electron analyzer angle of detection was set at 0° with respect to the polarization vector of the horizontal linearly polarized light. After an ionization event, the Received: August 12, 2014 Revised: September 17, 2014 Published: September 18, 2014 11688

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Figure 2. (a) Overview of S 2p photoelectron−ion−ion-coincidences. Each regression corresponds to a dissociation pathway. (b) Two body breakup of the parent dication along the C1−C2 bond. (c) Three body breakup along the C1−C2 and N−C2 bond bond.

certain procedure was performed: Data was also collected with artificially generated start triggers, interleaved with the true electron triggers, and under the same experimental conditions. The generated data set was then subtracted from the photoelectron data set, see ref 20 for details. Because of their velocity distribution in the spectrometer axis, the ions have a deviation in their time-of-flight with relation to those with zero velocity. This time deviation is proportional to the fragment’s momentum, and is related to the kinetic energy release (KER), which is the difference in potential energy between the final dissociative state and the fragments states. KER can thus be used to identify the electronic states involved in nuclear dynamic processes in polyatomic molecules.23 The absolute value of an ion’s linear momentum can be calculated from the time-of-flight deviation ΔT, via the equation

energy selected photo electron is detected in coincidence with multiple photoion’s (PEPIPICO). The ability to monitor both the electronic states involved and the resulting time-dispersed cationic fragments from the same ionization event provides a unique probe into the dynamic processes taking place in the molecular world. The cysteine sample was evaporated into the extraction region using an effusion cell at around 112 °C. Experimental studies of gas-phase amino acids are hindered by their high melting points and associated low vapor pressures which, combined with low thermal stability, makes many of these compounds decompose before melting. Therefore, the temperature was increased very slowly and a mass spectra at 50 eV photonenergy was monitored both during the heating and once every hour during the data collection as a control mechanism. Any deviation in fragment ratio would have revealed thermal decomposition. In this experiment, PEPIPICO data was collected at the S 2p (hν = 185 eV), C 1s (hν = 330 eV), O 1s (hν = 580 eV), and N 1s (hν = 425 eV) edges, with the aim of comparing the fragmentation pathways dependence on siteselective core-ionization. The pass energy was set at 100 eV and the entrance slit of the analyzer was 1.6 mm, which corresponds to the energy resolution of about 750 meV and a photoelectron energy window of about 9 eV. The photon resolution is much better than electron resolution and has negligible influence on the spectrum. In principle for this experiment, no photo electron spectra calibration is required since our interest is not in the exact binding energy of the photolines. Nonetheless, at the oxygen and carbon edges, calibration of the electron kinetic energy scale was done by comparison to the known carbonmonoxide O 1 s−1 and C 1 s−1 spectra that we collected with the same experimental parameters. At the N 1s and S 2p edges, no calibration was done. In order to subtract false coincidences where the ion or ions are detected in an event where the start trigger is noise or a photoelectron that originates from a different molecule, a

p = ΔT ·U ·q

(1)

where q is the ion’s charge and U is the electric field over the p2

extraction region.24 The kinetic energy is given as EK = 2·m , where m is the ion’s mass. In the present experiment, the length of the extraction region is 21 mm and the applied voltage over it is 200 V (+100 V on kicker plate and −100 V on extractor plate), so U = 9.52 V/mm. KER in a particular fragmentation channel is the sum of the kinetic energy of all its charged and neutral fragments. When a photoelectron is detected in coincidence with two photoions, the time-of-flight data for each event can be presented so that the first ion to reach the detector is on the abscissa and the second ion is on the ordinate. For many events, a regression pattern is thus formed. For multibody breakups, the fragmentation is characterized not only by KER, but also by the regression slope of the ion-pairs which reveals how the total KER is partitioned between the fragments. Simon et al.25 developed a slope analysis method for determining bond breaking dynamics. For example, a sequential 11689

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Table 1. Regression Slope and Maximum Kinetic Energy Released for All Observed Dissociation Channelsa dication fragmentation mass (amu)

dissociation channels

46/75 45/59 34/42 15/45

CO2H2+/C2SNH5+ CO2H+/C2SH3+ SH2+/C2NH4+ NH+/CO2H+ + +

16/28

44/44 28−30/45−47

15/33

slope

KER (eV)

DP

± ± ± ±

0.3 0.5 0.6 0.5

a a a a

−0.8 ± 0.1

7.0 ± 0.7

a

−1.0 ± 0.1 −1.0 ± 0.3

7.1 ± 0.7 4.5 ± 0.5

b b

−5.3 ± 0.5

3.7 ± 0.3

c

−1.0 −0.8 −1.2 −4.9

NH /CSH H2N+/CO+ O+/CO+ O+/CNH2+ CS+/CO2+ NCH2−4+/CSH1−3+ NCH2−4+/CO2H1−2+ OCH0−2+/CSH1−3+ NH+/SH+

± ± ± ±

0.2 0.1 0.1 0.4

3.1 5.6 5.9 5.6

a

The possible ion coincidences are presented with the most likely pathways in boldface. DP stands for the dissociation process that is shown in Figure 3.

Figure 3. Variety of dissociation channels has been categorized into three main groups: (a) Sequential pathways initiated by ejection carboxyl acid. (b) Concerted breakup. (c) Two step sequential dissociation where SH cation is the first fragment to be released followed by H2N+.

the first ion has its maximum time-of-flight, the second ion has its minimum and vice versa.25 The slope of the pattern reflects this anticorrelation and contains information about the dissociation dynamics. At the S 2p edge, ions were detected in coincidence with both S 2p1/2 and S 2p3/2 photoelectrons. As expected, no correlation between fragmentation pathway and the spin−orbit splitting was found. Different ion-pairs can be distinguished due to the negative slope of the regression (see Table 1 for an overview). In Figure 2a, the range of the abscissa and the ordinate has been chosen so that no detected ion-pairs are outside of the selected time window. Because of electronic noise for time-of-flight below 1 μs, the lightest cations, H+ and H2+ which are likely to be produced, could not be detected in our experiment. A few additional islands can be seen, but their lack of correlation prevents us from identifying them as true pathways, since they can also be false coincidences that were not fully subtracted with our algorithm. Our first objective is to assign and disentangle the nuclear dynamics for all electron−ion−ion-coincidences. We have categorized them into three main groups that we illustrate in

three body breakup of a dication: ABC2+ → A+/BC+ → A+/B/ C+; the momentum ratio, and subsequently the slope is p m S= A =− C pC mBC (2) where m is the ion’s mass. This model is based on the assumption that in the second bond break, where no Coulomb explosion is involved, the kinetic energy is small so that when calculating KER only the first step must be taken into consideration.



RESULTS AND DISCUSSION Dissociation Channels. First, we identify the dissociation pathways observed at various core-ionization conditions. The data recorded at the S 2p edge is the most suitable example for this purpose due to its highest quality. Figure 2a shows the photoion-photoion-coincidence map after S 2p core ionization. A characteristic feature of ion-pair patterns from molecular breakup is the time-of-flight anticorrelation meaning that when 11690

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discussed two body breakup, since also the involved neutral fragments that evade detection gain some velocity. In the first step in eq 3 the linear momentum vector of the two fragments must be exactly opposite. The linear momentum of carboxyl ion is known from eq 1, which gives us also the momentum of the intermediate cation fragment. The total KER is the sum of the two fragments kinetic energy which we calculate to ∼5.6 eV. Ion-pair 34/42 amu we assign as SH2+/C2NH4+. The existence of the SH2 cation means proton migration to sulfur which is reasonable since proton migration is a common and well documented process in ionized organic molecules.28,29 In amino acids, several conformers are known to exist whereof proton migration is more likely in some.30,31 The slope of −1.2 ± 0.1 can be explained via deferred charge separation involving the bonds C1−C2 and C3−S. The almost exact anticorrelation of the cation pair suggest that neutral fragment does not gain much kinetic energy, and we estimate the total KER value ∼5.9 eV. For polyatomic molecules such as amino acids, due to a wealth of possible fragmentation channels, it is sometimes difficult to assign a peak pattern to a specific ion pair. The ionpair 15/45 amu can correspond either to NH+/CSH+ or NH+/ CO2H+ which share the same mass-charge ratio. The slope is −4.9 ± 0.4 which can be explained with a sequential process where the first bond-break is either C1−C2 or C2−C3. We have previously argued that the dominating bond-breaking is C1−C2; therefore, most likely, the dissociation sequence is primary ejection of CO2H+ followed by the NH+ fragment. On the basis of the same argument as for the previous sequential pathway, we find the KER ∼ 5.6 eV. An ion−ion-coincidence that we detect with an abundance at the O 1s and C 1s ionizations, but not at S 2p−1 or N 1 s−1 is 16/28, which is difficult to assign. It can be O+/CNH2+, O+/ CO+, or H2N+/CO+. For the similar amino acid glycine, Itälä et al.4 compared with 13C isotope substituted in amine-group after core ionization to C 1 s−1 state. They could conclude that H2N+/CO+ is the only possible pathway. Cysteine has more complicated side-chain than glycine, but since for neither possible ion-pair the side-chain is involved, we assume that both amino acids share the same fragmentation mechanism for this ion-pair. This implies four-body breakup of the bonds C1−O2, C1−C2, and C2−C3. The slope is −0.8 ± 0.1, meaning that also the neutral fragments must gain some kinetic energy. This slope value also excludes contribution from O+/CO+ fragments from residual CO2 gas, since two-body breakups must have exact anticorrelation. On the basis of our model in eq 2, primary release of the neutral side-chain followed by some three-body breakup can not explain this slope. Instead we propose a more complex process involving primary breakup of C1−C2, then both fragments dissociate in a second step. The same dissociation sequence was proposed for glycine by Itälä et al.4 Under the assumption that the energy released in the second step can be neglected, we calculate KER ∼ 7.0 eV. The process in Figure 3a is a primary C1−C2 bond break followed by additional bond cleavages in a sequential manner. A time scale for this process in the nanosecond range would imply that the second breakup does not take place in the extraction region and would be seen as characteristic tails in the regression plots in Figure 2. A time scale in the femtosecond range would mean that in the second breakup, the cations are sufficiently close for Coulomb forces to have an impact on fragments linear momentum, thus the results would not be

Figure 3. For the amino acid glycine, an additional type of process was identified as water elimination,4 that for cysteine, however, we could not find evidence of. Carboxylic Acid Ejection. It is well-known that for direct valence ionization of cysteine and other amino acids, severing of the C1−C2 bond is the most favorable process, since it is the easiest to break. This has been demonstrated both theoretically and experimentally.10,26,27 Furthermore, calculations regarding core-ionization on the similar amino acid methionine5 found that C1−C2 is the bond which requires the least amount of energy to break. On the basis of these previous studies, when in our analysis ambiguities occur regarding cation assignments, we assume that fragmentation between the carboxyl and amine groups is the most likely process. A weak but rather interesting pathway is the ion-pair with masses 46 and 75 amu. (See Figure 2b for expanded view.) Their combined mass is 121 amu, that of the parent ion, meaning that this is a clean two-body breakup. The predicted slope of a two-body process is exactly −1. The observed pattern is too weak to determine the experimental slope accurately, but it can be seen that the slope of −1 would fit quite well on this pattern. If we assume no isomerization involving the larger atomic constituents takes place prior to dissociation, then we can assign the peak to the cation-pair CO2H2+/C2SNH5+, which implies a nuclear dynamics process of proton-migration from either the amine or the thiol group to the carboxylic acid-group prior to or together with the severing of the C1−C2 bond. Indeed, a theoretical study of cysteine showed hydrogen bonds to exist from the carboxyl group to both the amine and the thiol group.26 For a two body breakup with no undetected neutral products, KER is simply the sum of the two cation’s kinetic energy. With eq 1 we estimate the KER to be ∼3.1 eV for the cation pair CO2H2+/C2SNH5+. Another detected ion-pair of interest is 45 and 59 amu. Its expanded view is presented in Figure 2c. It can conclusively be assigned to CO2H+/C2SH3+ with a neutral NH2 fragment and a hydrogen atom released. The peak-broadening suggests possible contributions from 45/58 and 45/60, which means that on the heavier ion, there can be one hydrogen atom less and one more, respectively. The slope is −0.8 ± 0.1, from which we can gather additional information. On the basis of eq 2, the process is interpreted as a two step sequential dissociation. Considering primary ejection of the carboxyl cation from the doubly charged parent molecule followed by secondary breakup to C2SH3+, neutral H2N and a hydrogen: CH 2SHCHNH 2COOH2+ → CH 2SHCHNH 2+/COOH+ → CH 2SHC+/H/NH 2 /COOH+

(3)

Since the velocity of the neutral fragments contributes to the pattern’s broadening, the narrow highly anticorrelated regression of this ion-pair suggests that the kinetic energy released in the second step is small. This sequence predicts the slope S =

(

59 59 + 16

) = −0.79.

Indeed, from the excellent

agreement between the measured slope and the model, the two step dissociation pathway can be established, thus demonstrating that the main contribution to the KER comes from the first step, and the second step can be neglected. Total KER estimation for a sequential dissociation process is nonetheless not as straightforward as for the previously 11691

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consistent with the model in eq 2, which they are. We thus conclude that the time scale is in the picosecond range where the fragments can rotate between the breakups. Concerted Breakup. On the diagonal, we find the more intense ion-pair 44/44, which we identify as CS+/CO2+. The slope is very close to −1 and the regression is broader then what we have previously seen. We conclude that the breakup is not sequential, but rather a concerted one step Coulomb explosion of the C1−C2 and C2−C3 bonds, that takes place following Auger decay. Likely with significant internal energy considering that the cation’s have lost all their hydrogens. The mean kinetic energy released of ∼7.1 eV is larger than most other breakups. In the region (28−30)/(45−47) amu, there are a few overlapping regressions that can not be disentangled, but must be analyzed together. They are most likely an overlap of the two dissociation pathways NCH (2−4) + /CO 2 H (1−2) + and NCH(2−4)+/CSH(1−3)+. In both cases, the slope ∼−1.0 ± 0.3 suggests a concerted three body breakup involving the bonds C1−C2 and C2−C3. The large uncertainty in slope error of this pattern is due to overlapping of several processes, making the slope value determination more challenging than normal. Figure 3b presents the two observed cases of concerted breakup where cysteine splits into the three functional groups: carboxyl, amine and thiol, thus demonstrating that each of them can survive as a stable unit on a μs time scale. Sequential Dissociation. Ion-pair 15/33 is NH+/SH+. The slope of −5.3 ± 0.4 and its relatively narrow shape is in excellent agreement with a two-step fragmentation pathway where SH+ is the first fragment to be ejected followed by ejection of NH+. Figure 3c presents this sequential pathway of two body breakup that is initiated by the C3−S in the thiolgroup and followed by the C2−N bond in the amine group. Chemical Shift and Site-Selective Ionization. One of our main objectives was to study the fragmentation dependence on the localization of the core hole. The strength of the PEPIPICO technique is the ability to study correlation between photoions and photoelectrons and thereby disentangle site selective fragmentation pathways. The eight regressions that we have discussed were observed at various intensities at the different edges as will be discussed in this section. On the other hand, we found no site-selective dependence of neither the slope nor the KER, suggesting that the final dissociative states and end products are the same for all the studied ionization edges. The carboxyl acid group has two oxygen atoms within different chemical environments. In hydroxyl it is labeled O1 and in carbonyl it is labeled O2, see Figure 1. The O 1s binding energies are, as a consequence different, which is referred to as chemical shift.18 In the literature we could find no reference values of the binding energies for the gas-phase cysteine molecule, but from our data we retrieve the binding energies 537.6 ± 0.3 eV for carbonyl and 539.5 ± 0.3 eV for hydroxyl. At the oxygen 1s edge the two most intense ion−ioncoincidences are the ones we identified as 16/28 and (28− 30)/(45−47) amu Figure 4a presents the ion yield of them, including error bars, as a function of the coincident photoelectron’s binding energy over the carbonyl and hydroxyl O 1 s−1 states. The vertical dashed lines indicate the two separate regions. Since these channels are rather weak ones, the statistics is not good and also the two photopeaks are not well resolved. Nonetheless a significant correlation between dissociation pathways and the electronic states is evident.

Figure 4. Relative intensities of various pathways as a function of binding energy: (a) O 1 s−1 and (b) C 1 s−1.

Similarly to our study, the O 1s site-selective dependence in the carboxyl group in liquid acetic acid has been studied with X-ray emission spectroscopy by Tokushima et al.32 They found dramatic differences in the final populated valence states after core-excitation. Although our study differs in several ways from that of Tokushima et al., the site selective O 1s core hole creation in the carboxyl group is similar and suggest that it is the population of different valence states in the host molecule which subsequently determines the fragmentation pathways. Another possible explanation for the site-selective dependence is nuclear motion in the core-ionized molecule. This alternative can in principle be analyzed with our technique by studying how the relative intensity of the channels changes as a function of the photoelectron energy, since by tuning over the O 1 s−1 core hole we probe the internal vibrational energy of the intermediate state.33 However, our statistics and resolution is insufficient to determine this reliably. Cysteine has three carbon atoms within different chemical environments. In the carboxyl group it is labeled C1, in the amine group it is labeled C2 and in the thiol it is labeled C3, see Figure 1. For C2 and C3 we find the binding energies 292.4 ± 0.3 eV. C1 gives the binding energy 294.6 ± 0.2 eV. At the carbon 1s edge in Figure 4b, three additional ion-pairs have sufficient statistics to be presented. C1 1s is well resolved, while for C2 1s and C3 1s, the chemical peaks overlap. We find the combined intensities of the C2 and C3 peaks to be about twice that of C1, which is a reasonable result since the cross sections of the lines are expected to be approximately equal.2 For any of the five dissociation channels, no systematic differences in the fragmentation ion-pair yields can be observed. This indicates that no nuclear motion strong enough to impact fragmentation takes place after core-ionization, also suggesting that the barrier for charge migration across the carbon atoms is low. This observation is in agreement with a similar study on glycine4 where also no site selective dependence was found at the C 1s edge. As a means to quantify the fragmentation pathways dependence on site selective inner shell ionization, in Figure 5, we present a bar diagram where the total ion-pair yield for each ionization site has been normalized to unity. Each group represents a site-specific ionization and each color corresponds to a dissociation pathway. This visualization method gives us an overview of both the total intensity of a certain pathway, as well 11692

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Figure 5. Branching ratios of all dissociation channels at the different core ionizations.

nuclear motion in the core ionized state and the relaxation process. For SH+/NH+ that is the only pathway of process c, the relative branching-ratio is about 5% regardless of the siteselective ionization. Our coincidence technique excludes the possibility of direct valence ionization. Instead we propose that the valence orbitals of the final dissociative state leading to this ion-pair are delocalized over the entire species.

as its relative intensity compared to other core ionizations. For different ion-pairs, significant variations are evident. The two weak ion-pairs 46/75 and 45/59 are almost exclusively detected on the S 2p−1 and the N 1 s−1 state. Indeed, Ha et al.5 showed with Auger electron-photoionphotoion coincidences on methionine that after S 2p ionization, the relaxation process has an impact on the fragmentation channels so that larger fragments are associated with vacancies in outer molecular orbitals. This suggests that 46/75 and 45/59 are the result of final dissociative states that are not easily accessible from other core hole ionizations. From the breakups that are initiated with release of the carboxyl group in Figure 3a, we find that three of the ion-pairs have the highest abundance at the S 2p−1 state: 46/75, 45/59, and 34/42. Consider the concerted process in Figure 3b: The ion-pair 44/44 which is coincidences between thiol and carboxyl cation’s reaches its maximum at S 2p−1. We have thus found that the coincidence-pairs that dominate after S 2p ionization all have cationic fragments containing the thiol moiety. Furthermore, the deferred charge separation channel SH2+/C2NH4+, where the carboxyl moiety is a neutral fragment, is remarkebly weak at O 1s ionizations, which suggests a high barrier for charge migration from oxygen. Regarding the N 1 s−1 state: Although it is dominated by the ambiguous ion-pair (28−30)/(45−47) that can correspond to two different pathways, both possibilities include the amine cation. From Figure 5, we find the general trend that the O 1 s−1 and N 1 s−1 states mostly lead to fragments where the charges are located on the carboxyl acid and amine groups. S 2p ionization on the other hand primarily leads to cationic fragments involving the sulfur atom. A possible explanations for this is that, at O 1s, N 1s, and S 2p core holes, dissociation is not only dependent on Auger decay, but also on nuclear motion and breakup in the core-ionized state taking place on the same time scale as the relaxation, thus isolating the charge at one moiety. One must also consider that although charge migration in amino acids can be an ultrafast process,6 site selective core-ionization might initiate Auger decay to final electronic states with valence orbitals that do not extend over the whole molecule, thus preventing charge migration from the moiety with the selected nuclei. Subsequently, dissociation primarily produces cationic fragments with the selected atomic site as a constituent. The most dramatic site-selective effect can be seen at the hydroxyl O 1 s−1 site, where the cation pair NH2+/CO+ is the dominating dissociation channel. The fragmentation involves three different bond ruptures in a sequential manner, where the charge localization and bond breaking is not concentrated to the carboxyl moiety. This suggests a complex interplay between



CONCLUSION

The performed study presents a systematic analysis of the fragmentation pattern of core ionized cysteine. We have identified eight different pathways, including one with proton migration and clean two-body breakup. These have been catagorized into three groups of dissociation processes. We have concluded that the general trend after final dicationic states have been populated, is that the bond between the amino group and the carboxylic acid group will break, usually followed by a secondary dissociation. We have identified two concerted Coulomb explosions that produce the three moieties: carboxyl, amine and thiol. There is correlation between the localized core ionization and the fragmentation channels. In particular, some channels are stronger at one specific core hole. The site-specific effect can be as strong as to change the dominant dissociation pathway. For example, in most cases the dominant channel involves ion pairs with the NCH(2−4)+ fragments, inferring rupture of the C−C bonds to the central carbon C2. However, in the case of oxygen 1s ionization, the NH2+/CO+ pathway (where the C2−N bond ruptures) gains strength and for the O1 atom (in the hydroxyl group), it even becomes the dominant one. In this instance, the bond breakage and charge localization pattern is modified not in the immediate vicinity of the core ionization site. It would be of interest in future studies to look into the fragmentation site-specificity within the carboxyl group also in other carboxylic acids. Another example is the enhancement of the pathway containing the CS+ fragment when the sulfur 2p core holes are created. The site-specific core-hole localization effects are not related to particular bond breakages or charge localization in a straightforward way. Instead, fast Auger decay creates dicationic states with electron charge density depending on the hole creation in particular molecular orbitals (which can be strongly core hole dependent). Also, nuclear motion initiated in the core-ionized state can favor certain dissociation pathways, such as observed in the case of core-excited states.32,34 11693

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AUTHOR INFORMATION

Corresponding Author

*(J.L.) E-mail: [email protected]. Present Address ∥

(J.L.) MAX-lab, Lund University, P.O. Box 118, SE-22100 Lund, Sweden. Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS We acknowledge assistance from the MAX IV laboratory staff, in particular to Maxim Tchaplyguine. Financial support from the Academy of Finland, the EU Transnational Access to Research Infrastructures programme and The National Doctoral Programme in Nanoscience of the Ministry of Education of Finland is acknowledged. E.R. acknowledges funding from the Swedish Research Council (VR). Finally, we would like to thank the Electron Spectroscopy Group of the University of Oulu for the opportunity to share their experimental equipment.



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The Journal of Physical Chemistry B

Article

(32) Tokushima, T.; Horikawa, Y.; Harada, Y.; Takahashi, O.; Hiraya, A.; Shin, S. Selective Observation of the Two Oxygen Atoms at Different Sites in the Carboxyl Group (−COOH) of Liquid Acetic Acid. Phys. Chem. Chem. Phys. 2009, 11, 1679−1682. (33) Mocellin, A.; Wiesner, K.; Sorensen, S. L.; Miron, C.; Le Guen, K.; Céolin, D.; Simon, M.; Morin, P.; Machado, A. B.; Björneholm, O.; et al. Site Selective Dissociation Upon Core Ionization of Ozone. Chem. Phys. Lett. 2007, 435, 214−218. (34) Laksman, J.; Månsson, E. P.; Grunewald, C.; Sankari, A.; Gisselbrecht, M.; Céolin, D.; Sorensen, S. L. Role of the Renner-Teller Effect After Core Hole Excitation in the Dissociation Dynamics of Carbon Dioxide Dication. J. Chem. Phys. 2012, 136, 104303.

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dx.doi.org/10.1021/jp508161s | J. Phys. Chem. B 2014, 118, 11688−11695