Role of Resonance Electron Attachment in Phytoremediation of

Article pubs.acs.org/JPCB

Role of Resonance Electron Attachment in Phytoremediation of Halogenated Herbicides Stanislav A. Pshenichnyuk,*,†,‡ Alberto Modelli,§,∥ Eleonora F. Lazneva,‡ and Alexei S. Komolov‡ †

Institute of Molecule and Crystal Physics, Ufa Research Centre, Russian Academy of Sciences, Prospeκt Oktyabrya 151, 450075 Ufa, Russia ‡ St. Petersburg State University, Universitetskaya nab. 7/9, 199034 St. Petersburg, Russia § Dipartimento di Chimica “G. Ciamician”, Università di Bologna, via Selmi 2, 40126 Bologna, Italy ∥ Centro Interdipartimentale di Ricerca in Scienze Ambientali, via S. Alberto 163, 48123 Ravenna, Italy S Supporting Information *

ABSTRACT: This study is aimed to point out the important role played by resonance electron attachment in reductive dehalogenation, in particular in phytoremediation of organic pollutants under conditions of excess negative charge. To model enzymatic reactions occurring in reductive conditions, low-energy electron capture by the halogenated herbicides atrazine and bromoxynil was studied in vacuo using electron transmission spectroscopy. A variety of decay channels of the temporary molecular negative ions was discovered by means of dissociative electron attachment spectroscopy. The experimental results were interpreted with the support of quantum-chemical calculations. Dehalogenation of atrazine and bromoxynil was found to be the dominant decay of the molecular negative ions formed at thermal energies of the incident electrons. It is concluded that formation of negative ions by electron donation in enzymatic active centers followed by their dissociation along the σ bond can be considered as the main mechanism of reductive dehalogenation.

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tive electron transfer5,6 could be involved in the dehalogenation of all compounds possessing a high electron affinity (EA). Redox reactions and, in particular, the electron attaching properties of halogenated herbicides have been considered to be of importance in the mechanisms of herbicide reactions, their products playing a role in biochemistry.7,8 Indeed, electron transfer in enzymatic reactions is suggested to be a key event in the metabolism of the model toxicant carbon tetrachloride to chloroform.9 As suggested for a series of nonsteroidal anti-inflammatory drugs (NSAIDs),10 the phase I metabolism can be mediated by dissociative electron transfer inside active centers of cytochrome P450 enzymes responsible for the detoxification of organic contaminants in both animals and plants. The EA of NSAIDs is comparable with that of molecular oxygen, thus allowing them to compete with cellular O2 for the capture of electrons available in biological media.11 Of course the EA of halogen-containing chemicals is expected to be even higher, so that these species are able to withdraw electrons from their usual pathways in living cells and to act as unnatural electron acceptors. In the present case, reductive dehalogenation of ATR and BRX, that is, the main way of their

INTRODUCTION Contamination of the environment with anthropogenic organic chemicals including polycyclic aromatic hydrocarbons, petroleum hydrocarbons, and halogenated hydrocarbons is considered to be a global problem of the modern world, influencing both the mankind and plants via pollution of soil, water, and air.1 However, a possible solution is suggested by the plant kingdom. Phytoremediation represents a smart and ecologyfriendly way to protect the environment by removing or neutralizing harmful pollutants with plants that metabolize xenobiotic species to nontoxic metabolites via enzymatic reactions.2 The whole process is certainly very complex, and deep degradation of the contaminants can also include their “remote” transformation by specific microbes in the rhizosphere, translocation in plant tissues, and “terminal” emission of the volatile products into the atmosphere.3,4 The present study is aimed only to a better understanding of the initial elementary step of transformation of xenobiotic molecules inside active centers of the detoxifying enzymes of plants, such as cytochrome P450-containing monooxygenases, peroxidases and phenoloxidases.2 We consider here two specific halogenated herbicides, atrazine (1-chloro-3-(ethylamino)-5-(isopropylamino)-2,4,6-triazine, ATR) and bromoxynil (3,5dibromo-4-hydroxybenzonitrile, BRX). However, the proposed mechanism of dehalogenation initiated by resonance dissocia© 2016 American Chemical Society

Received: October 7, 2016 Revised: November 3, 2016 Published: November 4, 2016 12098

DOI: 10.1021/acs.jpcb.6b10149 J. Phys. Chem. B 2016, 120, 12098−12104

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The Journal of Physical Chemistry B metabolic transformation, can be driven by electron transfer accompanied by cleavage of covalent bonds of the so-formed molecular anions. The present paper describes the formation of gas-phase temporary anion states12,13 and their dissociative decay channels12,14,15 in ATR and BRX, extensively used to control broadleaf weeds all over the world. The experimental data are assigned with the support of density functional theory calculations. These findings are used to propose a mechanism of reductive dehalogenation of herbicides through the resonant capture of extra electrons in enzymatic active centers, followed by dissociation of the molecular anions. The use of gas-phase data partially fits the conditions in the enzymatic centers, actually intermediate between those in the gas-phase and aquatic media. Due to their hydrophobic nature, the enzymatic active centers are in fact accessible to a very few water molecules.16 The first step of electrochemical reduction of BRX in solution was associated with formation of the molecular anion radical, followed by cleavage of a carbon−halogen bond.17 The gas-phase dissociative electron attachment (DEA) process, that is, the simple chemical reaction M + e− → M(*)− → fragments (where M stands for a neutral molecule and M(*)− a temporary molecular anion) represents, therefore, a suitable way to model the decomposition of halogenated herbicides. DEA spectra, at variance with electrochemistry, provide complete information on the fragments formed by oneelectron reduction, their identification being quite important in light of their possible toxicity. Although BRX can easily be degraded via several pathways,18 ATR is still widely distributed in the ecosystems, and its removal from the environment is a necessary task.19 ATR is in fact able to cause endocrine disruptions and is suspected to possess carcinogenic activity.20 The present data on the electron-acceptor properties and DEA to ATR and BRX shed some light on the pathways of degradation of halogenated pollutants and are important for understanding the elementary mechanism of their sustainable remediation. The present results expand our knowledge on low-energy electron-driven chemistry in biological systems21−25 and disclose the role of the normally empty electronic levels in bioactivity, whereas the role played by the filled orbitals has been considered elsewhere.26,27

Figure 1. Derivative of transmitted electron current as a function of incident electron energy for atrazine (ATR) and bromoxynil (BRX). B3LYP/6-31G(d) representation of the vacant MOs. Experimental VAEs and calculated VOEs are labeled by green and blue bars, respectively. The lowest unoccupied MOs (LUMOs) are indicated.

capture into the third π* MO, in nice agreement with the value (3.94 eV) calculated for this shape resonance. In contrast with ATR, the first three MOs of BRX (the lowest two possessing π* ring character, the third one with mainly σ*C−Br character) are predicted to give rise to stable anion states (Table S1), thus being not observable in ETS.30 The predicted position (1.16 eV) of the second σ*C−Br MO is in good agreement with the first VAE (1.3 eV) measured in the ET spectrum, although the empirical equations used to predict σ*C−Br VAEs are less reliable than those available for σ*C−Cl MOs.31 However, a significant unresolved contribution to this signal is expected to come from electron capture into the π*CN MO parallel to the ring plane, labeled π*CN|| in Figure 1, its scaled B3LYP/6-31G(d) energy being 1.64 eV. Electron capture into a π* MO mainly localized on the cyano group and the benzene ring of BRX leads to formation of the resonance displayed at 2.7 eV, its predicted VAE being 2.33 eV. The higher lying π* VAE is calculated to be 4.15 eV, close to the energy (4.3 eV) of the third resonance displayed by the ET spectrum of BRX. The decay channels of the temporary molecular anions of ATR and BRX were studied with the dissociative electron attachment spectroscopy (DEAS) technique.32 Both compounds show a large dissociative cross section at thermal energies (close to zero energy), mainly leading to formation of dehalogenated species. Currents of the most intense fragment negative ions as a function of incident electron energy are presented in Figure 2 (ATR) and Figure 3 (BRX). The complete set of experimental results also includes the metastable slow (microseconds) decay of BRX−, reported in Figures S5−S7 and Table S2 of the Supporting Information. In line with other chlorine derivatives14,33,34 the most intense

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RESULTS Formation of temporary negative ions of ATR and BRX, unstable with respect to both electron detachment and dissociation, was studied using electron transmission spectroscopy (ETS).28 The measured energies of vertical electron attachment (VAEs) were 0.61, 1.0, 2.61, and 4.0 eV in ATR, and 1.3, 2.7, and 4.3 eV in BRX, as shown by the vertical bars reported in the ET spectra of Figure 1. According to B3LYP/631G(d) calculations (Table S1 and Figure S3 in Supporting Information) the two lowest empty molecular orbitals (MOs) of ATR possess π* character and are mainly localized on the aromatic ring (Figure 1), and their energies scaled with an empirical linear equation (see the Supporting Information for description of the method) predict VAEs (0.59 and 1.01 eV) in excellent agreement with the first two (partially overlapped) features displayed in the ET spectrum (VAEs = 0.61 and 1.0 eV). The relatively broad resonance centered at 2.61 eV matches well the position (2.66 eV) calculated for the lowest σ* MO of ATR, with mainly C−Cl character. The VAE of the corresponding σ*C−Cl resonance in chlorobenzene is 0.15 eV smaller.29 The feature detected at 4.0 eV is ascribed to electron 12099

DOI: 10.1021/acs.jpcb.6b10149 J. Phys. Chem. B 2016, 120, 12098−12104

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Figure 2. Currents of mass-selected negative ions formed by resonance electron attachment to atrazine (ATR) as a function of incident electron energy. The most likely strictures of the fragment species and their B3LYP/6-31+G(d) total energies (only electronic contribution) relative to that of the ATR neutral ground state. Optimized geometries of neutral and anionic ATR, C−Cl bond length, and the singly occupied MO (SOMO) are reported.

Figure 3. Currents of mass-selected negative ions formed by resonance electron attachment to bromoxynil (BRX) as a function of incident electron energy. The most likely strictures of the fragment species and their B3LYP/6-31+G(d) total energies (only electronic contribution) relative to that of the BRX neutral ground state. Optimized geometries of neutral and anionic BRX, C−Br bond length, and the singly occupied MO (SOMO) are reported.

dissociative decay of ATR− leads to formation of chloride anions and dechlorinated neutral radical fragments of ATR at incident e− energy of 0.6 eV, in agreement with the thermodynamic energy threshold calculated at the B3LYP/631+G(d) level and reported in Figure 2 (all calculated thresholds and structures of the corresponding fragments can be found in Table S3 and Figure S4 of the Supporting Information).

The currents with m/e = 136 and 179, although 2 orders of magnitude less abundant, are ascribed to negative fragments that do not contain the chlorine atom. Indeed, elimination of the ethylamine substituent together with a neutral chlorine atom, to give the rearranged closed-shell molecule H2NCHClCH3, can be responsible for the observed m/e = 136 signal at zero energy. Elimination of a neutral HCl molecule from ATR− to form the m/e = 179 fragment anion at 12100

DOI: 10.1021/acs.jpcb.6b10149 J. Phys. Chem. B 2016, 120, 12098−12104

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predicted to be very close to zero, but slightly negative. In this case the occurrence of dipole bound molecular anions serving as a “doorway”42,43 to formation of a long-lived valence anion state seems to be unlikely. To complete the presentation of the main results, we briefly discuss the predicted electronic properties of the two molecules under study and the fragments formed by DEA in aquatic ambient (Table S3). The calculated EA (−0.04 eV) of ATR in the gas phase is quite small in comparison with that of BRX (1.43 eV). However, the calculations predict a strong stabilization (3.05 eV) for ATR− on going from the gas-phase to water solvent conditions, whereas BRX− is stabilized by only 0.88 eV. It is to be mentioned that the EA of aquatic ATR is numerically the same (with opposite sign) as the threshold for chloride formation (Table S3), and that the C−Cl bond of ATR− in water is calculated to be 7.476 Å, indicating that ATR is likely to be efficiently dechlorinated by electron attachment in aquatic media.

low electron energy must be accompanied (on energetic grounds) by migration of a H atom to replace the chlorine one. The above-mentioned fragments likely originate from the decay of the lowest π* anion state of ATR, although it cannot be excluded that the zero energy signals can be associated with formation of a dipole bound state. According to the present B3LYP/6-31+G(d) calculations, the dipole moments of both ATR and BRX (4.606 and 3.857 D, respectively) are supercritical (>2.5 D), sufficient to bind an electron in a diffuse σ* orbital.35 Dehydrogenation of ATR is observed at higher energy (1.6 eV) and can be ascribed to electron addition to a mainly σ*C−Cl MO. A sizable shift to lower energy of the DEA peak relative to the corresponding VAE is wellunderstood in terms of survival probability factor.36−38 In contrast to the usual findings in brominated compounds, where DEA mainly produces Br− species,39,40 in BRX the intensity of the bromide signal at thermal electron energies is comparable to that of the complementary fragment anion [BRX−Br]−. In both cases the most stable structures of the fragments produced involve migration of a H atom from an hydroxyl group to replace the outgoing bromine atom (Figure 3). A similar migration likely takes place for the elimination of an HBr molecule from BRX− to form the m/e = 195 anion at thermal energies, in agreement with the calculated energy threshold. Full debromination of BRX is achieved under formation of the m/e = 116 anion, associated with elimination of a Br atom and an HBr neutral molecule. This signal, however, is weak and peaks at 5.1 eV, well above the calculated threshold of 2.69 eV. Owing to the presence of a hydroxyl group (O−H bonds are relatively weak) dehydrogenation of BRX is observed at thermal electron energies, likely through formation of a vibrational Feshbach resonance (VFR)12,14,15 associated with one of the lowest three (vibrationally excited) anion states. The maximum at 5.1 eV in the m/e = 116 current lies above the energy of the higher-lying shape resonance, thus being ascribed to a core-excited resonance,12 whereas the m/e = 167 peak at 3.8 eV (loss of HC(O)Br, Figure S6) originates from debromination accompanied by cleavage of the aromatic ring of the temporary anions formed through the higher π*(ring)/π*CN resonance. Therefore, no signal associated with dissociation of the mainly σ*C−Br and π*CN resonances (VAEs = 1.3 and 2.7 eV) are detected in the DEA spectra of BRX. The presence of long-lived (microseconds) relaxed molecular anions ATR− (m/e = 215) and BRX− (m/e = 277) at thermal energies has some specific importance. According to the calculated optimized geometries of these anions (reported in Figures 2 and 3) the carbon−halogen bond is elongated to 2.423 Å (ATR) and 2.695 Å (BRX), with the captured electron located in a σ* singly occupied MO. However, the excess negative charge on the halogen atom is predicted to be only 0.610 e− (ATR) and 0.504 e− (BRX), so that these partly dissociated species can probably account for the observation of long-lived molecular anions with intensities lower (by 2 orders of magnitude) than that of dehalogenated fragments. Indeed, also in previous work41 long-lived molecular anions were detected in chlorocarbons with a similar (calculated) charge on the chlorine atom and a similar C−halogen distance, but not in DDT, where both the negative charge (0.845 e−) and elongation of the C−Cl bond (4.378 Å) are calculated to be sizably larger. Formation of molecular anions in BRX at thermal energies can reasonably be associated with formation of a VFR. Observation of long-lived ATR− molecular anions is somewhat more surprising, given that the adiabatic EA of ATR is

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DISCUSSION The present findings indicate that efficient dehalogenation of herbicides under investigation is possible not only through a large cross section for formation of fragment halide anions but also via elimination of neutral halogen atoms and hydrogen halides initiated by gas-phase DEA following electron attachment to the lowest unoccupied MOs, also accessible to e− transfer in biological media.44 An analogous mechanism leading to cleavage of a carbon−halogen bond due to electron transfer into vacant MOs was found to be responsible for electrochemical debromination of BRX.17 Reductive dechlorination of ATR in aqueous solution can be mediated by cobalt or nickel porphyrins utilizing various reducing agents as electron donors.45 Under natural conditions ATR undergoes phytoremediation by enzymatic detoxification via cytochrome P450,46,47 and both herbicides can be dehalogenated through microbial metabolism.48,49 Due to the hydrophobic nature of active centers16 the present gas-phase findings can serve as a model for enzymatic reductive reactions. It is thus plausible that the initial mechanism of natural (microbial or vegetable) reductive dehalogenation of ATR and BRX is connected with electron capture followed by dissociation of the substrate molecule, as discussed in the case of metabolic conversion in a series of NSAIDs by P450 enzymes.10 In fact, herbicides are usually characterized by a very high electron-withdrawing ability, responsible for their action as inhibitors of the photosynthetic electron transport.50,51 Similarly, the main pathway of degradation of ATR and BRX is also related to their high EA, as brought forward in pioneering work by Lovelock.7 Provided that xenobiotics are enzymatically transformed by DEA-related pathways, the structures of the metabolites initially formed can be preliminary predicted from DEAS studies. Actually, the fragmentation pathways of a specific molecule possessing high EA are not easily predictable but can be unveiled with relatively simple DEA experiments. For instance, xenobiotics containing an ester bond are mainly transformed in vivo by ester bond cleavage,2 and the same bond is also efficiently broken by gas-phase DEA.52,53 Organic pollutants containing nitro groups undergo microbial reduction with elimination of NO2 substituents,2 in analogy with the corresponding intense decay observed in DEA at thermal electron energies.54−56 Whether the mechanism of reductive dehalogenation is stepwise or concerted57,58 is closely related to 12101

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The Journal of Physical Chemistry B the mechanism of σ bond cleavage, which can occur either via direct formation of a σ* anion state59 or through π*/σ* mixing caused by out-of-plane vibrations to overcome symmetry restrictions. It is also worth mentioning that the energy of the lowest unoccupied MO has been recognized by Burrow and co-workers60,61 as a molecular descriptor to model the rate of dechlorination by zerovalent iron, this process being of particular importance in bioremediation of environmental ATR.62

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CONCLUSIONS Resonance DEA in the gas phase can be considered as a unifying model for the initial mechanism of natural reductive dehalogenation of organic pollutants via enzymatic processes, including phytoremediation by the P450 system of plants. Basic information on initial metabolites can be suggested by DEAS investigations, whereas the MOs involved in electron transfer processes and evaluations of the reduction rates can be investigated with ETS studies and measurements of the absolute DEA cross sections (not accessible under the present experimental conditions). The present findings attract attention on the role of the resonance electron attachment mechanism in electron-driven chemical processes of biological importance, and the usefulness of the electron spectroscopic techniques employed here.

AUTHOR INFORMATION

Corresponding Author

*S. A. Pshenichnyuk. E-mail: [email protected]. Tel/Fax: +7-3472843538. ORCID

Stanislav A. Pshenichnyuk: 0000-0001-5318-3638 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors acknowledge Saint-Petersburg State University (research grant 11.38.219.2014), the Russian Foundation for Basic Research (grants #15-29-05786, #15-02-02809 and #1403-00087) and the Italian Ministero dell’Istruzione, dell’Università e della Ricerca for financial support.

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EXPERIMENTAL AND COMPUTATIONAL METHODS Electron transmission spectroscopy12,13,30 is used in the format devised by Sanche and Schulz.28 To enhance the visibility of the sharp resonance structures, the impact energy of the electron beam is modulated with a small ac voltage, and the derivative of the electron current transmitted through the gas sample is measured. Each resonance is characterized by a minimum and a maximum in the derivative signal. The energy of the midpoint between these features is assigned as the VAE. The electron beam resolution was about 50 meV (fwhm). The energy scale was calibrated with reference to the (1s12s2)2S anion state of He. A general overview of DEAS may be found elsewhere.14,15,32 A magnetically collimated electron beam of defined energy was passed through a collision cell containing a vapor of the substance under investigation. A current of magnetically massselected negative ions was recorded as a function of the incident electron energy in the 0−14 eV energy range. The electron energy scale was calibrated with the SF6− signal, generated by attachment of thermal electrons to SF6. The fwhm of the electron energy distribution was 0.4 eV. A complete description of the experimental equipment including a schematic representation and description of specific conditions can be found in Supporting Information and in ref 63. Atrazine (Sigma-Aldrich #45330) and bromoxynil (#45355) samples with purities 98.8% and 99.6%, respectively, were evaporated at 100 °C, that is, much below their melting points (173.5−175.9 and 189.8−190.7 °C, respectively). The collision cell was held at 110 °C to prevent condensation.

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All calculated virtual orbital energies (VOEs) and their scaled values; structures of the fragment species; calculated total energies of the fragment species relative to that for neutral molecules in the gas phase and water solution; compound and fragment structures; graphic representation of the empty MOs; ET and mass spectra; all DEA spectra in graphic and digitized forms; detailed description and schematic presentation of experimental techniques and specific conditions; description of computational methods (PDF)

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.6b10149. 12102

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DOI: 10.1021/acs.jpcb.6b10149 J. Phys. Chem. B 2016, 120, 12098−12104