Kinetics and Mechanism of Oxidation of Tryptophan by Ferrate (VI)

Article pubs.acs.org/est

Kinetics and Mechanism of Oxidation of Tryptophan by Ferrate(VI) Erik M. Casbeer,† Virender K. Sharma,*,† Zuzana Zajickova,‡ and Dionysios D. Dionysiou§ †

Chemistry Department, Florida Institute of Technology, 150 West University Boulevard, Melbourne, Florida 32901, United States Department of Physical Sciences, Barry University, 11300 NE Second Avenue, Miami Shores, Florida 33161-6695, United States § Environmental Engineering and Science Program, School of Energy, Environmental, Biological, and Medical Engineering (SEEBME), 705 Engineering Research Center, University of Cincinnati, Cincinnati, Ohio 45221-0012, United States ‡

S Supporting Information *

ABSTRACT: Kinetics of the oxidation of tryptophan (Trp) and kynurenine (Kyn), precursors of nitrogenous disinfection byproducts (N-DBP), by ferrate(VI) (FeVIO42−, Fe(VI)) were investigated over the acidic to basic pH range. The secondorder rate constants decreased with increase in pH, which could be described by the speciation of Fe(VI) and Trp (or Kyn). The trend of pH dependence of rates for Trp (i.e., aromatic α-amino acid) differs from that for glycine (i.e., aliphatic α-amino acid). A nonlinear relationship between transformation of Trp and the added amount of Fe(VI) was found. This suggests that the formed intermediate oxidized products (OPs), identified by LC-PDA and LC-MS techniques, could possibly compete with Trp to react with Fe(VI). N-Formylkynurenine (NFK) at pH 7.0 and 4-hydroxyquinoline (4-OH Q) and kynurenic acid (Kyn-A) at pH 9.0 were the major OPs. Tryptophan radical formation during the reaction was confirmed by the rapid-freeze quench EPR experiments. The oxygen atom transfer from Fe(VI) to NFK was demonstrated by reacting Fe18O42− ion with Trp. A proposed mechanism explains the identified OPs at both neutral and alkaline pH. Kinetics and OPs by Fe(VI) were compared with other oxidants (chlorine, ClO2•, O3, and •OH).

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INTRODUCTION In recent years, there is increasing interest in dissolved organic nitrogen (DON) in source waters because of the generation of nitrogenous disinfection byproducts (N-DBPs) in treatment processes.1,2 Sources of DON include algal organic matter, urban runoff, upstream wastewater discharge, organic fertilizer runoff from agricultural regions, and pharmaceutical and pesticide effluents.3,4 Analyzed N-DBPs in treated water include N-nitrosodimethylamine (NDMA), haloacetonitriles (HANs), halonitromethanes (HNMs), and haloacetamides (HAcAms).1,5,6 Both chlorination and chloramination of water can result in the formation of these N-DBPs.4,7,8 Amino acids, peptides, and proteins are present in significant fractions of DON in river and wastewater.9,10 The reaction of chlorine and chloramines with amino acids are shown to be rapid, producing N-DBPs.1,11,12 For example, chlorination of glycine and aspartic acid leads to the formation of cyanogen chloride (CNCl) and haloacetamides, respectively.13,14 Chloramination of amino acids generates CNCl, dichloroacetonitrile (DCAN), and chloropicrin.7 Constituents of urine and sweat from the human body, such as urea and amino acids, are released to swimming pool water.15 The chlorination of swimming pools thus also contributes to N-DBP formation.16,17 Chlorination of Microcystis aeruginosa, a source of toxic microcystins in water, also revealed the production of N-DBPs.18 © 2013 American Chemical Society

N-DBPs in treated and pool waters are of great concern because toxicity tests have shown that NDMA, HANs, HNMs, and HAcAms have more in vitro geno- and cyanotoxicity than trihalomethanes (THMs) and haloacetic acids (HAAs).19,20 Chlorine dioxide (ClO2•) as an alternative disinfectant has attracted significant attention because of its potential to decrease the amount of THMs.21,22 However, ClO2−, the reduced product of ClO2•, may cause undesirable health effects at high dosages.21 Ozone (O3) is able to oxidize precursors of THMs and HAAs, and most of the generated oxidized products detected were aldehydes and short-chained carboxylic acids.8,23,24 Over the past few years, progress on the role of aliphatic amines and amino acids to generate N-DBPs has been made, but similar knowledge on the potential role of nitrogencontaining aromatic compounds is lacking. This is important considering aromatic side chains may produce more yields of N-DBPs than that of aliphatic side chains of amino acids. Tryptophan (Trp) is an α-amino acid with aromatic rings (Figure S1 of the Supporting Information) and is the focus of the present study. Received: Revised: Accepted: Published: 4572

December March 15, March 21, March 21,

24, 2012 2013 2013 2013

dx.doi.org/10.1021/es305283k | Environ. Sci. Technol. 2013, 47, 4572−4580

Environmental Science & Technology

Article

Corrections to pseudo first-order rate constants were done for the spontaneous decay of Fe(VI) at the different pH values. These corrections for Fe(VI) decomposition were ≤5%. The kinetic modeling of the rate constants was conducted using SigmaPlot 2001 software. Stoichiometry and Product Studies. The stoichiometry of the reaction was determined by preparing 2 × 10−4 M Trp solutions and various concentrations of Fe(VI) ranging from 1.0 × 10−4 to 1.0 × 10−3 M. Reactions were completed within 10 min, and the pH of the reaction was determined after mixing. A Waters Alliance 2695 Analytical HPLC instrument connected to a 996 PDA was used for chromatographic analysis. The stoichiometry was determined by comparing the peak area of the Trp remaining in the reaction mixtures to a calibration curve. A Restek C18 5 μm column (150 × 2.1 mm) was used for separation. The sample (100 μL) was injected, and the mobile phase consisted of 10% methanol and 90% aqueous 0.1% acetic acid. Analytes were separated using isocratic elution at a flow rate set at 0.200 mL/min. Chromatograms were detected at 278 nm. Chromatographic analysis (LC-PDA-MS) of organic oxidized products (OPs) of the reaction between Fe(VI) and Trp were conducted using a high-performance liquid chromatography system consisting of a Finnigan Surveyor MS Plus pump, a Finnigan Surveyor Plus autosampler equipped with 25 μL loop, and a Finnigan Surveyor PDA Plus detector. This system was further connected to a Thermo Scientific LCQ Fleet ion trap mass spectrometer equipped with electrospray ionization source. Brownlee Choice C18 5 μm column (100 × 2.1 mm, PerkinElmer) was used for separation together with 95:5% water and methanol (each containing 0.1% acetic acid) as the mobile phase at a flow rate of 0.200 mL/min. Isocratic elution was monitored up to 40 min with 20 μL sample injection. Chromatograms were produced by detection at 225, 278, and 330 nm, and absorption spectra were acquired by scanning 600 to 200 nm. The mass spectrometer was first tuned for sample of tryptophan by direct injection at 5 μL/min and adjustment of electrospray ionization source to the following parameters: spray voltage 5 kV in a positive mode, spray current 1.56 μA, sheath gas flow rate (nitrogen) 5 arb, capillary voltage 0.98 V, and capillary temperature 275 °C. Mass spectra were acquired in a 50−500 m/z range. The same conditions with further adjustment of sheath and auxiliary gas flow rates were used during the LC-PDA-MS analysis. The OPs of the reaction were confirmed by both UV−vis and mass spectra (Figures S3−S7).47 LC-ESI-MSn measurements were also performed for further structural confirmation.48−51 Standard solutions of Trp, Kyn, and 4-hydroxyquinoline (4-OH Q) were used for direct injection measurements. Tuning of the instrument utilizing each individual standard was followed by collision induced dissociation which allowed fragmenting of parent ion resulting in formation of daughter ions. Possible fragmentation patterns of daughters ions were deduced in conjunction with patterns reported in the literature (Figures S3, S4, and S6).48,49 Peak identification in the chromatogram, representing individual degradation products of Trp, was first based on m/z of parent ion and was followed by collision induced dissociation in subsequent run. Acquired parent and daughter ions as well as fragmentation pathways proposed in published literature allowed structure identification of additional OPs, N-formylkynurenine (NFK) and kynurenic acid (Kyn-A) (Figures S5 and S7).50,51

Ferrate (FeVIO42−, Fe(VI)) is an emerging oxidant for treating water and wastewater, which is expected not to produce halogenated DBPs. Fe(VI) can oxidize a wide range of pollutants, including amines, pharmaceuticals, phenolic estrogens, sucralose, and odorous flue gases.25−36 Fe(VI) is effective in precipitating phosphate and metals from wastewater27,37,38 and also inactivates bacteria and viruses, including bacteriophage MS2 and E. coli.39−41 The reactivity of α-amino acids with Fe(VI) has been carried out mostly at high alkaline pH 12.4.42 Detailed kinetics and product identification studies for amino acids have been performed only for glycine (Gly).43 The oxidized products (OPs) of the oxidation of Gly were CO2, ammonia, acetate, and nitrogen.43 The present paper is the first detailed study of kinetics, stoichiometry, and product identification in the oxidation of Trp by Fe(VI) over a wide pH range. The kinetics study was also performed on kynurenine (Kyn) (Figure S2), which is a metabolite product of Trp, which upon chlorination creates N-DBP.44 The objectives of the present paper are: (i) to measure the kinetics of oxidation of Trp and Kyn over an acidic to basic pH range in order to learn the reactivity of Fe(VI) with the amino acid having both aliphatic and aromatic amine moieties, (ii) to postulate a mechanism of the oxidation of Trp by carrying out rapid-freeze quench (RFQ)-electron paramagnetic resonance (EPR) experiments and by identifying OPs by mass spectrometry (MS) techniques, and (iii) to compare the kinetics and products of Fe(VI) oxidation of Trp with other known selective and nonselective oxidants.

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EXPERIMENTAL SECTION Reagents. Organic compounds (Trp, CAS #73-22-3, Kyn, CAS #2922-83-0) and salts were purchased from Sigma-Aldrich or Fischer Scientific, which were of reagent grade or better, and used without further purification. 4-Hydroxyquinoline (CAS #611-36-9) was purchased from Alfa Aesar. Solutions were prepared using distilled water passed through an 18MΩ Milli-Q cm water purification system. Tryptophan and kynurenine solutions were prepared in a 0.01 M sodium phosphate buffer (mono, di, or tribasic depending on desired pH). The pH of the solutions was adjusted before adding ferrate(VI) with the addition of H3PO4 or NaOH and tested using an Orion 720A pH meter equipped with an accumet pH probe. Ferrate(VI) was prepared at high purity (>98%) as potassium ferrate (K2FeO4) by the wet chemical method.45 Fe(VI) solutions were prepared by adding solid K2FeO4 to a 0.005 M Na2HPO4/ 0.001 M Na2B4O7·10H2O buffer solution at pH 9.00. The concentration of Fe(VI) was determined by measuring the absorbance of the solution at 510 nm (ε510 = 1150 M−1 cm−1).45 The pH of the reaction mixtures was determined after mixing either Trp or Kyn and Fe(VI) solutions. Fe18O42− was prepared by mixing solid K2FeO4 with H218O (97 atom % 18 O). The sample was allowed to equilibrate for 15 min, followed by vacuum freeze-drying to remove the solvent.46 Kinetic Studies. Kinetics experiments were carried out using a stopped-flow spectrophotometer (SX.18MV, Applied Photophysics, UK) equipped with a photomultiplier. Measurements were made under pseudo first-order conditions in which [substrate] ≫ [Fe(VI)]. The obtained curves were analyzed using a nonlinear least-squares algorithm in the SX.18MV software. The obtained pseudo first-order rate constants were an average of at least five runs at various concentrations. The kinetics of the reactions of Fe(VI) with Trp and Kyn were performed in the acidic to basic pH range (pH 2.0−12.4). 4573



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Sample freezing for radical determination was carried out in EPR tube by using a System 1000 rapid-freeze quenching apparatus (Update Instruments Inc.) with a cold isopentane bath (−140 °C). The EPR spectra were collected at liquidhelium temperature on a Bruker ER2000D spectrometer in which the sample temperature was maintained with IT503S controller, an ESR910 cryostat, and a LLT650/13 liquid helium transfer tube (Oxford Instruments, Concord, MA).

k[Fe(VI)]Tot [Trp]Tot =

kijαiβj[Fe(VI)]Tot [Trp]Tot (2)

where [Fe(VI)]Tot = [H3FeO4 ] + [H2FeO4] + [HFeO4−] + [FeO42−] and [Trp]tot = [H2Trp+] + [HTrp] + [Trp−]. αi and +

βj represent the species distribution coefficients for Fe(VI) and Trp, respectively, and i and j represent each of the four species of Fe(VI) and each of the three species of Trp, respectively. Of the possible 12 reactions between Fe(VI) and Trp, from the mathematical expression in eq 2, only four reactions (eq 3 or 4, eq 5 or 6, eq 7, and eq 8 or 9) were needed to fit the experimental values of k (solid line in Figure 1). Reactions 3 and 4, reactions 5 and 6, and reactions 8 and 9 involve a proton ambiguity for contribution to the rate constants.

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RESULTS AND DISCUSSION Kinetics. The reaction of Fe(VI) with Trp under pseudo first-order conditions was monitored by following the absorbance of Fe(VI) as a function of time. Decreases of absorbance for the decay of Fe(VI) fit nicely to singleexponential decay. Plots of observed pseudo first-order rate constants (k1) showed linear relationships with concentrations of Trp in both acidic and alkaline media (r2 = 0.99) (e.g., Figure S8). Plots of log k′ versus log[Trp] gave a first-order term with respect to the concentration of Trp throughout the entire pH range. The rate law can then be written as: −d[Fe(VI)] = k[Fe(VI)]tot [Trp]tot dt

∑ i = 1,2,3,4 j = 1,2,3

H3FeO4 + + HTrp → Fe(OH)3 + product(s) k 3 = 8.11(± 0.33) × 105 M−1s−1

(3)

H 2FeO4 + H 2Trp+ → Fe(OH)3 + product(s) k4 = 1.34(± 0.05) × 105 M−1s−1

(1)

The second-order rate constants were determined as a function of pH (2.0−12.4). The rate of the reaction decreases with an increase in pH (Figure 1). The pH dependence is possibly

(4)

H 2FeO4 + HTrp → Fe(OH)3 + product(s) k5 = 9.23(± 0.36) × 104 M−1s−1

(5)

HFeO4 − + H 2Trp+ → Fe(OH)3 + product(s) k6 = 1.22(± 0.04) × 106 M−1s−1

(6)

HFeO4 − + HTrp → Fe(OH)3 + product(s) k 7 = 1.00(± 0.25) × 103 M−1s−1

(7)

HFeO4 − + Trp− → Fe(OH)3 + product(s) k 8 = 1.04(± 0.20) × 103 M−1s−1

(8)

FeO4 2 − + HTrp → Fe(OH)3 + product(s) k 9 = 8.50(± 0.10) × 101 M−1s−1

(9)

The oxidation of Kyn by Fe(VI) also had similar results (Figure 1). The analysis of the variation of k with pH was conducted using three pKa values of Kyn (H2Kyn+ ⇌ H+ + HKyn pK′a1 = 2.21; HKyn ⇌ H+ + Kyn−, pK′a2 = 7.75) (Figure S2). Using the kinetic model of eq 2, only three of the possible 12 reactions between Fe(VI) and Kyn were needed. Reactions 10 and 11 and reactions 13 and 14 introduce a proton ambiguity. When fitting the data, either reaction 10 or 11 could be used to fit the same portion of data with a proton being donated from either the Fe(VI) or Kyn; similarly, reaction 13 or 14 could be used when fitting the data at basic pH. In each case there was no distinct variation in the predicted trend; therefore it is indistinguishable if the proton in the reaction comes from either Fe(VI) or Kyn.

Figure 1. Second-order rate constants (k, M−1 s−1) as a function of pH at 25 °C for the oxidation of Trp, Kyn, Gly, and EDTA. Data for Gly were taken from ref 43.

related to protonations of Fe(VI) and Trp. Fe(VI) is a stronger oxidant upon protonation;52,53 and usually the apparent reaction rate constant increases at lower pH values; therefore, the reaction rate constant of Trp with Fe(VI) is expected to be higher at lower pH. These kinetic measurements at different pH were evaluated using the species of Fe(VI) and Trp over the entire pH range (H3FeO4+ ⇌ H+ + H2FeO4, pKa1 = 1.9; H2FeO4 ⇌ H+ + HFeO4−, pKa2 = 3.5;25 HFeO4− ⇌ H+ + FeO42−, pKa3 = 7.2354 and H2Trp+ ⇌ H+ + HTrp, pK′a1 = 2.38; HTrp ⇌ H+ + Trp−, pK′a2 = 9.3955) (Figure S1). The following model was used to interpret the data in Figure 1 (eq 2)

H3FeO4 + + HKyn → Fe(OH)3 + product(s) k10 = 3.62(± 0.03) × 106 M−1s−1

(10)

H 2FeO4 + H 2Kyn+ → Fe(OH)3 + product(s) k11 = 8.89(± 0.07) × 105 M−1s−1 4574

(11)



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increase in the molar ratio resulted in a decrease in the concentration of Trp. Significantly, the decrease in the concentration of Trp was not linear, and the required concentration of Fe(VI) for complete removal of Trp was ∼4 times over the concentration of Trp at both pH. A slightly greater amount of Fe(VI) was required for transformation of Trp at pH 7.0 as compared to pH 9.0. For example, 80% of Trp transformation needs a molar ratio of 2.5 at pH 7.0, while the same percentage of Trp oxidation requires a molar ratio of 2.0 at pH 9.0. The remaining 20% decrease in Trp was achieved using additional molar ratios of 2.0 at each pH. The stoichiometry results indicate that Fe(VI) in the reaction mixture was not only consumed by the Trp but also by the oxidized product (OPs) of the reaction. It appears that the rates of the reactions of Fe(VI) with OP(s) are similar to cause the competition with the reaction of Fe(VI) with the parent molecule. Furthermore, the rates of the competing reactions may also vary with pH to give small variation in stoichiometry at pH 7.0 and 9.0. Oxidized Products. The OPs identified were NFK (m/z 237), Kyn (m/z 209), 4-OH Q (m/z 146), and Kyn-A (m/z 190). In the reactions of Fe(VI) with Trp, the amount of OPs formed varied with respect to pH. The relative amounts of these products with respect to peak area on the HPLC chromatogram at pH 7.00 and 9.00 are shown in Figures 2a and b. NFK formation gradually increased to a ratio of approximately 4:1 at pH 7.00, followed by a slight decrease (Figure 2a). At pH 9.00, the same trend was seen; however a much smaller amount of NFK was formed (Figure 2b). Kyn formation at pH 7.00 also showed a gradual increase up to the 4:1 ratio, followed by a slight decrease as the amount of Fe(VI) increased. At pH 9.00, however, a larger amount of Kyn was initially formed in a ratio of approximately 3:1, followed by a sharp decrease as the amount of Fe(VI) increased, and eventually no Kyn was seen at a ratio of 10:1. The formation of 4-OH Q showed a gradual increase at both pH 7.00 and pH 9.00, but at pH 9.00 the amount formed was significantly greater than at pH 7.00. Kyn-A showed almost no formation at pH 7.00; however, at pH 9.00 there was a steady increase as the ratio was increased. At pH 7.0, the maximum amount of NFK formed in the reaction was quantified to ∼80 μM (or 80% of Trp) using its molar absorptivity (ε260 = 10980 M−1 cm−1 or ε321 = 3750 M−1 cm−1).57 At pH 7.00, Kyn, 4-OH Q, and KynA were therefore in minor amounts (Figure 2a). The estimated amounts of Kyn and 4-OH Q at pH 7.00, based on peak areas, were 1.8 μM and 2.2 μM (total 4% of Trp). However, when the pH was increased to 9.00, the amount of NFK formed was significantly less while the other three products were formed in greater amounts (Figure 2b). The calculated concentrations of Kyn and 4-OH Q were 5.9 μM and 4.7 μM, respectively. Formation of Kyn-A was much more at pH 9.00 than that at pH 7.0 (Figure 2a and b). This indicates that a greater amount of Trp was transformed to Kyn-A in a basic medium. However, additional unidentified OPs may also be formed in the oxidation of Trp by Fe(VI). Plausible Mechanism. The initial step of the oxidation of Trp by Fe(VI) was examined using the previously established relationship of the rate constant for the reaction of HFeO4− with 1 − e− redox potential of the substrate (log k(1 − e−) = 6.39(±0.05) − 1.83(±0.04) E(1)0)58 to learn the possible formation of Fe(V) and tryptophan radical via a 1 − e− transfer process. Using the calculated rate constant of the reaction of HFeO4− with Trp− (k8 = 1.04 × 103 M−1 s−1; eq 8), the redox

HFeO4 − + HKyn → Fe(OH)3 + product(s) k12 = 4.72(± 0.36) × 103 M−1s−1

(12)

HFeO4 − + Kyn− → Fe(OH)3 + product(s) k13 = 1.39(± 0.14) × 103 M−1s−1

(13)

FeO4 2 − + HKyn → Fe(OH)3 + product(s) k14 = 4.94(± 0.50) × 102 M−1s−1

(14)

The variation of k with pH seen in the present study is compared with aliphatic amino acid, glycine (Gly, NH3+CH2COOH) (dashed lines, Figure 1).43,56 Trp and Kyn had much higher rates of the reaction in acidic media and showed decrease with an increase in pH. In the case of the aliphatic amino acid glycine (Gly, NH3+CH2COOH),43 reaction rates were fastest in the pH range 6.0−10.0 and decreased above and below this range. The comparison in Figure 1 indicates that the reactivity of Fe(VI) with Trp and Kyn may be influenced by the aromatic rings. Otherwise, the kinetic trends would be expected to follow more closely to that of Gly. Stoichiometry. The stoichiometry of the reaction of Fe(VI) with Trp was determined at pH 7.00 and 9.00 by varying the molar ratio of Fe(VI) to Trp (Figures 2a and b). An

Figure 2. Stoichiometry of the reaction between Fe(VI) and Trp and integrated peak areas of OPs at different pH. TrpTryptophan, NFKN-Formylkynurenine, KynKynurenine, 4-OH Q4-Hydroxyquinoline, and Kyn-AKynurenic acid. 4575



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potential for the Trp radical, E0(1) (Trp•+/Trp) was obtained as 1.31 V, which is reasonably close to the reported E0(1) = 1.21 V in the literature.47 Hence, the reaction may initially follow the 1 − e− transfer step (eq 15a). The formation of the radical was explored by stopped-flow UV−visible experiments to see the diagnostic absorption bands of Trp-radical in the visible region. However, due to the fact that the intense and broad optical absorption bands of the Fe(VI) overlap the targeted wavelength range for radical detection (Figure S9), no useful information could be obtained from this set of experiments. The experiments showed only the reactivity of Fe(VI) with Trp. Rapid freeze quench (RFQ) EPR experiments were then attempted by preparing four RFQ samples of the reaction system of (1 × 10−4 M Fe(VI) + 2.5 × 10−3 M L-Trp), which were freeze-quenched at 5 ms, 25 ms, 100 ms, and 320 ms, aiming to trap the putative Trp-radical species. The results are presented in Figure S10. In the 5 ms sample, a very weak radical signal was observed, which vanished in the samples freezequenched at longer time scales. However, this radical disappeared with a half-life of several milliseconds or even less to be trapped by the RFQ technique.59 The disappearance of the radical may be related to its reaction with Fe(VI) to form an adduct, followed by subsequent formation of Fe(III) and Trp-OH (eq 15b). It is assumed that oxygen present in the reaction did not influence the product formation because tryptophan radical has shown a slow reaction with molecular oxygen (k < 106 M−1 s−1),60 whereas the reaction of Fe(VI) with tryptophan radical is expected to be very fast (k ∼ 109 M−1 s−1).61 The formation of an adduct has been suggested in the reaction of Trp with chlorine dioxide.47 The adduct formation in the present study could not be observed in the stopped-flow UV−vis experiments (see Figure S9). This adduct may be decaying at a less than millisecond time scale. Further reaction of Trp-OH with Fe(VI) results in NFK formation (eq 15c). The transformation of Trp to Trp-OH to NFK involved twooxygen atoms transfer, which could be either from Fe(VI) or the solvent, water. HFe VIO4 − + Trp− → HFe V O4 2 − + Trp•

(15a)

(16c)

shows the mass spectrum of obtained NFK, which has three masses (m/z 237, m/z 239, and m/z 241). Additional masses of m/z 239 and m/z 241 were not seen in the mass spectrum of NFK in which unlabeled FeO42− was used (Figure S11). Figure 3 indicates that both one and two oxygen atoms may be transferred from the oxidant to NFK with m/z of 239 and 241, respectively. One oxygen atom might be transferring from the oxidant through one of the possible four reactions 15b, 15c, 16b, and 16c). All four reactions (15b, 15c, 16b, and 16c would form two 18O labeled NFK. In that case, only 18O labeled NFK would form, which contradicts the experimental observation (Figure 3). Hence, two oxygen atoms in NFK may be produced from either reactions 15b and 16c or 15c and 16b. It should be pointed out that all of the oxygen atoms being transferred could be directly from Fe18O42−, followed by an exchange of oxygen from the solvent with 18O. Nevertheless, 18O labeled experiments demonstrate the involvement of oxygen atoms of Fe(VI) in the oxidation of Trp to NFK. Further reactions of NFK with Fe(VI)/Fe(V) species would form Kyn (eq 17). The occurrence of the reaction 17 is supported by the significant reactivity of Fe(VI) with Kyn (Figure 1).

(15b)

HFe VIO4 − + Trp‐OH + H 2O → → Fe(III) + NFK (15c)

The formed Fe(V) species in the reaction 15a may undergo three possible reactions (eqs 16a−c), which are selfdecomposition to Fe(III) (eq 16a), reaction with Trp− to yield Trp-OH (eq 16b), and subsequent formation of NFK (eq 16c). Reactions 16b and 16c are shown as 2-e− transfer steps because a previous work has shown such step in the reactivity of Fe(V) with amino acids, glycine, serine, methionine, and phenylalanine.62 Reactions 16b and 16c caused transformation of two oxygen atoms to form NFK from Trp. These oxygen atoms could be either from Fe(V) or H2O, similar to the reactions 15b and 15c. HFe V O4 2 − + HFe V O4 2 − + 4H 2O → 2Fe(OH)3 + 4OH + O2

HFe V O4 2 − + Trp‐OH + H 2O → Fe(III) + NFK

Figure 3. Zoomed in peaks of mass spectra at m/z 237, 239, and 241 of NFK product in the oxidation of Trp by Fe18O42− (Experimental conditions: [Fe(VI)]:[Trp] = ∼4:1, pH 7.0).

→ → Fe(VI)‐Trp adduct

−

(16b)

The source(s) of oxygen atoms in NFK were examined by reacting isotopically labeled Fe18O42− ion with Trp at pH 7.0. The solution of labeled Fe(VI) was prepared by adding solid K2Fe18O4 into borate/phosphate solution while solid Trp was in the phosphate solution. Both solutions were mixed to keep the molar ratio of Fe(VI) to Trp as ∼4:1 at pH 7.0. In this study, the reaction completed within seconds, and the reaction mixture was immediately subjected to LC-MS analysis. Figure 3

HFe VIO4 − + Trp• + H 2O → Fe(III) + Trp‐OH

HFe V O4 2 − + Trp− + H 2O → Fe(III) + Trp‐OH

HFe VIO4 − /HFe V O4 2 − + NFK → → Fe(III) + Kyn

(16a)

(17) 4576



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Scheme I

decrease from 9.0 to 7.0. For example, the rate constant for the reaction of Fe(V) with phenylalanine decreases from 2.7 × 106 M−1 s−1 at pH 8.8 to 1.2 × 105 M−1 s−1 at pH 7.7.62 Comparative rates suggest that Fe(VI) and Fe(V) may be less likely to react with NFK at pH 7.0 compared to at pH 9.0. Furthermore Fe(V) may be preferentially disappearing by selfdecomposition (reaction 16a) rather than by reacting with NFK (reaction 17). Therefore, NFK remains in the reaction solution at pH 7.0 and does not participate significantly in further reactions (Figure 2a). Since, a little amount of Kyn formed at pH 7.0, the yields of oxidized products of Kyn were small (Figure 2a). At pH 9.0, reactions of NFK with Fe(VI)/Fe(V) species are favorable, which was also seen experimentally in which NFK had a little growth because of its simultaneous decay to Kyn (Figure 2b). Furthermore, Fe(V) would less likely be disappearing by reaction 16a at pH 9.0, which also enhances the possibility of the reaction of Fe(V) with NFK to yield Kyn (eq 17). Once, Kyn formed, it transformed to 4-OH Q and Kyn-A. At pH 9.0, much more of 4-OH Q and Kyn-A were formed due to a higher amount of Kyn formation from the decay of NFK (Figure 2b). The oxidation of Trp by Fe(VI) to yield OPs may be presented by reaction pathways shown in Scheme I. The initial step is the formation of the radical, followed by transfer of one oxygen atom from Fe(VI)/Fe(V) species, which may result in Trp-OH as an intermediate (I). A further reaction of Trp-OH with ferrate species possibly transfers another oxygen atom to

Kyn is an intermediate species (see Figure 2), hence it reacts with Fe(VI)/Fe(V) species to yield 4-OH Q and Kyn-A (eq 18). Formation of Fe(III) as the final reduced iron species of the reaction of Fe(VI) with Trp was confirmed by using 57Fe Mössbauer spectroscopy.63 HFe VIO4 − /HFe V O4 2 − + Kyn → → Fe(III) + 4‐OHQ + Kyn‐A

(18)

Reaction 18 was independently studied by mixing Fe(VI) with Kyn at a molar ratio of 5:1 ([Fe(VI)] = 5.0 × 10−4 M; [Kyn] = 1.0 × 10−4 M; pH 9.0). The degradation of Kyn was 91%, and both 4-OH Q and Kyn-A were seen as oxidized products of the Kyn. The amount of 4-OH Q was estimated to be 2.0% of Kyn. Kyn-A may be formed in larger amounts, but other unidentified products may also account for degradation of Kyn by Fe(VI). Product distribution in Figure 2 at different pH may thus be explained by considering relative rates of the reactions 15−18. Reactions 15a−15c and 16a−16c have strong pH dependence. The oxidation of NFK by Fe(VI)/Fe(V) species may be similar to oxidation of glycine, which had higher rate at pH 9.0 than at 7.0.43,62 The rate constant for self-decomposition of Fe(VI) as well as Fe(V) species (reaction 16a) increases with the decrease in pH. For example, 2kobs for the Fe(V) reaction increases from ∼107 to ∼108 as pH decreases from 9.0 to 7.0.64,65 Comparatively, the rate constants of reactions 15c and 16b are expected to decrease by an order of magnitude as pH 4577



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products were produced from the attack of •OH to both the pyrrole moiety and at the C-2 and C-3 bond and the benzene ring.67 The former process yielded NFK while phenolic compounds resulted from the attack on the benzene ring of Trp.68 Such products were also observed in the oxidation of Trp using Fe(II) and hydrogen peroxide (Fenton reagent)69 (Table 1). This study also showed the formation of Trp radicals, and products included the Trp-Trp dimer. Products of the oxidation of Trp by Fe(VI) had pH dependence. Similar to other oxidants, Fe(VI) had NFK, a major product at neutral pH. However, lower molecular weight transformative products, 4-OH Q and Kyn-A, were generated at the alkaline pH.

form NFK with two oxygen atoms. Subsequent reaction(s) of NFK with ferrate species yield Kyn as another intermediate (II). The oxidation of Kyn by Fe(VI) to 4-OH Q and Kyn-A may be occurring by two separate pathways (Scheme I). Initially, Fe(VI) oxidizes the side chain of Kyn in which attack on amine yields an intermediate III. This step is similar to the oxidation of amines by Fe(VI) through two-electron transfer processes.25,28 The intermediate III may be cleaved to the final OPs by two possible bond cleavages a and b. The first, shown by blue arrows (bond a cleavage), is an attack at the carbon of the carboxylic acid group to release CO2. From this point a ring closure mechanism is followed to form 4-OH Q. In the second pathway, shown by red arrows (bond b cleavage), the Fe(VI) attack occurs at the H-atom leaving the carboxylic acid group intact. A similar ring closure mechanism then occurs to form Kyn-A. Comparison with Other Oxidants. The rate constants of the reaction of Fe(VI) with Trp are compared with selective oxidants (chlorine, ClO2•, and O3) and nonselective oxidant (•OH) (Table 1). Fe(VI) is considered a selective oxidant, and

■

S Supporting Information *

Figures S1−S11: Species of tryptophan and kynurenine with corresponding pKa values; UV−vis and ESI/MS of protonated tryptophan, kynurenine, N-formylkynurenine, 4-hydroxyquinoline, and kynurenic acid; pseudo first-order rate constants versus concentration of tryptophan; stopped-flow UV−vis spectra and EPR spectra of the reaction between Fe(VI) and Trp; and zoomed-in peaks of mass spectrum of NFK product. This material is available free of charge via the Internet at http://pubs.acs.org.

Table 1. Second-Order Rate Constants and Major Oxidized Products of the Reaction of Trp with Different Oxidants oxidant chlorine ClO2 ozone Fe(VI) •

OH

Fenton reagent

pH

k, M−1 s−1

ref

7.2−7.4 7.0 8.0 7.0

1.1 × 10 3.4 × 104 7.0 × 106 1.0× 103

70 47 71 this study

9.0 6.5−8.5

7.0 × 10 1.3 × 1010

7.4

4

2

73

major OPs NFK, Kyn NFK NFK NFK 4-OH Q, Kyn-A NFK, Kyn, and hydroxyl tryptophan NFK, and mono- and dihydroxy tryptophans

ASSOCIATED CONTENT

ref

■

66 47 72 this study

AUTHOR INFORMATION

Corresponding Author

*Phone: 321-674-7310. Fax: 321-674-8951. E-mail: vsharma@ fit.edu.

68

Notes

69

■

The authors declare no competing financial interest.

ACKNOWLEDGMENTS V.K.S. and D.D.D. acknowledge the support of the United States National Science Foundation (CBET 1236331) for this research. We wish to thank professor Aimin Liu for his help in RFQ EPR experiments. We also thank anonymous reviewers for their comments which improved the paper greatly.

it had the least reactivity with Trp among the oxidants (Table 1). However, Fe(VI) has sufficient reactivity (t1/2 = 14 s, 10 mg K2FeO4/L or 2.8 mg Fe/L at pH 7.0) to transform Trp. Additionally, Fe(VI) may be advantageous in treating aromatic nitrogeneous compounds in water because it does not react with Br−, a possible component of the water matrix.58 Comparatively, chlorine (i.e., HOCl) can react with Br− to form HOBr, which can produce toxic halogenated byproducts. O3 also reacts with Br− to form carcinogenic bromate ion.23 Hydroxyl radicals react with organic molecules indiscriminately and have a diffusion-controlled rate constant (Table 1). Because of such high reactivity, •OH may be easily consumed by all kinds of matrix components including Br− and hence may lower the transformation efficiency of nitrogenous compounds. The products of the oxidation of Trp by HOCl are not clear, but UV−vis spectroscopy identification suggested the formation of NFK and Kyn (Table 1).66 The radical-mediated mechanism was proposed to yield the products of the reaction. NFK was also the major product of the oxidation of Trp by ClO2 (Table 1).47 However, a recent study demonstrated a number of products depending on the molar ratio of ClO2 to Trp.22 ClO2 attacks the nitrogen atom of the amino acid and the indole ring to yield the products of the oxidation. In using excess ClO2, the most abundant products were oxalic and fumaric acid, which indicates the extensive C−C bond breaking in Trp.22 Oxidation of Trp by •OH is complicated, and oxidized

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Kinetics and Mechanism of Oxidation of Tryptophan by Ferrate (VI)

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