Enhanced Indirect Photochemical Transformation of Histidine and

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Enhanced Indirect Photochemical Transformation of Histidine and Histamine through Association with Chromophoric Dissolved Organic Matter Chiheng Chu,† Rachel A. Lundeen,† Christina K. Remucal,‡ Michael Sander,*,† and Kristopher McNeill*,† †

Institute of Biogeochemistry and Pollutant Dynamics (IBP), Department of Environmental Systems Science, ETH Zurich, 8092 Zurich, Switzerland ‡ Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, Wisconsin 53706, United States S Supporting Information *

ABSTRACT: Photochemical transformations greatly affect the stability and fate of amino acids (AAs) in sunlit aquatic ecosystems. Whereas the direct phototransformation of dissolved AAs is well investigated, their indirect photolysis in the presence of chromophoric dissolved organic matter (CDOM) is poorly understood. In aquatic systems, CDOM may act both as sorbent for AAs and as photosensitizer, creating microenvironments with high concentrations of photochemically produced reactive intermediates, such as singlet oxygen (1O2). This study provides a systematic investigation of the indirect photochemical transformation of histidine (His) and histamine by 1O2 in solutions containing CDOM as a function of solution pH. Both His and histamine showed pH-dependent enhanced phototransformation in the CDOM systems as compared to systems in which model, low-molecular-weight 1O2 sensitizers were used. Enhanced reactivity resulted from sorption of His and histamine to CDOM and thus exposure to elevated 1O2 concentrations in the CDOM microenvironment. The extent of reactivity enhancement depended on solution pH via its effects on the protonation state of His, histamine, and CDOM. Sorptionenhanced reactivity was independently supported by depressed rate enhancements in the presence of a cosorbate that competitively displaced His and histamine from CDOM. Incorporating sorption and photochemical transformation processes into a reaction rate prediction model improved the description of the abiotic photochemical transformation rates of His in the presence of CDOM.

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INTRODUCTION Dissolved amino acids (AAs) are ubiquitous in surface waters in which they make up a substantial fraction of the dissolved organic nitrogen pool.1 Dissolved AAs are major nitrogen and carbon sources for environmental microorganisms in these systems.2 As a consequence, chemical transformations of dissolved AAs affect the biogeochemical cycling of these nutrients in surface waters. Previous work has demonstrated that abiotic photochemical oxidation is a major transformation pathway of AAs in sunlit waters.3−5 Photooxidation may occur both directly and indirectly, depending on whether the oxidation follows direct light absorption by the AAs or the oxidation of the AAs occurs by reaction with dissolved photochemically produced reactive intermediates (PPRI).5−10 A major source of PPRI in sunlit waters is chromophoric dissolved organic matter (CDOM).11 Upon light absorption, CDOM can be promoted to an excited state that subsequently transfers energy either internally or to another molecule (e.g., oxygen) to form a suite of PPRI, including singlet oxygen (1O2), hydroxyl radical (•OH), hydrogen peroxide (H2O2), and triplet-state excited chromophoric organic matter (3CDOM*). © 2015 American Chemical Society

PPRI largely affect the cycling of major elements (i.e., carbon, sulfur, and nitrogen), as well as biologically important trace metals in sunlit waters.11−15 Boreen et al.5 demonstrated that tryptophan (Trp), methionine (Met), tyrosine (Tyr), and histidine (His) are photolabile in CDOM-rich solutions. The relative contribution of indirect phototransformation by reaction with CDOM-formed PPRI to the total phototransformation varies substantially among the different AAs.5 The major indirect transformation pathway of Trp is via reaction with 3CDOM*16 and likely involves both oxidation via electron transfer17,18 and reaction by energy transfer.19,20 Met and Tyr may react relatively unselectively with •OH, H2O2, 3 CDOM*, and 1O2.5,21 Conversely, the phototransformation of His in CDOM-containing solutions is exclusively indirect and due to reaction with 1O2.5 Received: Revised: Accepted: Published: 5511

January 27, 2015 March 31, 2015 April 1, 2015 April 1, 2015 DOI: 10.1021/acs.est.5b00466 Environ. Sci. Technol. 2015, 49, 5511−5519

Environmental Science & Technology

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AAs may associate with organic matter, and such association affects the distribution,22−24 transformation,25 and bioavailability26,27 of AAs. Although the importance of indirect photolysis of AAs involving CDOM has been demonstrated, previous studies have not systematically assessed whether the association of AAs with CDOM leads to enhanced photochemical reactivity. Such enhanced reactivity can be expected given the heterogeneous distribution of CDOM-derived PPRIs in solution with much higher concentrations within and near the CDOM macromolecules than in the bulk solution.28 Enhanced phototransformation has previously been demonstrated for organic molecules other than AAs when associated with CDOM, as compared to the reactivity of the same molecules in bulk solution without CDOM. Burns et al.13 reported enhanced reactivity of mirex with solvated electrons when associated with dissolved chromophoric humic substances. Enhanced photochemical reactivity was also observed for hydrophobic 1O2 probe molecules,28,29 methyl mercury,30,31 and silver ions as a result of association with CDOM.32 The enhanced phototransformation rates of positively charged radical probes over neutral or negatively charged probes in CDOM containing solutions were ascribed to enhanced sorption of the positively charged probes to CDOM through attractive electrostatic interactions.33 Whereas the association of AAs with CDOM has previously been reported34 and was shown to involve both physisorption (i.e., association through electrostatic attraction and the hydrophobic effect) and chemisorption,22,26,35−39 a systematic assessment of enhanced photochemical transformation through association of AAs with CDOM is missing from the literature. This assessment is important to advance our understanding and capability to predict the fate and availability of AAs and the cycling of proteinaceous nitrogen and carbon in sunlit surface waters. The goal of this study was to systematically assess the photochemical transformation of His and histamine in aqueous solutions containing CDOM. To determine the effects of probe compound speciation and association with CDOM on phototransformation, irradiation experiments were carried out over a wide pH range and with either CDOM or one of three model photosensitizers: Rose Bengal, perinaphthenone, or lumichrome. Irradiation experiments were complemented by sorption experiments to determine the extent of His and histamine sorption to CDOM. In this study, His was chosen due to its high and selective reactivity with 1O2.5 Furthermore, His is an ideal probe compound given that the imidazole side chain has an acidity constant (pKa) of 6.0 and thus undergoes protonation/deprotonation reactions over the environmentally relevant pH range. Although the protonated species is expected to have lower reactivity with 1O2 than neutral His, it is also expected to sorb more strongly to the negatively charged CDOM and may hence experience enhanced 1O2 concentrations. Finally, as compared to other AAs, His is of particular interest because it is a highly valuable substrate for microorganisms both in terms of its high N content and thermodynamic cost of formation.40,41 We included histamine, an important metabolite of His,42 for many of the same reasons. Furthermore, because histamine does not contain the carboxylate moiety of His, it is an interesting structural analog of His that is positively charged at neutral pH and hence is expected to sorb more strongly to CDOM than His.

Article

MATERIALS AND METHODS

Materials and Sample Preparation. L-Histidine, Lhistamine, L-phenylalanine, disodium hydrogen phosphate, lumichrome, Rose Bengal (RB), perinaphthenone, 1,3dimethylimidazolium methanesulfonate ((Me2Im)(MeSO3)), and sodium methanesulfonate (Na(MeSO3)) were obtained from Sigma-Aldrich. Deuterium oxide (D2O, 99.8 atom % D) and deuterium chloride (DCl, 1.0 M in deuterium oxide, 99.8 atom % D) were obtained from Armar Chemicals. Acetic acid and boric acid were obtained from Fluka, potassium dihydrogen phosphate and borax were from Merck, and sodium acetate was from VWR. These chemicals were used as received. All solutions were prepared using purified water (milli-Q water, 18.2 MΩ·cm; from a Barnstead Nanopure Diamond Water Purification System). Furfuryl alcohol (FFA) was used as a probe to determine the steady-state 1O2 concentration in the bulk aqueous phase ([1O2]aq). FFA was obtained from SigmaAldrich and distilled prior to use. 6-Aminoquinolyl-Nhydroxysuccinimidyl carbamate (AQC), an amino acid derivatizing agent, was synthesized and prepared according to literature procedures.6,43 Suwannee River Natural Organic Matter (SRNOM, lot 1R101N) was purchased from the International Humic Substances Society (IHSS) and used as received. SRNOM was chosen as a model for aquatic CDOM because it is soluble in water in high concentrations (>100 mg C/L) at pH 4.0−9.0 (see Supporting Information (SI) Section S1 for SRNOM solution preparation). All SRNOM solutions used in the photolysis and sorption experiments had a concentration of 11.4 mg C/L. No effort was made to quantify the background histidine and histamine concentrations in SRNOM because the background concentrations are expected to be small relative to the added amounts of His and histamine. Photolysis of His and Histamine in Homogeneous and Microheterogeneous Systems. The sensitized photolyses of His and histamine were carried out in separate experimental setups over a range of pH values using either (i) one of three model 1O2-sensitizers (i.e., lumichrome, RB, or perinaphthenone; see SI Section S2 for the structures of sensitizers), or (ii) SRNOM as the sensitizer. We refer to the first systems as homogeneous systems because photolysis of these low-molecular-weight sensitizers led to a uniform distribution of 1O2 in the solution. Conversely, the SRNOM system is hereafter referred to as microheterogeneous system, with 1O2 being nonuniformly distributed with higher concentrations in the SRNOM than in the bulk solutions.28 In the homogeneous systems, we used lumichrome and RB as the 1O2 sensitizers for His and histamine at pH > 4.0, respectively. Perinaphthenone was used as a 1O2 sensitizer for both His and histamine at pD < 4.0. The latter experiments at low pD were conducted in D2O to achieve higher steady state concentrations of 1O2 as compared to using H2O. Solutions with pD < 4.0 were pDadjusted with DCl where pD = pH* + 0.4 (pH* corresponds to the uncorrected pH meter reading). Solutions with pH > 4.0 were pH-buffered using either acetate (pH 4.0−6.0), phosphate (pH 6.0−7.8), or borate (above pH 7.8), all at 2 mM. Photolysis did not affect the solution pH. The solutions used in photolysis experiments contained His or histamine (both at initial concentrations of 40 μM), FFA (initial concentrations of 40 μM), and a 1O2 sensitizer (i.e., either one of the three model 1 O2-sensitizer or SRNOM). Prior to photolysis, solutions containing SRNOM were stored overnight in the dark at 4 °C 5512

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derivatized with AQC and subsequently analyzed by UPLC with fluorescence detection. Detailed information on sample preparation, UPLC separation, and detection parameters is provided in the SI. Calculation of 1O 2 Reaction Rates of His and Histamine. The photolysis rate constants of His and histamine were calculated according to the same procedure, as detailed in the following for His only. The bimolecular reaction rate constant, krxn (units of M−1 s−1), of His with 1O2 was calculated from the observed rate constant of His pseudo-first-order phototransformation (kHis obs) and the steady state concentration of 1O2, [1O2]aq (eq 1). The steady state concentration of 1O2 7 −1 −1 46 was determined according to eq 2 (kFFA s ), rxn = 8.3 × 10 M FFA where kobs corresponded to rate constant of first-order fits to the degradation curves of FFA and corresponded the secondorder rate constant for FFA with 1O2.

to allow for attainment of apparent sorption equilibrium of His or histamine to the SRNOM. Sensitizer-free solutions served as controls to measure any direct phototransformation of His and histamine. All photolysis experiments were conducted in borosilicate test tubes and in duplicate. Lumichrome-, perinaphthenone-, and SRNOM-sensitized photolyses were conducted in a photochemical reactor (Rayonet) equipped with two to ten 365-nm bulbs (Southern New England Ultraviolet Co., RPR3500 Å). RB-sensitized photolyses were conducted using a xenon lamp (300 W; Newport) with a 455-nm long-pass filter. At designated time points, aliquots from the photolysis solution were taken for kinetic analysis. Aliquots were divided into two for (i) FFA analysis and (ii) His or histamine analysis following AQC derivatization (see below). Photolysis of His and Histamine in Microheterogeneous Systems in the Presence of a Sorptive Competitor. Analogous His and histamine photolyses with SRNOM were carried out as described above but here in the presence of excess Me2Im+ with the anion MeSO3−, a sorptive competitor (400 μM). The control photolysis solutions contained identical concentration of SRNOM, His or histamine (40 μM), and the inert salt Na(MeSO3) (400 μM) instead of Me2Im+. Photolysis experiments were conducted using the Rayonet setup (see above). Sorption of His and Histamine to SRNOM. Sorption experiments were carried out over a range of initial His concentrations (32.6−76.6 μM) and from pH 4.3 to 7.8, all at a constant concentration of SRNOM (i.e., 11.4 mg C/L). Following sorptive equilibration (around 18 h), the concentration of freely dissolved His was determined after passing the solution over centrifugal membrane filters (2000 MWCO Hydrosart regenerated cellulose membrane; Vivacon 500, Sartorius AG, hydrophilic and nonprotein binding) to remove SRNOM. We note that SRNOM could not be removed from solution by standard centrifugation. The cutoff size of the membrane was sufficiently small to make it impermeable to the larger SRNOM components but permeable to the much smaller molecular weight compounds (e.g., His). Centrifugation was carried out in a fixed-angle centrifuge rotor for 15 min at 7500g. The aqueous concentration of His in the filtrate was subsequently quantified (see below). The His concentration sorbed to SRNOM was calculated by mass balance using the known initial and measured final concentration of freely dissolved His. Sorption of histamine to SRNOM was assessed using the same approach. A number of control experiments were run to rule out any possible filtration artifacts: for instance, membrane filtration of solutions containing either His or histamine but no SRNOM resulted in full sample recovery, where the recovery of His and histamine was 98.9% and 99.0% at pH 5.0, respectively. For solutions containing only SRNOM, 19% at pH 5.0 and 17% at pH 7.0 of SRNOM in terms of absorbance at 365 nm were found to pass through the membrane (see SI). Partial transfer through the membrane was consistent with the polydisperse character of CDOM44 including low molecular weight components.45 In separate sorption experiments we demonstrated that His did not sorb to the SRNOM fraction that passed through the membrane (SI, Section S8). Quantification of FFA, His, and Histamine. FFA concentrations were quantified using a Waters ACQUITY ultra high-pressure liquid chromatography (UPLC) coupled to a photodiode array detector. His and histamine were

His k rxn =

His kobs

[1O2 ]aq

[1O2 ]aq =

(1)

FFA kobs FFA k rxn

(2)

In the homogeneous systems (i.e., model photosensitizers) with uniform concentrations of 1O2, the determined second-order rate constants for His, kHis rxn , reflected the true bimolecular rate constant. However, in the microheterogeneous system, in which photolysis of SRNOM resulted in a microheterogeneous distribution of 1O2, the second-order rate constants determined for His were apparent rate constants. In many cases, the apparent rate constants for His were significantly higher than the true rate constants, due to association of the His with SRNOM and hence exposure of His to higher [1O2] as compared to the bulk solution. The probe FFA does not sorb to SRNOM and hence experienced the bulk solution [1O2].28 Prediction Model of Sorption-Enhanced Phototransformation. In the homogeneous systems, the fractions of neutral and protonated His species (i.e., f His0 and f His+) can be calculated based on the pKa of the imidazolium ring and the solution pH. Using the respective reaction rate constants of His 0 in either the neutral or protonated form with 1O2 (kHis rxn and +

kHis rxn ) allows for the prediction of the reaction rate (kpred) as a function of pH (eq 3). 0

+

His His k pred = k rxn fHis0 + k rxn fHis+

(3)

In the microheterogeneous system, the kinetic model to predict His photochemical reactivity needs to account for the sorption of His to SRNOM. A binding constant, Kb (with units of M−1) was used to describe sorption of His+ to anionic sites in SRNOM (CDOM−). The cation binding equilibrium was used to fit the pH-dependent sorption isotherms of His to SRNOM (eq 4), where [His+], [His+CDOM−], and [CDOM−] are the concentrations (M) of free His+, His+ sorbed to SRNOM and negatively charged sites in SRNOM, respectively. Concentrations of free His+ and sorbed His+ were calculated based on the equilibrium of acid dissociation (eq 5, where [His0] is the concentrations of free His0, Ka is the acid dissociation constant of His (M)) together with mass balance of His (eq 6, where [Histot] is the total concentration of His (M)). [His+CDOM−] = Kb[His+][CDOM−] 5513

(4)

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Figure 1. Phototransformation for singlet oxygen (1O2)-mediated transformation of histidine (His) in solutions containing the photosensitizers (a) lumichrome or (b) SRNOM with pH ranging from 4.3 to 7.8. His transformation (natural logarithm of the ratio of His concentration at time point t and initial concentration, ln([His]t/[His]0)) was normalized to a representative 1O2 steady state concentration of 11.3 pM in the lumichromesensitized photolysis experiments and 0.6 pM in the SRNOM-sensitized photolysis experiments and plotted versus photolysis time (t). Solid lines represent the first-order fits of the experimental data (symbols). Error bars represent the range in values of duplicates. When error bars are invisible, they are contained within the marker symbols.

Ka =

[His0][H+] [His+]

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RESULTS AND DISCUSSION Phototransformation Rates of His and Histamine in Homogeneous Systems. The photochemical transformation rates of His and histamine in homogeneous systems were assessed as a function of solution pH. Photolysis of the sensitizers lumichrome and RB resulted in steady state concentrations of 1 O2 during the photolysis over the tested pH range (SI Tables S1 and S2, respectively). The phototransformation of His by reaction with 1O2 followed first-order kinetics at all investigated pH values (Figure 1a). The rate constants of His transformation were highly pH-dependent and increased from pH 4.4 to 7.1. The rate constants at pH 7.1 and 7.7 showed statistically no difference (95% confidence interval) (Figures 1a and 2a). The observed dependence of His krxn with 1O2 on pH was consistent with previous studies.48,49 Although the pH dependence of histamine krxn with 1O2 was not previously reported, it had comparable pH trend as His, and the krxn also increased as the pH increased from 4.2 to 7.7 (Figure 2c). The observed pH dependency resulted from the much higher 1O2 reaction rate constant (over 3000 times, see below) of the nonprotonated imidazole in His0 and the singly protonated histamine (i.e., histamine+, with protonation of the amine group) than of the protonated imidazolium in His+ and the doubly protonated histamine (i.e., histamine2+, protonation of both the amine and imidazole groups). Detailed information on His and histamine phototransformation rate constants are provided in SI Tables S1 and S2. Using the respective rate constants for different protonation states of His and histamine and their respective pKa values, the reaction rate constants (kpred) with 1O2 could be predicted as a function of solution pH. We first determined the krxn of neutral 0 7 −1 −1 and protonated His with 1O2 (i.e., kHis s at rxn = 6.5 × 10 M + His 4 −1 −1 pH 7.7 and krxn = 2.0 × 10 M s at pD 2.5, respectively) + 2+ ) and histamine2+ (khistamine ) (i.e., and of histamine+ (khistamine rxn rxn + 2+ 7 −1 −1 histamine khistamine = 8.8 × 10 M s at pH 7.7 and k = 2.8 × rxn rxn 104 M−1 s−1 at pD 2.5, respectively). Herein, we assumed that 1 O2 was the only oxidant for His and histamine, based on our prior study of the indirect photochemistry of His.5 We subsequently calculated kpred values, according to eq 3, as a

(5)

+ −] = [His [His0] + [His+] + [HisCDOM tot ]

(6)

The overall concentration of negatively charged moieties in SRNOM ([CDOM−]) as a function of solution pH was calculated using a modified Henderson−Hasselbalch equation for two classes of binding sites and the parameters for SRNOM published by the IHSS (eq 7).47 ⎛ ⎞ ⎛ ⎞ Q1 Q2 ⎟ ⎜ ⎟ Q tot = ⎜⎜ + ⎟ ⎜ + 1/ n1 + 1/ n2 ⎟ ⎝ 1 + (K1([H ]) ⎠ ⎝ 1 + (K 2([H ]) ⎠ (7)

Qtot is the overall negative charge density of SRNOM, Q1 and Q2 are the maximum charge densities of the two classes of binding sites with K1 and K2 as the corresponding proton binding constants, and n1 and n2 are empirical parameters that describe the distribution of proton affinities for both binding sites. [CDOM−] was calculated by multiplying overall negative charge density with the CDOM concentration, [CDOM] (mg C/L), via eq 8. [CDOM−] = [CDOM]Q tot

(8)

The reaction rate contributions of His0 and His+ were calculated based on their respective amounts in bulk solution or sorbed to SRNOM and reaction rate constants. Together with the binding constant obtained above, a kpred curve that accounted for the sorption of His (i.e., considering the fractions of dissolved His0 (f His0) and dissolved and sorbed His+ (f His+ and f His+CDOM−)) was made (eq 9) and fit with krxn measured in CDOM solution. The term [1O2]CDOM /[1O2]aq was introduced to describe the 1O2 concentration ratio between CDOM ([1O2]CDOM) and the bulk aqueous phase ([1O2]aq). 0

+

His His k pred = k rxn fHis0 + k rxn fHis+ +

[1O2 ]CDOM 1

[ O2 ]aq

+

His k rxn fHis+

CDOM−

(9) 5514

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Figure 2. (a) Phototransformation rate constants for singlet oxygen (1O2)-mediated transformation of His at different solution pH values from the following experiments: Lumichrome-sensitized photolysis of His (homogeneous system; red squares); SRNOM-sensitized photolysis of His (microheterogeneous system; blue diamonds). (b) Experimentally measured 1O2-mediated reaction rate constants of His compared to predicted rate constants, krxn /kpred, in lumichrome- and SRNOM-sensitized experiments. (c) Phototransformation rates for 1O2-mediated transformation of histamine at different solution pH from the following experiments: Rose Bengal (RB)-sensitized photolysis of histamine (homogeneous system; red squares); SRNOM-sensitized photolysis of histamine (microheterogeneous system; blue diamonds). (d) Experimentally measured 1O2-mediated reaction rate constants of histamine compared to predicted rate constants, krxn /kpred, in RB- and SRNOM-sensitized experiments. The solid lines in panels (a) and (c) correspond to the predicted rate constants (kpred) calculated from eq 2 herein. krxn /kpred values at different pH values in (b) and (d) are connected to show the tendency of rate enhancement over pH (dashed lines). Error bars in (a) and (c) represent the ranges of duplicates.

with 1O2 in microheterogeneous systems allows the determination of krxn of His and histamine with 1O2 as a function of solution pH. Because FFA does not associate with CDOM, the FFAmeasured [1O2]aq values in microheterogeneous systems represent the 1O2 concentration in the bulk solution.28 For solution conditions under which His and histamine do not sorb to SRNOM, the calculated krxn of His and histamine should therefore be the same as measured in homogeneous systems. Conversely, under solution conditions that lead to association of His and histamine with SRNOM and hence exposure to elevated 1O2 concentrations than in the bulk solution measured by FFA, the measured krxn values are expected to be higher than the predicted values. In a first step, we characterized the sensitizing efficiency and the photostability of SRNOM. The quantum yield of 1O2 generation from the photolysis of SRNOM using 365-nm light (i.e., ΦSRNOM) was determined using perinaphthenone as a quantum yield standard (Φperi = 0.98).50 The 1O2 quantum yields of SRNOM ranged from 1.00 ± 0.01% at pH 4.3 to 0.77 ± 0.01% at pH 7.6 (SI, Section S4). These quantum yields are slightly lower than the reported literature value of 2.02% measured at pH 7 with exposure to solar-simulated light.51 We further established that photolysis of the SRNOM did not lead to photobleaching or irradiation-induced precipitation, with no difference on the absorbance spectrum of SRNOM before and after the irradiation (data not shown).

function of solution pH by considering its effect on the speciation of His (pKa = 6.0) and histamine (pKa = 5.8). The kpred values were in very good agreement with the experimental krxn values over the entire tested pH range for both His and histamine in homogeneous systems (Figure 2a and c). The good agreement between experimental data and predictions was also evident from Figure 2b and d in which we plotted the ratio (krxn /kpred) as a function of pH. This ratio was close to unity over the entire pH range. The good agreement of kpred values with experimental krxn values from photolysis of solutions containing established 1O2 senstizers validated the experimental setup. Furthermore, it demonstrated that the pH-dependent krxn of His and histamine with 1O2 could be well predicted in homogeneous systems (i.e., uniform distribution of 1O2 in the system and no association of the probes (His and histamine) to the sensitizers). Phototransformation Rates of His and Histamine in Microheterogeneous Systems. The foregoing discussion focused on the pH-dependent indirect photochemistry of His and histamine in homogeneous systems. This section addresses the phototransformation of His and histamine in microheterogeneous systems, where SRNOM photolysis resulted in a nonuniform distribution of 1O2. It is important to recall that indirect phototransformation of His sensitized by CDOM is dominated by its reaction with 1O2, while other PPRI (e.g., • OH or 3CDOM*) are only minor contributors.5 Similar to homogeneous systems, the selective reaction of His and histamine 5515

DOI: 10.1021/acs.est.5b00466 Environ. Sci. Technol. 2015, 49, 5511−5519

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Figure 3. Ratios of the experimental reaction rate constants and the predicted reaction rate constant, krxn/kpred, of (a) His and (b) histamine as a function of solution pH in the presence of either the sorptive competitor (Me2Im)(MeSO3) (green solid triangles) or sorptive control, Na(MeSO3) (purple open triangles). All photolysis experiments were conducted in the presence of SRNOM in solutions (herein described as microheterogeneous systems). The krxn/kpred values at different pH are connected by straight lines to help visualize the pH dependencies. The dashed line at krxn/kpred= 1 represents the ratio expected for homogeneous systems.

His and Histamine Phototransformation Kinetics in Microheterogeneous Systems in the Presence of a Sorptive Competitor. To provide independent evidence for the proposed sorption-enhanced phototransformation mechanism in microheterogeneous systems, binary solute experiments were conducted containing His or histamine as the target compounds and excess amounts of the sorptive competitor Me2Im+ (e.g., structure in Figure 4). A control experiment with Na(MeSO3) was also conducted to assess potential effects of changes in solution ionic strength on phototransformations. As hypothesized, the presence of Me2Im+ at pH > 6 had no measurable effect on the krxn value of His, such that the krxn/ kpred ratio remained around unity (Figure 3a). By contrast, at pH 5.1, the presence of Me2Im+ markedly decreased the krxn of His: the krxn/kpred ratio decreased from 3.5 to 1.3 (cf., Figures 2b and 3a). The krxn value therefore approached kpred, which is consistent with competitive displacement of His+ from SRNOM by Me2Im+ and loss of the sorption-enhanced transformation of His. The addition of Na+ in the control experiment at the same concentration as Me2Im+ did not affect krxn (cf., Figures 2b and 3a), demonstrating that changes in solution ionic strength had no effect on His phototransformation. Similarly, the transformation rate constants of histamine were suppressed upon addition of Me2Im+ at low pH (Figure 3b), while no effect was detected upon addition of Na+. The competitive bisolute experiments shown in Figure 3 were conducted at different pH values, but at constant concentration ratios of the competitor to either His or histamine. We further assessed the transformation of His at a constant pH value (pH 5.1) with increasing concentrations of Me2Im+. In these experiments, Na(MeSO3) was added to the same solutions to achieve a total concentration of 400 μM ((Me2Im)(MeSO3) + Na(MeSO3)). The His transformation rate constant decreased with increasing amounts of added Me2Im+: as [Me2Im+] increased from 0 to 400 μM, the krxn/ kpred ratio dropped from 3.1 to 1.2 (Figure 4). The decreased His and histamine transformation rate constants upon addition of Me2Im+ to SRNOM solutions directly support the proposed sorption-enhanced phototransformation mechanisms of His and histamine. Sorption of His and Histamine to SRNOM. The photolysis experiments of His and histamine strongly suggested that sorption-enhanced transformation was occurring. Direct

Following the studies on sensitizing efficiency of SRNOM, separate photolysis experiments with His and histamine were conducted in the presence of 11.4 mg C/L SRNOM. The phototransformation kinetics of both His (Figure 1b) and histamine (kinetic data not shown) with 1O2 in SRNOM solutions followed first-order kinetics at all pH values. The underlying reaction rate constants of His (Figure 2a) and histamine (Figure 2c) with 1O2 increased with increasing solution pH. At pH > 6.0, the experimental krxn values of His in the SRNOM system were in good agreement with the predicted values, kpred (Figure 2a). The good agreement of observed and predicted krxn at pH > 6 is also evident from plots illustrating the krxn/kpred ratios, which are close to unity (Figure 2b). Conversely, between pH 4.0 and 6.0, the measured His transformation rates in SRNOM solutions were higher than the predicted rates (Figure 2a and b). For instance at pH 5.1, the experimental krxn was more than three times higher than the predicted rate, suggesting that His underwent enhanced phototransformation through association with SRNOM. Unlike His, histamine data show enhanced phototransformation rates over the entire tested pH range (Figure 2c) as compared to homogeneous systems. Histamine does not contain the negatively charged carboxylate group in His (cf., structures in Figure 2a and c) and therefore carries a net positive charge at high pH values (i.e., pKa = 9.4 for the amino group). The net positively charged histamine likely showed minor sorption to SRNOM and hence slightly enhanced reactivity as compared to homogeneous system. The enhancement of krxn/kpred at high pH values was, however, much lower than the ratio at low pH, suggesting much weaker cation binding via the positively charged amine than the protonated imidazolium ring to SRNOM (Figure 2d). This explanation is supported by a study of Droge et al.52 who systematically determined the binding affinity of various organocations to CDOM. Of the examined organic cationic functional groups, charged imidazoles had a particularly high binding affinity to CDOM because heterocyclic N atoms are hydrogen-bond donors.52 The enhanced phototransformation of His and histamine in SRNOM-containing solutions compared to homogeneous systems over part of or the complete tested pH range is therefore consistent with the proposed sorption-enhanced phototransformation process in microheterogeneous systems. 5516

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Article

Environmental Science & Technology

His transformation rate constants measured under these pH conditions (Figure 2a and 2b). Alternatively, the concentration of sorbed His increased with decreasing pH from pH 7.1 to 6.0 and 5.1, suggesting a higher sorption affinity due to specific cation binding of the protonated His+ to negatively charged carboxylate (and phenolate) moieties in the SRNOM. Interestingly, decreasing the pH from 5.1 to 4.3 resulted in decreasing His sorption, which is consistent with a similar trend previously reported for the sorption of the positively charged sulfonamide antibiotic to humic acids.53 This decrease can be ascribed to increasing protonation of carboxylate groups in SRNOM with decreasing pH and hence a decrease in the number of negatively charged sites in SRNOM available for cationic binding of His+. This explanation was subsequently verified by modeling the pH-dependent binding of His+ while accounting for the pH-dependent concentration number of negatively charged moieties in SRNOM, as detailed below. The fitted Kb values of His+ to anionic sites (CDOM−) were determined based on eq 4. The binding constants were relatively stable at pH 4.3−6.0 (i.e., 2.6 ± 0.0 × 105 M−1 at pH 4.3, 2.5 ± 0.0 × 105 M−1 at pH 5.1, and 2.9 ± 0.1 × 105 M−1 at pH 6.0; SI Figure S5). Above pH 7.0, the sorption was too weak to fit Kb values with little His+ present in solutions. The fitted Kb value therefore suggests that there was no sorption between His0 and SRNOM, while His+ had an affinity to SRNOM due to ionic interaction. Sorption experiments for histamine were carried out only at pH 5.0 because histamine tended to sorb to the centrifugal membrane above pH 6.0. At pH 5.0, the fraction of sorbed histamine was slightly higher than the fraction for His (SI Figure S5), likely reflecting the higher positive net charge of histamine than His at this pH. The correspondence between sorption and photolysis experiments further supports that phototransformation rates of AAs in the presence of CDOM may be largely enhanced through association of the AAs with the CDOM. Quantitative Analysis of His Sorption to SRNOM and Transformation Rates. Following the analysis of His sorption and photochemical transformation, we sought to develop a quantitative model to integrate the effect of His sorption to SRNOM into predictions of the rates of His photochemical transformation. Utilizing the binding constant (averaged Kb = 2.7 ± 0.2 × 105 −1 M ) obtained above, a new predicted krxn curve was calculated that accounts for the partitioning of the neutral and cationic His in the system (i.e., freely dissolved His0 (f His), freely dissolved His+ ( f His+), and sorbed His+ (fHis+ − )) and the micro-

Figure 4. Ratio of measured singlet oxygen (1O2)-mediated reaction rate constants of His in SRNOM-containing solutions (microheterogeneous systems) over the prediction rate constants for homogeneous systems, kpred, as a function of added concentration of the sorptive competitor ((Me2Im)(MeSO3)). The photolysis experiments were conducted at pH 5.1. The ratios krxn/kpred obtained in SRNOM-sensitized photolysis (without (Me2Im)(MeSO3) or Na(MeSO3)) and lumichrome-sensitized photolysis experiments at pH 5.1 were also plotted for comparison (black dashed lines). Error bars represent the ranges of duplicates.

evidence for sorption to SRNOM was obtained from independent sorption experiments. Figure 5 shows the pH-

Figure 5. Sorption isotherms of His to SRNOM as a function of solution pH. Sorption is expressed as the concentration of sorbed His (μmol His per g carbon of SRNOM) versus the freely dissolved concentration of His in the filtered solutions (μM).

CDOM

heterogeneous distribution of 1O2. The sorption model is based on cation binding equilibrium of His+ to negatively charged moieties in SRNOM. As shown above, His0 sorption to SRNOM is small and can be neglected. The His+ reaction rate is known to be low (see above), such that we can assume that + + the contribution of kHis rxn f His is negligible and remove it from eq 9 to give eq 10.

dependent sorption isotherms of His to SRNOM, expressed as sorbed His versus the final measured free His concentration in solution as a function of pH. At pH 7.1 and 7.8, His did not sorb to SRNOM to any measurable extent and thus was excluded from Figure 5. The low His sorption at pH > 7.0 is consistent with the expectation of only weak interactions of the zwitterionic His (i.e., no net charge) with CDOM. Weak electrostatic binding might occur for the positively charged amine in zwitterionic His with SRNOM.52 Yet this electrostatic attraction was likely compensated by anion repulsion of the negatively charged carboxylate moiety from negatively charged groups in SRNOM. The absence of measurable sorption is consistent with the good agreement of measured and predicted

0

His k pred = k rxn fHis0 +

[1O2 ]CDOM 1

[ O2 ]aq

+

His k rxn fHis+

CDOM−

(10)

The sorption-enhanced phototransformation model was fit to the measured His krxn from microheterogeneous systems in Figure 2a. Accounting for the sorption of His+ to SRNOM into our model greatly improved the fit of the experimental data 5517

DOI: 10.1021/acs.est.5b00466 Environ. Sci. Technol. 2015, 49, 5511−5519

Article

Environmental Science & Technology (Figure 6). At the same time, the measured krxn was higher than the prediction between pH 5.0 and 6.0. At present, the reason

chemical transformation processes is currently being addressed in ongoing work.

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ASSOCIATED CONTENT

S Supporting Information *

Supporting figures, tables, detailed experimental methods, and the results of additional experiments described within the manuscript. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Authors

*Phone: +41 (0)44 6328314; fax: +41 (0)44 6331122; e-mail: [email protected]. *Phone: +41 (0)44 6324755; fax: +41 (0)44 6321438; e-mail: [email protected]. Figure 6. Quantitative prediction model for the experimental phototransformation rate constants of His, krxn, in microheterogeneous systems containing SRNOM as a function of solution pH (blue diamonds; identical to that in Figure 2a). The curve fits correspond to the predicted rate constants, kpred, based on a model that assumes a homogeneous distribution of singlet oxygen in the system (black line) and a model that accounts for the sorption of His to SRNOM as well as the microheterogeneous distribution of singlet oxygen in the system (red line).

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by a grant from the Swiss National Science Foundation (Project 200021_138008). REFERENCES

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