Kinetics and Mechanisms of Ciprofloxacin Oxidation on Hematite

Article pubs.acs.org/est

Kinetics and Mechanisms of Ciprofloxacin Oxidation on Hematite Surfaces Sébastien Martin,†,‡ Andrey Shchukarev,‡ Khalil Hanna,† and Jean-François Boily*,‡ †

Ecole Nationale Supérieure de Chimie de Rennes, UMR CNRS 6226, 11 Allée de Beaulieu, F-35708 Rennes Cedex 7, France Department of Chemistry, Umeå University, Umeå, SE-901 87, Sweden

‡

S Supporting Information *

ABSTRACT: Adsorption of antibiotics at mineral surfaces has been extensively studied over the past 20 years, yet much remains to be learned on their interfacial properties and transformation mechanisms. In this study, interactions of Ciprofloxacin (CIP), a fluoroquinolone antibiotic with two sets of synthetic nanosized hematite particles, with relatively smooth (H10, 10−20 nm in diameter) and roughened (H80, 80−90 nm in diameter) surfaces, were studied by means of liquid chromatography (LC), mass spectrometry (MS), and spectroscopy (vibration and X-ray photoelectron). Attenuated Total Reflectance Fourier Transform Infrared (ATR-FTIR) spectroscopy provides evidence for inner-sphere bidentate complex formation of CIP at hematite surfaces in 0.01 M NaCl, irrespective of pH and particle size. ATR-FTIR spectroscopy also revealed that the sorbed mother CIP molecule decayed to other surface species over a period of at least 65 h. This was supported by the detection of three daughter products in the aqueous phase by LC/MS. The appearance of NH3+ groups during the course of these experiments, revealed by cryogenic XPS, provides further evidence that CIP oxidation proceeds through an opening of piperazine ring via N-dealkylation. Additional in vacuo FTIR experiments under temperature-programmed desorption also showed that oxidation of sorbed byproducts were effectively degraded beyond 450 °C, a result denoting considerably strong (inter)molecular bonds of both mother and daughter products. This work also showed that rougher, possibly multidomainic particles (H80) generated slower rates of CIP decomposition but occurring through more complex schemes than at smoother particle surfaces (H10). This work thus uncovered key aspects of the binding of an important antibiotic at iron oxide surfaces, and therefore provided additional constraints to our growing understanding of the fate of emerging contaminants in the environment.

1. INTRODUCTION Fluoroquinolones (FQs) are broad-spectra antibiotics used in the treatment of tuberculosis in humans, and also widely used in veterinary medicine for treatment and prevention of infectious diseases.1 Of the various forms of FQsincluding ciprofloxacin (CIP), norfloxacin (NOR), enrofloxacin (ENR), and ofloxacin (OFL)CIP is one of the most widely used.2 As up to 75% of administered doses of antibiotics can be excreted through urine and faeces,2 FQs have been detected in surface and groundwater. For example, CIP has been detected in levels of several hundred ng per L in wastewater effluents and surface waters in Europe and the U.S.A.2−4 The fate and behavior of antibiotics in the environment are consequently a growing concern in current-day studies.5 Generally, sorption to solid surfaces and associated heterogeneous electron transfer (redox) reactions are major processes affecting the transport and fate of organic contaminants in the environment.6−10 Reactions involving iron oxides are of particular interest given the widespread occurrence and reactivity of these phases in nearsurface and groundwater systems11 and the impact they can exert on aquatic life.12 © XXXX American Chemical Society

While numerous studies have investigated interactions of FQs with metal oxides,8,9,13−17 very few have dealt with the surface speciation of FQs together with their chemical transformations at mineral surfaces. Liquid chromatography (LC) couple to mass spectrometry (MS) can be used to monitor desorbed soluble oxidation products.8,9 Oxidation can be initiated at the iron oxide/water interface by direct coordinative (inner-sphere) binding with surface ferric iron surface sites, via ligand exchange reactions involving Fe-bound hydroxo or aquo-groups.18−20 This coordination mode facilitates electron transfer processes between sorbed molecules and metal active sites,18−20 a time-dependent process that can span several hours.9 Molecular transformations of FQs at metal oxide surfaces, including complexation mechanism and oxidation schemes, have however been scarcely explored. Received: June 11, 2015 Revised: September 28, 2015 Accepted: September 29, 2015

A

DOI: 10.1021/acs.est.5b02851 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

Figure 1. Ciprofloxacin and oxidation byproducts of CIP (the M-X indicates the net mass loss or gain of the product from the parent CIP).

ments revealed no other surface contaminants than the commonly found hydrocarbons (285.0 eV of the C 1s region) and retrieved (O+OH)/Fe ratios close of 1.5, consistent with the expected O/Fe stoichiometric ratio of hematite. Transmission electron microscopy (TEM; Jeol JEM 1230 microscope) images (Figure S1 in the Supporting Information (SI)) revealed platy- to spheroid-type particles with diameters between 9 and 30 nm for H10 (mode = 13 nm, median = 15 nm, mean = 16 ± 5 nm), and between 30 and 90 nm for H80 (mode = 80 nm, median = 78 nm, mean = 74 ± 12 nm) (Figure S2). The specific surface area, measured (Tristar, Micromiretics) by a 90-point N2(g) adsorption/desorption isotherm on samples previous dried at 110 °C for 16 h under a stream of N2(g), are 67.8 m2/g for H10 and 39.3 m2/g for H80. The mean diameter (d) of spherical particles estimated from these B.E.T. values as (6/(ρd), where ρ is the hematite density, ρ = 5.24 × 106 g/m3) of H10 (16 nm) was highly comparable to that from TEM (mean =16 ± 5 nm), while the one for H80 (29 nm) was considerably lower (74 ± 12 nm) (Figures S1 and S2). This discrepancy could be explained by imperfections in H80 particles seen as large fissures by TEM (Figure S1). A Barrett−Joyner−Halenda (BJH) pore analysis of the N2(g) adsorption/desorption data also accordingly shows that the pore volume of H80 (0.8 cm3/g) is twice that of H10 (0.4 cm3/ g). These findings thus fall in line with the concept that iron (oxyhydr)oxide particles grown slowly (H10) exhibit less surface imperfections/roughness than those grown by instant addition of reagents (H80) where, in contrast, surfaces with high free energies are favored.27 The impact of these effects on mineral surface charge development was, moreover, demonstrated in several studies from our group.28−30 2.3. Batch Experiments and Chromatographic Analyses of Solutions. Suspensions of each hematite preparation in 0.01 M NaCl were reacted with 20, 100, 500, and 1000 μM CIP in polyethylene test tubes at pH 4.0, 5.5, and 7.0. Solution pH was adjusted by addition of standard solutions of HCl (0.1 N) and NaOH (0.1 N) in a CO2-free atmosphere by sparging with N2(g). The resulting suspensions were equilibrated for different time periods (1 and 65 h) and then centrifuged for 20 min at 4000 rpm. CIP concentrations in supernatants were then determined by a high performance liquid chromatography (HPLC) system with an auto sampler (Waters 717 plus), using a C18 column (250 × 4.6 mm2, with an internal diameter of 5 μm) and a UV detector operating at 275 nm (Waters 2489). The mobile phase was a mixture of water/acetonitrile (75:25 v/

In this study, we resolved molecular-level aspects of CIP adsorption and oxidation by hematite (α-Fe2O3) surfaces using Fourier Transformation Infrared (FTIR), LC/MS, and cryogenic X-ray photoelectron spectroscopy (XPS). Hematite was selected as a redox-active sorbent due to its great thermodynamic stability and abundance in soils and sediments.21 Reactions on two synthetic hematite particle types of distinct particle size and surface roughness were monitored in an effort to study the impact of environmentally induced variations in crystal growth conditions producing particles of possibly distinct reactivity.22−26 The findings presented in this study point to important changes in CIP oxidation states at hematite surfaces over the course of several hours via the opening of the piperazine ring (Figure 1) and to the concomitant release of daughter products and ferrous iron to the aqueous solution. Implications to these reaction mechanisms on the fate of FQs in natural waters are also discussed.

2. MATERIALS AND METHODS 2.1. Materials. All reagents were used without further purification. Ciprofloxacin (99% of purity) and FeCl3 6H2O (98%) were purchased from Sigma-Aldrich and used as received. All solutions were prepared with doubly distilled deionized water, and the ionic strength was adjusted to 0.01 M NaCl. 2.2. Hematite Synthesis and Characterization. Two types nanosized hematites (H10 and H80) were synthesized by forced hydrolysis of 2 L solutions containing 0.002 M HCl and 0.02 M FeCl3 6·H2O (10.8 g) at 98 °C. Particles were made by adding a stock solution of FeCl3 6·H2O to the preheated 0.002 M HCl solution. Addition was made dropwise for H10 over a 1 h period, and in one rash single addition for H80. The resulting solutions were kept at 98 °C for 2 weeks for H10 and 4 weeks for H80. The samples were thereafter dialyzed over a 1-week period with doubly distilled deionized water, during which time the dialysis water was changed on a daily basis, until the conductivity of the dialysis water matched that of doubly distilled deionized water. Electrophoretic mobility measurements (Zen3600, Malvern Instruments) of H10 and H80 suspensions revealed an isoelectric point of 9.5. A portion of the dialyzed suspension was oven-dried (80 °C) for additional particle characterization. Powder X-ray diffraction (D8, Bruker) confirmed that hematite was the sole crystallographic phase, while FTIR (Vertex v70, Bruker) measurements revealed no adventitious iron (oxy)hydroxides. XPS measureB


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Environmental Science & Technology v) containing 0.1% of formic acid. The flow rate of the mobile phase was set at 1 mL/min in isocratic mode. The byproducts were, in turn, analyzed with a Waters ultra HPLC-MS (Acquity UPLC) system using a Waters BEH C18 column (100 × 2.1 mm2, 1.7 μm). The mobile phase consisted of acetonitrile containing 0.1% of formic acid (eluant A) and mixture acetonitrile/water 10%/90% containing 0.1% of formic acid (eluant B) with gradient 0 min/0% A − 1 min/0% A − 9 min/ 100% A − 12 min/0% A and a flow rate equal to 400 μL/min. An electrospray ionization (ESI) was used for the MS measurements in positive ionization mode and full scan acquisition. Finally, dissolved Fe2+ was determined by UV− visible spectrophotometry (Cary 50 probe, Varian) using the 1−10 phenanthroline method.31 2.4. ATR-FTIR. The centrifuged wet pastes of hematite obtained from the batch experiments after 1 h equilibration time were analyzed by Attenuated Total Reflectance (ATR; Golden Gate, single bounce diamond, Specab) FTIR spectroscopy. Wet pastes were applied on the ATR cell under a vacuum-tight lid during which time spectra were collected every hour for H80 over a 65 h period and every 0.5 h for H10 over a 16 h period. A portion of the supernatant was also used to obtain a background for each sample. Spectra of the wet hematite pastes were then obtained by subtracting spectral contributions of the background from the raw spectra. All spectra were collected with a Bruker Vertex 70/V FTIR spectrometer, equipped with a DLaTGS detector in a room kept at 25 ± 1 °C. Measurements were carried out in the 600− 4500 cm−1 range at a resolution of 2.5 cm−1 and at forward/ reverse scanning rate of 10 Hz resulting in 1000 coadded spectra for each sample. The data were treated with a Blackman-Harris 3-term apodization function with 16 cm−1 phase resolution and the Mertz phase correction algorithm. In an additional effort to characterize reaction products, the thermal stabilities of mother and daughter species in the dry states were investigated by temperature-programmed desorption (TPD). These experiments were carried out on H80 samples equilibrated with CIP at pH 5.5 for 1 and 65 h. The centrifuged wet pastes were first dried onto a fine-tungsten mesh (Unique wire weaving, 0.002″ mesh diameter) under a stream of N2(g), then placed into a copper-heating shaft. The sample was thereafter heated at a constant rate of 10 °C min−1 from 30 to 500 °C in a reaction chamber (AABSPEC #2000A), equipped with KBr windows, under an operating pressure below 2.5 mTorr, the detection limit of the pressure sensor used for these measurements (MKS, Baratron). All spectra were collected and treated under the same conditions as the ATR-FTIR spectra, except that the spectra were collected in transmission mode, resolution was of 4.0 cm−1, and each spectrum was an average of 25 scans to enable a sufficiently rapid spectral acquisition under TPD. 2.5. FTIR Spectral Analyses. Spectra of hematite-bound CIP were first obtained by subtracting contributions from the supernatant, and notably those of the water bending modes. The resulting time-resolved ATR-FTIR spectra of the 1200− 1800 cm−1 region were then analyzed by multivariate curve resolution (MCR) analysis32 to identify spectral and normalized concentration profiles (as these FTIR measurements cannot be used to obtain absolute concentration values) of end-member spectral components representing the purest chemical species possible. Spectra sets were expressed in the matrix A (m rows of wavenumber and n columns of measurements), and offset to zero absorbance at 1800 cm−1, where absorption by the wet

hematite pastes is constant. The spectra were expressed in terms of a linear combination of spectral profiles (ε), akin to molar absorption coefficients, and their related normalized concentration profiles (C), and are related by A= εC as in the Beer−Lambert law. The number of chemically relevant linearly independent vectors accounting for the variance of A was estimated by singular value decomposition (SVD). Calculations of ε and C were made with the MCR-ALS program32 in the computational environment of MATLAB (The Mathworks, Inc.). This program executes a model-free analysis of the absorbance data by rotating SVD-derived left-singular (linearly independent) vectors into a real chemical space, such that ε ≥ 0 and C ≥ 0. No assumptions regarding the spectroscopic responses of the different species are made through this process. 2.6. Cryogenic XPS. Wet centrifuged hematite pastes that were reacted with CIP were analyzed for surface composition by cryogenic XPS. The samples were precooled using liquid nitrogen to preserve water in the sample under vacuum.33 This procedure involves precooling the end of the sample transfer rod (20 min at −170 °C) and then waiting 45 s after loading the wet paste before pumping the introducing chamber. After pumping to (4−5) × 10−5 Pa, the frozen paste was transferred to the precooled (−155 °C) manipulator where it was kept until a base vacuum of 2−4 × 10−7 Pa in the analysis chamber was reached. Wide (pass energy 160 eV) and narrow (pass energy 20 eV) spectra were acquired with a Kratos Axis Ultra DLD electron spectrometer using a monochromatic AlKα source operated at 150 W, hybrid lens system with magnetic lens, and charge neutralizer. At least two measurements were performed on each sample, and the data (atomic ratios) were reproducible within 15%. The binding energy (BE) scale was referenced to the C 1s line of aliphatic carbon, set at 285.0 eV. Processing of the spectra was accomplished with Kratos software and CasaXPS program package.

3. RESULTS AND DISCUSSION 3.1. Incipient CIP Loadings and Coordination Modes. CIP exists as cationic, zwitterionic, and anionic forms under circumneutral aqueous conditions, with pKa1= 5.46 and pKa2 = 7.67 (Figure S3).9 CIP binding at hematite surfaces at 1 h equilibration time was accordingly greatest under circumneutral pH where hematite surfaces are positively charged and CIP carboxylate groups deprotonated (Figure S3). Preliminary results (not shown) also revealed that 99% of the sorbed CIP was recovered by desorption at pH 11, and therefore no oxidation occurred at least within the first hour of equilibration. Unlike previous studies where the adsorption affinity was larger for smaller particle sizes,25,26 both H10 (67.8 m2/g) and H80 (39.3 m2/g) acquired comparable loadings of CIP, with values lying in the 0.2−6.7 μmol/m2 range (i.e., ∼0.1−4.0 molecules/ nm2) (Figure S4). These values are consistent with the typical reactive (e.g., singly coordinated OH group) density of ∼3−4 site/nm2 at hematite surfaces.34 However, we note that adsorption isotherms (at fixed pH) also reveal that adsorption maxima were attained at lower total loadings in H10 than in H80, namely where the former would follow more of a classical Langmuirian, while the latter a Langmuir−Freundlichian (or Sips) adsorption behavior. This could fall in line with the concept of kinetically inaccessible reactive site densities in H80 associated with its larger surface roughness discussed in Section 2.2 (Figure S1). C


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hematite surfaces. This was first confirmed by the appearance of various daughter species with m/z at 263, 306, 332, and 348 as measured by LC/MS (Figure S5), and through the production of ferrous iron (Figure S6). These data thus fall in line with the concept that CIP binding to hematite is followed by a heterogeneous electron transfer process resulting in the concomitant oxidation of CIP and reduction of surface-bound iron (≡FeIIIOH + CIP → ≡FeIIIOH − CIPad → ≡FeIIOH − CIP+•) and to the subsequent release of ferrous iron and of the daughter CIP products to the aqueous solution. Time-resolved ATR-FTIR spectra of hematite-bound CIP (Figure 4) provided further insight into these changes. The

ATR-FTIR spectra of sorbed CIP at pH 4.0, 5.5, and 7.0 (Figure 2) were generally invariant of pH, a result accordance

Figure 2. ATR-FTIR spectra for H10 and H80 reacted with CIP at pH 4.0−5.5−7.0 with an ionic strength of 0.01 M (NaCl) and 1 h of equilibration time. Total ligand loadings are 14.8 μmol/m2 for H10 and 25.5 μmol/m2 for H80. Figure 4. ATR-FTIR spectra of hematite reacted with CIP for H10 during 16 h and H80 for 65 h at pH 4.0−5.5−7.0 with an ionic strength of 0.01 M (NaCl); t = 0 corresponds to first spectrum recorded after 1 h of equilibration time. Total ligand loadings are 14.8 μmol/m2 for H10 and 25.5 μmol/m2 for H80.

with previous efforts toward CIP adsorption on magnetite.15 In all cases, the most significant spectral changes, in relation to the unbound CIP (aromatic ring stretch = 1485 cm−1; υCO ketone = 1628 cm−1; υCO carboxyl = 1710 cm−1; υCOOas = 1580 cm−1; υCOOs = 1360 cm−1; positions shown in Figure 1)14 lie in the disappearance of the COOH peak at 1710 cm−1 in relation to the unbound CIP species, indicating the involvement of carboxylic group in surface binding.13 The involvement of the keto CO group in binding can also be seen by a red-shift of the original 1628 cm−1 band of aqueous CIP to 1617 cm−1 upon adsorption. Furthermore, the original bands of unbound CIP at 1580 cm−1 (COO−as; asymmetric stretch) and at 1360 cm−1 (COO−s; symmetric stretch) were shifted to 1527 and 1385 cm−1, respectively, upon binding to hematite surfaces. This consequently suggests that CIP predominantly binds to as bidentate complexes, i.e., involving one oxygen atom of the carboxylic group and one oxygen atom of the carbonyl group (Figure 3). These observations are thus consistent with those of Gu and Karthikeyan13 and Trivedi and Vasudevan14 for CIP adsorption on other metal oxide surface, and also with aqueous complexes of CIP with dissolved Fe3+.35 3.2. CIP Breakdown at Hematite Surfaces. Reaction times exceeding 1 h lead to oxidative breakdown of CIP at

spectra reveal systematic changes in the aforementioned collection of bands in the 1200−1800 cm−1 region over several hours of reaction time. Modifications in the CIP molecule can be especially noted through variations in N-bond strengths of amine groups near 1600−1700 cm−1.36 Further changes taking place over the course of the reactions moreover point to the possibility that slower reaction mechanisms may occur rather than readsorption phenomena. In fact, soluble CIP oxidation byproducts (Figure S5) and ferrous iron (Figure S6) were still generated after 65 h of reaction time. MCR analyses of the time-resolved ATR-FTIR data provided a means to extract (linearly independent) spectral (ε) and relative concentration (C) profiles of the salient chemical components over the reaction times (cf. Section 2.5). This analysis provides evidence for the predominance of 2 spectral components for H10 and 3 components for H80, shown in Figure 5. Component MCRxa (where x = [1,3] corresponds to each of the three tested pH values for H10, and x = [4,6] for H80) corresponds to the spectrum of CIP adsorbed after 1 h reaction time, while MCRxb and MCRxc are the spectra of the new CIP-derived surface species. These new, time-dependent, spectral profiles, we note, result from the combined effects of (i) CIP breakdown to daughter molecules, (ii) possible changes in surface speciation of coexisting mother CIP molecules, and (iii) desorption of daughter CIP and ferrous iron to the aqueous solution. The normalized concentration profiles (C) obtained by MCR, as shown in Figure 6, provided further insight into the time-dependence of these changes. These profiles, factored in by the original CIP loading determined by batch adsorption experiments (molecule/nm2 in Figure 6), underscore the progressive replacement of MCRxa by MCRxb/xc over the

Figure 3. Structure of the CIP−hematite surface complex. D


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course of several hours. While H10 required only these two components, the rougher H80 particles necessitated the generation of a third component which is presumably generated upon the disappearance of MCRxb. We describe the decay of the mother CIP and formation of new species by using a pseudo-second order kinetic model. This order was chosen after an extensive search for best-fitting kinetic models accounting for these concentration profiles. Given the complexity of heterogeneous reactions, our model pertains to an apparent reaction order accounting for the disappearance of the mother compound through the following: −

d[CIP] = kdis[CIP]2 dt

(1)

We note that this model does not attempt to account for possibly diverse elementary steps associated with CIP breakdown. Linearization of the integrated form of eq 1 gives the following:

Figure 5. Spectral components of CIP and byproducts for H10 (A) and H80 (B). CIP total ligand loadings are 14.8 μmol/m2 for H10 and 25.5 μmol/m2 for H80; at pH 4.0, 5.5, and 7.0 with ionic strength of 0.01 M of NaCl. MCRxa corresponds to the spectrum of mother CIP sorbed. MCRxb and MCRxc are the spectra of the new surface species. x = [1,3] for H10 and x = [4,6] for H80. x = 1 or 4 (pH 4.0); x = 2 or 5 (pH 5.5); and x = 3 or 6 (pH 7.0).

1 1 − = 2kdist [CIP] [CIP]0

(2) 2

where [CIP]0 and [CIP] (molecule/nm ) are the initial amount and the amount of CIP decayed at any time t, respectively, and

Figure 6. Variation of surface amounts versus time (0−16 h for H10 and 0−65 h for H80) and pseudo-second order kinetic modeling fits (solid lines). Total ligand loadings are 14.8 μmol/m2 for H10 and 25.5 μmol/m2 for H80, at pH 4.0, 5.5, and 7.0 with ionic strength of 0.01 M of NaCl. E


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Environmental Science & Technology kdis (nm2/molecule/h) is the pseudo-second order rate constant of the CIP disappearance. The pseudo-second order equation for the formation of the new compound is written as follows: dP = k for(Pmax − Pt )2 dt

decreased from pH 4.0 to 7.0. We also note that rate constants (Figure 6) are substantially lower in H80 as it achieved higher CIP loadings and likely due from contributions associated with its rougher surface. 3.3. Thermal Stabilities of Interfacial Products. TPDFTIR experiments (in the 30−500 °C range) of dried mother and daughter CIP products sorbed at the hematite surface helped corroborate that the aforementioned spectral changes result from CIP oxidation at hematite surfaces, and not merely changes in surface speciation during the time-resolved collection of the room temperature ATR-FTIR spectra. Metal atom site-induced oxidation of organic compounds is generally considered as endothermic, and so an increase of temperature should certainly catalyze oxidation.37 The temperature resolved FTIR spectra (not shown) were treated by MCR analysis, and produced three spectral MCR components and (normalized) concentration profiles (Figure 8). The model highlights the temperature dependence of the low-temperature sorbed species (MCRxα), in relation to the appearance of its thermal decomposition products (MCRxb and MCRxc where x = [7, 8] corresponds to the equilibration time, i.e., 7 to 1 h and 8 to 65 h). More specifically, the original bands of the sorbed species, which are highly comparable to their hydrated counterparts (Figure 2), are replaced by new band sets corresponding to their thermal decomposition products. The model also points to the nearly complete disappearance of the three spectral components corresponded at 450 °C, a result pointing to the full oxidation of ciprofloxacin and its byproducts. In these experiments, the thermal degradation behaves differently for samples analyzed immediately after sorption equilibrium (i.e., 1 h), compared to those undergoing a preliminary room temperature-oxidation on ATR crystal for 65 h. It should be noted that the mother molecule had fully disappeared after 65 h of reaction time and before starting TPD experiments, while the sample analyzed just after 1 h of equilibration time contained only the sorbed mother molecule. Interestingly, component MCR 8α (65 h) decreased in importance more rapidly beyond 100 °C compared to MCR 7α (1 h), a result suggesting that the thermal oxidation of “ciprofloxacin byproducts” was higher than that of the mother molecule. Daughter compounds may consequently be more favorable for thermal degradation, thus adding further

(3)

where Pmax is the maximum amount of new product formed (molecule/nm2), Pt is the amount of product formed at time t, and kfor (nm2/molecule/h) is the pseudo-second-order rate constant of the new product. Again, linearization of the integrated form of eq 3 gives the following: t 1 1 = + t Pt Pmax k forPmax 2 (4) to describe the appearance of the new compounds. We note that only the second formed species (MCRxc) in H80 was subject for kinetic modeling. The pseudo-second order rate constants of the CIP disappearance and formation of new species were calculated from linear regressions of eq 2 and 4 (regression coefficients higher than 0.95) at three pH values, and shown in Figure 6. While no significant impact of pH was observed on the formation rate constants of H80, the rate constant for disappearance is larger at pH 4.0 than at pH 5.5 and 7.0 Figure 7. In contrast, only the formation constants of H10

Figure 7. pH-Variation of the pseudo-second order rate constants of CIP disappearance kdis (nm2/molecule/h). This rate constant refers to the disappearance of component MCRxa, and of the formation of one byproduct kfor (nm2/molecule/h), referring to the formation of component MCRxb for H10 and MCRxc for H80.

Figure 8. MCR analysis of TPD-FTIR spectra and profile of component of H80 samples equilibrated to 1 h (A) and 65 h (B) with CIP. Samples were prepared from 1 g/L hematite suspension and CIP 1 mM at pH 5.5 in 0.01 M NaCl, then dried under N2(g) for TPD experiments. In MCRx, x = [7, 8] corresponds to the equilibration time, i.e., 7 to 1 h and 8 to 65 h. F


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Environmental Science & Technology independent support to the concept that the CIP has indeed been transformed on hematite surfaces during the timeresolved collection of the room temperature ATR-FTIR spectra. 3.4. Heterogeneous CIP Oxidation Mechanisms. As previously reported for the FeIII-induced oxidation of organic molecules,19,20 CIP can be oxidized by hematite through electron transfer from the N atom of piperazine ring to surfaceFe3+ generating a surface-bound FeII and CIP cation radical (R1). The formed radicals can then undergo further changes through C-hydroxylation and/or N-dealkylation, causing ring opening and subsequent formation of several byproducts,8,9 such as those detected by LC/MS (Figure S5). This sequential oxidation pathway corroborates with the time-dependence of the ATR-FTIR spectroscopy results. More specifically, the Ndealkylation pathway of the CIP piperazine ring, as highlighted in Figure 1, must have occurred under our experimental conditions, as two byproducts corresponding to m/z 306 (M26) (CIPox1 in R2) and m/z 263 (M-69) (CIPox2 in R3) were detected by LC/MS over 65 h reaction time (Figure S5):

Table 1. Atomic Ratios (Relative Error of 10%) Derived by XPSa pH 4.0

(R1)

>Fe IIOH − CIP+• → >Fe IIOH + CIPox1 + C2H6

(R2)

III

99:1 162:1

pH 7.0

N:F

Fe:NH3+

N:F

Fe:NH3+

N:F

3.5:1 3.2:1

57:1 56:1

3.0:1 3.2:1

79:1 12:1

3.9:1 3.3:1

This contrasts with H10 where variations in these ratios are not as pronounced and, according to our kinetic model, associated with faster rates of decomposition. Finally, we note that all N:F atomic ratios determined in this work (Table 1) were not considerably affected by our experimental conditions. Additionally, as amide (NCO) products were not detected by XPS, to piperazine ring N-dealkylation mechanism and of the concomitant appearance of NH3+ groups should be the preferential pathway through which CIP decomposes at the hematite surface.

4. ENVIRONMENTAL IMPLICATIONS FOR HETEROGENEOUS OXIDATION MECHANISMS Our work demonstrated that CIP, a widely used antibiotic, binds to hematite surfaces through inner-sphere bidentate complex, independently of pH and particle size. Rougher, possibly multidomainic, particles (H80) generate slower but more complex surface speciation and CIP decomposition schemes than smoother particle surfaces (H10). Redox reaction taking place over the reaction time of 65 h generated several soluble CIP byproducts and ferrous ion. The main oxidation pathway of CIP, i.e., N-dealkylation of the piperazine ring and appearance of NH3+ groups was confirmed (Figure 1). It is important to stress that the active functional groups of CIP serving as ligand to metal centers (i.e., carboxylic and ketone groups) remained unaltered during the oxidation on hematite surfaces. In contrast to the proposed pathway reported for the degradation of CIP in river water,42 no significant defluorination of CIP molecule was observed, suggesting that other natural factors may be responsible of the loss of F. Collectively, these results should have strong implications for the understanding of the transformation of emerging contaminants induced by minerals, and therefore their fate in the environment.

II

>Fe OH − CIPox1 → >Fe OH + CIPox2 + CH3CH 2NH3

H10 H80

pH 5.5

a Atomic ratios of Fe:NH3+ and N:F (N:F of CIP reference powder = 3.1:1) were obtained from fast-frozen wet pastes that were originally equilibrated for 16 h for H10 and 65 h for H80. Total CIP loadings are 14.8 μmol/m2 for H10 and 25.5 μmol/m2 for H80.

>Fe IIIOH + CIP → >Fe IIIOH − CIPad → >Fe IIOH − CIP+•

hematite

Fe:NH3+

(R3)

One more byproduct corresponding to m/z of 348 (M+16) or N-oxide analogue of CIP was also detected, suggesting that CIP can also be oxidized through O addition on N atom. In addition, low levels of dissolved ferrous iron were detected (Figure S6), which may be rapidly readsorbed by hematite following by interfacial electron transfer with structural Fe(III) in hematite.38 Recently, Frierdich et al.39 showed structural Fe(III) atoms of hematite exchanged with Fe(II) in solution, but this process remains very slow (>30 days). In order to confirm the surface oxidation pathway, we conducted cryogenic XPS measurements of H10 and H80 reacted with CIP at three pH values (4.0, 5.5, and 7.0). These measurements revealed three distinct chemical states of N (Figure S8 for H10 at pH5.5) with peaks at 400.1 eV (Naromatic), 401.3 (NH2+) and 402.6 eV (NH3+, protonated amine group). Note that the resilience of NH3 to protonation under circumneutral to acidic conditions can be understood through previous accounts pointing to important shifts in the pKa of such interfacially bound N-species.40,41 Furthermore, inspection of N 1s spectra of a fast-frozen aqueous solution of CIP, in relation to these results confirms further the changes undergone in the nitrogen functionality of hematite-bound CIP (Figure S8). Indeed, while ciprofloxacin has no NH3+ group in its nonoxidized form, only an opening of piperazine ring through N-dealkylation could have caused the appearance of NH3+ groups (Figure 1). It should be noted that the atomic ratio of Fe to protonated amine group NH3+ was dependent on pH and particle size (Table 1). A lower Fe:NH3+ ratio (i.e., relatively more NH3+) may suggest more oxidation (i.e., opening of piperazine ring), but the data reported in Table 1 does not permit to form a general conclusion. Still, as the lowest ratios for H80 were at pH 7.0 and the highest ratios at pH 4.0 different oxidation behaviors must predominate on these rougher H80 particles.

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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.est.5b02851. Additional results for the adsorption and oxidation of CIP with hematites (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: +46 90 786 5290; e-mail: jean-francois.boily@chem. umu.se (J.-F.B.). Notes

The authors declare no competing financial interest. G


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ACKNOWLEDGMENTS This work was supported by the Swedish Research Council (VR 2012-2976) and by the Kempe Foundation to J.-F.B. The authors thank Dr. M. Pasturel (XRD), Dr. S. Giraudet (BET), and Dr. V. Dorcet (TEM) for their assistance.

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Kinetics and Mechanisms of Ciprofloxacin Oxidation on Hematite

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