Adsorption of Tetracycline and Sulfamethoxazole on Crop Residue

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Adsorption of Tetracycline and Sulfamethoxazole on Crop Residue-Derived Ashes: Implication for the Relative Importance of Black Carbon to Soil Sorption Liangliang Ji,†,‡ Yuqiu Wan,† Shourong Zheng,† and Dongqiang Zhu†,* †

State Key Laboratory of Pollution Control and Resource Reuse and School of the Environment, Nanjing University, Jiangsu 210093, China ‡ Key Laboratory of Integrated Regulation and Resource Development on Shallow Lakes, Ministry of Education and College of Environmental Science and Engineering, Hohai University, Nanjing, 210098, China

bS Supporting Information ABSTRACT: The main objective of this study was to investigate the key factors and mechanisms of antibiotic adsorption on crop residue-derived black carbon, as well as the relative importance of black carbon to the overall sorption to soil. Batch sorption experiments were performed for two reference antibiotics (sulfamethoxazole and tetracycline) on wheat- and maize-residue-derived black carbon. After removal of the mineral fraction from the raw black carbon by acidification, tetracycline exhibited less enhanced adsorption than sulfamethoxazole, implying stronger complexation of tetracycline on the mineral components. The antibiotic adsorption on the demineralized black carbon was very strong (The measured Kd was in the order of 103
105 L/kg). The adsorbent surface area-normalized adsorption of sulfamethoxazole was higher on the demineralized black carbon than on nonporous graphite due to the micropore-filling effect. The opposite trend observed for bulky tetracycline was attributed to the size-exclusion effect. Owing to the strong surface complexation and/or cation exchange reaction, sorption of tetracycline to Naþ-exchanged montmorillonite, soil humic acids, and bulk soil was remarkably stronger than sulfamethoxazole. It was estimated that the contribution of black carbon to the overall sorption to bulk soil was important for sulfamethoxazole, but negligible for tetracycline.

’ INTRODUCTION Pharmaceutical antibiotics including tetracyclines and sulfonamides are produced in large quantities and extensively used in the farming industry as veterinary therapeutics and growth promoters.1 The antibiotics given to livestock are often poorly metabolized and absorbed, and a considerable fraction is consequently released into the environment.2,3 For example, survey studies reported that tetracycline concentrations in surface soil receiving liquid manure are up to 86.2 μg/kg on average.4 Antibiotic residues in the soil and aquatic environments have raised great concerns over the antibiotic resistance propagation in microorganisms.5
7 Sorption to soil is a fundamental process controlling the fate, bioavailability, exposure, and reactivity of organic contaminants. Thus, it is of great importance to evaluate the relative importance of different soil components to the overall sorption of pharmaceutical antibiotics. Black carbon refers to the carbonaceous materials generated from incomplete combustion of fossil fuel and biomass and is commonly present in natural soils.8,9 Recently, “biochar” intentionally made by biomass pyrolysis has received increasing attention as a possible soil amendment to increase fertility and sequester carbon, as well as a potential low-cost adsorbent to r 2011 American Chemical Society

control pollutant migration.10 Black carbon (biochar) can be considered structurally similar to activated carbon, consisting primarily of short stacks of graphite sheets with O-containing groups rimmed on the edge to form connected microporous networks. Owing to the large specific surface area and high surface hydrophobicity, black carbon often shows extraordinarily strong adsorption affinity for hydrophobic organic contaminants.11
13 It is well recognized that carbonaceous geosorbents (black carbon, humin/kerogen, and coal) play a key role in soil/sediment sorption of nonpolar hydrophobic organic compounds such as polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), and chlorinated benzenes, in particular at low solute concentrations (ref 14 and references therein). However, studies on adsorption of polar and ionic compounds on environmental black carbon are very limited in literature, and have mainly involved pesticides.15
18 Received: February 11, 2011 Accepted: May 24, 2011 Revised: May 18, 2011 Published: June 08, 2011 5580

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Environmental Science & Technology Despite the potential importance, unexpectedly no adequate attention has been paid to adsorption of pharmaceutical antibiotics on environmental black carbon.19 Studies on antibiotic sorption by natural geosorbents have focused on soils, iron/aluminum hydroxides, clay minerals, and humic substances.3,20
27 It was proposed that the multiple ionic/polar groups (phenol, amine, and alcohol) contained in antibiotic molecules may interact strongly with the corresponding structural components of the sorbents through ion exchange, ion bridging, and/or H-bonding. Thus, it seems reasonable to hypothesize that the functional groups in antibiotic molecules may also strongly complex with the hydroxyl groups of inorganic components (silicates and other minerals) associated with black carbon, and possibly the O-containing groups of the black carbon as well. Furthermore, environmental black carbon is known to be highly microporous.13,14 Dependent on the size and geometry of sorbate molecules, pronounced pore effect (micropore filling and size exclusion) might be induced when antibiotics sorb to black carbon. However, thus far no relevant studies have been performed to test the above-mentioned hypotheses. In this study, the batch technique was explored to investigate the adsorption properties of two heavily used antibiotics, tetracycline and sulfamethoxazole, to wheat and maize burn residues that represent soil back carbon. Crop residue burning is routinely practiced in land use in many agricultural regions in China and other countries, and provides an important way to deliver tremendous black carbon into the field soil. Effects of dissolved soil humic acids on the antibiotic adsorption were also examined. Presence of dissolved humic substances might significantly impact antibiotic adsorption via direct competitive adsorption for surface sites and/or blockage of the micropores of carbonaceous adsorbents.28
30 The relative importance of black carbon in the overall sorption of the two antibiotics to bulk soil was then estimated by comparing the sorption data between black carbon, soil, and other soil components (clays and humic acids).

’ EXPERIMENTAL SECTION Materials. The two antibiotic sorbates were sulfamethoxazole (99%, Sigma) and tetracycline (99%, hydrate, International Laboratory). Selected physicochemical properties of sorbates are summarized in Supporting Information (SI), Table S1. Their chemical structures and molecular sizes are given in SI, Figure S1. A Stagnic Anthrosol was collected from the surface horizon (0
20 cm) from Suzhou, Jiangsu Province in east China. Humic acids were extracted from the soil with NaOH according to the standard procedure.31 The content of clay fraction (14.3%, volume based in whole soil), organic carbon (1.96%, dry weight based), and black carbon (0.34%, dry weight based; quantified using the 375 °C combustion method), as well as the cation exchange capacity (CEC) (23.0 cmol/kg) of the soil, and detailed structural characterization of the extracted soil humic acids were reported in our previous studies.32,33 A domestic montmorillonite (Fenghong Inc., Zhejiang Province, China) was used to prepare Naþ-saturated clay fraction by cation exchange. On the basis of the information provided by the manufacturer, the CEC of the montmorillonite is 110 cmol/kg. Wheat straw and maize stalk were collected from the croplands of Shenyang, Liaoning Province and Suzhou, Jiangsu Province, respectively, in China. The air-dried wheat straw and maize stalk were burned in the air on a stainless steel plate (1  1 m) in an open field under natural conditions. The obtained ash content was divided into two portions. One portion was thoroughly rinsed with deionized

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water six times to remove excess soluble salts. The other portion was treated with a mixture of 1 M HCl and 1 M HF to intentionally eliminate all inorganic components and then rinsed with deionized water until a negative chloride testing by AgNO3. The resulting black carbon samples were oven-dried (110 °C) and stored in a desiccator for later use. After the demineralization treatment, the remaining content (black carbon) accounts for 19.7 ( 0.7% (standard deviation calculated from triplicate samples) of the raw wheat ash and 7.8 ( 0.3% of the raw maize ash. The raw and acid-treated wheat- and maize-residue-derived black carbon is referred to as wBCraw, wBCacid, mBCraw, and mBCacid, respectively. Characterization of Sorbents. Surface elemental composition of the crop residue-derived black carbon was quantified using an X-ray photoelectron spectrometer (XPS) (PerkinElmer PHI 550 ESCA/SAM), and content of inorganic components was determined by an X-ray fluorometer (XRF) (ARL9800, Switzerland). Transmission electron microscopy (TEM) images of the crop residue-derived black carbon were collected on a JEM-200 CX (JEOL, Japan). The crop residue-derived black carbon was also characterized by N2 adsorption/desorption, Zeta potential (ζ) analysis, and Raman spectra in the same manner as for our previous studies.34,35 Batch Sorption Experiments. A total of seven sorbents including wBCraw, wBCacid, mBCraw, mBCacid, bulk soil, Naþ-montmorillonite, and solid soil humic acids were used. Sorption isotherms were run with duplicate points (eight concentrations) for the two antibiotics to all sorbents except for humic acids, which were measured at a single concentration with six replicate samples. To initiate the experiments, a 40 mL amber glass vial equipped with polytetrafluoroethylene-lined screw cap received a weighed amount of sorbent, followed by stock solution of sorbate (prepared in water for tetracycline and in methanol for sulfamethoxazole) and a full volume of background solution (0.02 M NaCl). An operational background solution containing additional dissolved soil humic acids (50 mg/L) was also used, as needed. If methanol was used, its volume percentage was kept below 0.1% to minimize possible cosolvent effects on sorption. Single-concentration adsorption of the dissolved humic acids on wBCraw and mBCraw was measured separately with five replicate samples using a total organic carbon (TOC) analyzer (TOC 5000A, Shimadzu, Japan). The pH of the background solution was preadjusted with NaOH or HCl by considering the acid/basebuffering ability of the sorbent to ensure the desirable pH (5.0) at sorption equilibrium, as measured at the end of batch experiments. The samples were covered with aluminum foil and mixed endover-end at room temperature for 3 days to reach apparent sorption equilibrium (no further uptake) based on predetermined adsorption kinetics (results presented in SI, Figure S2). After centrifugation, solute was analyzed directly by highperformance liquid chromatography (HPLC) with an ultraviolet (UV) detector using a 4.6  150 mm SB-C18 column (Agilent). Isocratic elution was performed under the following conditions: 0.05 M phosphoric acid
acetonitrile (83:17, v:v) with a wavelength of 265 nm for sulfamethoxazole; 0.01 M oxalic acid
acetonitrile
methanol (80:16:4, v:v:v) with a wavelength of 360 nm for tetracycline. The detection and quantification limits are 0.32 mg/L and 1.08 mg/L for sulfamethoxazole,36 and 0.5 mg/L and 1 mg/L for tetracycline.22 To take account for possible solute loss from processes other than sorbent sorption (sorption to glassware and septum), calibration curves were obtained separately from controls receiving the same treatment as the 5581

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Table 1. Surface Elemental Composition, Surface Area, and Pore Volume Parameters for Raw and Acid-treated Wheat-ResidueDerived Black Carbon (wBCraw and wBCacid) and Maize-Residue-Derived Black Carbon (mBCraw and mBCacid) surface elemental compositiona surface areab (m2/g)

Vmicc(cm3/g)

Vmesd(cm3/g)

Vte (cm3/g)

Vmic/Vt

adsorbent

C%

O%

Si%

wBCraw

36.01

46.63

10.25

45

0.02

0.03

0.05

0.40

wBCacid

86.24

12.60

BDLf

464

0.23

0.28

0.51

0.45

mBCraw mBCacid

43.21 66.61

39.91 26.89

5.89 3.21

148 286

0.06 0.12

0.26 0.14

0.32 0.26

0.19 0.46

a

Determined by X-ray photoelectron spectroscopy (XPS). b Determined by N2 adsorption using the Brunauer
Emmett
Teller (BET) method. Micropore volume, calculated using the Horvath
Kawazoe method. d Mesopore volume, calculated by Vt
Vmicro. e Total pore volume, determined at P/P0 = 0.99. f Below detectable level. c

Figure 1. Adsorption isotherms plotted as adsorbed concentration (q, on unit mass basis) vs aqueous-phase concentration (Ce) at equilibrium for raw and acid-treated maize-residue-derived black carbon (mBCraw and mBCacid) and wheat-residue-derived black carbon (wBCraw and wBCacid). (a) Sulfamethoxazole. (b) Tetracycline. O = mBCraw; 0 = wBCraw; b = mBCacid; 9 = wBCacid. The lines represent the calculated Freundlich model fitting curves to adsorption data for the acid-treated black carbon fractionalized according to the black carbon content in the raw ash (solid line for wBCacid; dotted line for mBCacid).

sorption samples but no sorbent. Calibration curves included at least 14 standards over the tested concentration range. Based on the obtained calibration curves, the sorbed mass of solute was calculated by subtracting mass in the aqueous phase from mass added. It is noteworthy that no peaks were detected in the HPLC spectra for potential degraded/transformed products of the examined antibiotics.

’ RESULTS AND DISCUSSION Characterization of Adsorbents. Surface elemental compositions (C, O, Si), specific surface areas, and pore volume parameters of the crop residue-derived black carbon are presented in Table 1. Surface compositions of other elements are shown in SI, Table S2. The surfaces of wBCacid and mBCacid are dominated by graphitized carbon (more significant for wBCacid) and contain moderate content of O-containing groups (more significant for mBCacid). The respective untreated crop residuederived black carbon has larger content of Si and O, but lower content of C, suggesting the occurrence of silicates and other mineral oxides. The results are in line with the mineral compositions determined by XRF (results presented in SI, Table S3). Notably, under the tested pH (5.0) the silicate minerals are deemed insoluble. The TEM images (SI, Figure S3) also reflect that wBCraw and mBCraw have substantial mineral content. Additionally, the TEM images show that the carbon in wBCraw is powder-like, but in mBCraw fiber-like; meanwhile, the surface of wBCacid is coarser than the surface of mBCacid. Note that even with the demineralization treatment, high silicate content (13.4%

by XRF) is still conserved in mBCacid, probably because it is preserved in the inner pores of carbon fibers. The demineralization treatment markedly increases the specific surface areas and micropore volumes of the crop residuederived black carbon, in particular for the wheat ash (see Table 1). As shown from the ζ-pH relationships (SI, Figure S4), the surfaces of all crop residue-derived black carbon are negatively charged at the tested pH conditions (5.0 ( 0.2). Compared with wBCraw, the surface of mBCraw is much less negatively charged, likely resulting from the fairly high content of MgO (6.0% by XRF) that expectedly has high point of zero change (PZC). Results of Raman spectra (SI, Figure S5) verify that the demineralized black carbon is dominated by the graphitized carbon, but the structural order is much lower than pure graphite. Adorption Isotherms. Adsorption isotherms of sulfamethoxazole and tetracycline to raw and acid-treated crop residuederived black carbon are presented in Figure 1. The adsorption data are fitted to the Freundlich model, q = KFCen, by nonlinear regression (weighed on 1/q), where q (mmol/kg) and Ce (mmol/L) are the adsorbed concentration and aqueous-phase concentration, respectively, at adsorption equilibrium; KF (mmol1
n Ln/kg) is the Freundlich affinity coefficient; n (unitless) is the Freundlich linearity index. The fitting parameters are summarized in SI, Table S4. The Freundlich model fits all adsorption data reasonably (R2 > 0.95). It is evident from Figure 1 that sulfamethoxazole and tetracycline show different adsorption patterns. In general, the adsorption affinity can be ordered as follows: wBCacid > mBCacid > wBCraw > (sulfamethoxazole) = (tetracycline) mBCraw. The demineralization treatment removes most of the mineral components 5582

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Figure 2. Adsorption isotherms plotted as adsorbed concentration (q, on unit surface area basis) vs aqueous-phase concentration (Ce) at equilibrium for acid-treated maize- and wheat-residue-derived black carbon (mBCacid and wBCacid) and nonporous graphite. (a) Sulfamethoxazole. (b) Tetracycline. O = mBCacid; 0 = wBCacid; b = graphite.

(mainly silicates), and thus may create additional sites on the carbon surfaces to facilitate adsorption; however, this adsorption enhancement would be somewhat counteracted by the lowered contribution of the mineral components. In order to estimate the relative importance of the adsorption of black carbon, the adsorption data for the acid-treated black carbon are fractionalized according to the black carbon content in the raw ash (multiplied by 19.7% for wBCacid and by 7.8% for mBCacid), and the respective Freundlich fitting curves are also presented in Figure 1 for comparison. Note that the black carbon in the raw ash can only have equal or lower number of accessible adsorption sites than the same amount of demineralized black carbon. Thus, the fractionalized adsorption of the acid-treated black carbon serves as an upper bound for the adsorption of black carbon in the raw ash. For sulfamethoxazole, the fractionalized isotherms are displaced slightly below the measured isotherms, with differences less than 30% for the wheat-residue-derived black carbon, and less than 37% for the maize-residue-derived black carbon. Similar trends are observed for tetracycline, but to a larger extent, in particular for the maize-residue-derived black carbon. The differences between the measured and fractionalized isotherms stand for the minimum adsorption contribution of the mineral fraction. The more significant mineral contribution shown for mBCraw than for wBCraw may be possibly explained by the larger specific surface area of the mineral components in mBCraw (136 m2/g, estimated by subtracting the weighed surface area of mBCacid from the surface area of mBCraw). The more significant mineral contribution shown for tetracycline adsorption than for sulfamethoxazole adsorption is due to stronger surface complexation of tetracycline on the mineral components. It is well documented in literature that tetracyclines can strongly adsorb on the surfaces of iron/aluminum hydroxides and clay minerals via surface complexation (such as H-bonding) and/or ion exchange reaction.3,21
23 For example, the solid-to-solution distribution coefficient (Kd) for tetracycline adsorption on phyllosilicate minerals is up to 103 L/kg.3,23 However, the respective Kd values reported for sulfonamide antibiotics are generally within the order of 102 L/kg.20,24,27 Within the examined concentration ranges, the measured Kd values for adsorption on wBCacid and mBCacid are in the order of 104
105 L/kg and 103
104 L/kg for sulfamethoxazole, and 104
105 L/kg and 104 L/kg for tetracycline, respectively. Nonetheless, the comparison between the measured and fractionalized isotherms (differences in adsorption larger than 78% for the maize-residue-derived black carbon) is sufficient to prove that tetracycline adsorption on mBCraw is dominated by the mineral fraction (>90% over the

examined concentration range), while the black carbon plays only a minor role. It is further seen that removal of the mineral fraction from the crop residue-derived black carbon consistently increases the nonlinearity of antibiotic adsorption (stronger trends observed for tetracycline), as reflected by the decreased Freundlich n values (see SI, Table S4). To take tetracycline adsorption on the maize-residue-derived black carbon as an example, the Freundlich n value is reduced from 0.55 to 0.25 by removal of the mineral fraction. Removal of the mineral components may enhance the accessibility of certain adsorption sites on the black carbon and thus give rise to a more heterogeneous distribution of adsorption sites; as a result, more nonlinear adsorption is induced (Note on the basis of unit mass the black carbon overwhelms the mineral components with respect to both adsorption affinity and site heterogeneity). Effect of Black Carbon Porosity. As indicated by the pore size distribution analysis, the demineralized black carbon is highly microporous. The micropore volume accounts for 45% and 46% of the total pore volume of wBCacid and mBCacid, respectively (see Table 1). Correspondingly, the two examined antibiotics vary significantly in molecular size, and thus may exhibit sizedependent adsorption on the black carbon, as regulated by adsorbent porosity. To test this hypothesis, the adsorbent surface area-normalized adsorption isotherms of sulfamethoxazole and tetracycline are compared between wBCacid, mBCacid, and nonporous graphite (Adsorption data for graphite are adopted from ref 35) (results presented in Figure 2). For sulfamethoxazole, the normalized adsorption is higher on the black carbon than on nonporous graphite at low solute concentrations; however, the trend is reversed for tetracycline. The enhanced normalized adsorption of sulfamethoxazole on the black carbon likely results from the micropore-filling effect due to the low molecular size of adsorbate. Compared with tetracycline, sulfamethoxazole is a much narrower molecule (0.47 nm versus 0.81 nm, see SI, Figure S1). A similar mechanism was used in previous studies to explain the enhanced adsorption of low-sized adsorbate molecules (naphthalene and low-substituted monoaromatics) on commercial microporous activated carbon and wood-made black carbon (charcoal).13,35 Pronounced micropore-filling effect would occur at low solute concentrations because the high-energy small pores are preferentially occupied by low-sized adsorbates. On the other hand, the lowered adsorption of bulky tetracycline on the black carbon is probably due to size-exclusion effect. The size-exclusion effect was also proposed earlier as the mechanism for the impeded adsorption of 5583

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Figure 3. Adsorption isotherms plotted as adsorbed concentration (q, on unit mass basis) vs aqueous-phase concentration (Ce) at equilibrium for raw wheat-residue-derived black carbon (wBCraw) and raw maize-residue-derived black carbon (mBCraw) with and without presence of dissolved soil humic acids (DSHA, initially at 50 mg/L). (a) Sulfamethoxazole. (b) Tetracycline. O = mBCraw; 0 = wBCraw; b = mBCraw/DSHA; 9 = wBCraw/DSHA.

bulky adsorbate molecules (tetracycline and tetrasubstituted monoaromatics) on highly microporous carbonaceous adsorbents.13,35 It should be emphasized that many antibiotics are bulky molecules and expectedly induce marked size-exclusion effect when adsorbing on environmental black carbon. For both sulfamethoxazole and tetracycline, the adsorbent surface area-normalized adsorption is slightly lower on mBCacid than on wBCacid. Notably, the surface oxygen content of mBCacid is approximately twice as that of wBCacid (see Table 1). The higher surface oxygen content facilitates formation of larger and denser water molecule clusters around the oxygen groups, and in turn leads to stronger competitive adsorption for surface area on the graphitized carbon of adsorbents.37 However, the antibiotic adsorption on the black carbon examined in this study should still be dominated by the graphitized carbon. This is evidenced by the fact that the disparities in surface area-normalized adsorption between mBCacid and wBCacid are still relatively small, in spite of the very large difference in surface oxygen content between the two adsorbents. Our recent studies 34,35 indicate that the strong adsorption of sulfonamide and tetracycline antibiotics on synthetic carbon nanotubes and ordered micro- and mesoporous carbons is mainly driven by a combination of nonspecific van der Waals forces and specific π
π electron-donor
acceptor (EDA) interaction with the graphite surfaces. The ketone group or sulfonamide group in these antibiotic molecules has strong electronwithdrawing ability; therefore, the associated π-structures become electron deficient and thus act as π-electron-acceptors to interact strongly with the polarized π-electron-rich graphite surfaces (π-electron-donors) of carbonaceous adsorbents. Tetracycline and sulfonamide molecules would likely interact with the graphite surfaces of black carbon in similar fashion and therefore show strong adsorption affinity. Effect of Dissolved Soil Humic Acids (DSHA). The effect of DSHA on the antibiotic adsorption on the raw black carbon is displayed in Figure 3. In the presence of DSHA (50 mg/L), adsorption of sulfamethoxazole decreases more than one-third; however, adsorption of tetracycline stays nearly constant. The adsorption suppression caused by DSHA on sulfamethoxazole can be explained by direct competition for adsorption surface area on the black carbon (Note humic acids obviously have larger molecular sizes than sulfamethoxazole). Relatively strong adsorption of DSHA is shown on the raw black carbon. The measured Kd values from single-concentration adsorption of DSHA is 420 ( 20 L/kg (standard deviation calculated from four replicate samples) for wBCraw and 260 ( 40 L/kg for

mBCraw. Consistently, the suppressive effects of humic substances on adsorption of organic compounds on carbonaceous adsorbents were found to correlate negatively with adsorbent microporosity, but positively with adsorbate molecular size.28
30 Large humic molecules could be blocked from entering small micropores of adsorbents to access the adsorption sites. Likewise, in the same amount of adsorbed humic substances less adsorption space would be accessible to larger-sized adsorbates resulting from a coupled effect of competitive adsorption and size exclusion. One may argue that the DSHA-suppressed adsorption of sulfamethoxazole on the crop residue-derived black carbon is caused by competitive sorption to the free dissolved humic acids in aqueous solutions. However, this hypothesis can be ruled out, because otherwise, stronger DSHA-suppressed adsorption would have been observed for tetracycline, because tetracycline sorbs more strongly to humic acids than sulfamethoxazole (see more below). Surprisingly, despite the large molecular size tetracycline shows negligible humic-suppressed adsorption on the crop residue-derived black carbon. The observation can be attributed to a combination of two factors. First, for tetracycline the associated mineral components with black carbon make significant contribution to the overall adsorption (particularly for mBCraw); accordingly, the importance of black carbon adsorption and the caused suppression effect becomes lower. Also, the associated mineral components have low microporosity, and hence, the coadsorbed humic molecules on the mineral surfaces would only induce very slight size-exclusion effect on tetracycline adsorption regardless of the bulky size of adsorbate. Second, compared with sulfamethoxazole tetracycline has much stronger adsorption affinity toward both the black carbon and the mineral components, and thus is more capable of competing with humic molecules for adsorption surface area. It is also noted that the presence of DSHA consistently decreases the nonlinearity of antibiotic adsorption on the raw black carbon, as reflected by the increased Freundlich n values. Coadsorption of humic acids on microporous carbonaceous adsorbents may block certain surface sites and/or narrow the pore size distribution by occupying the large-sized pores.28 Consequently, the adsorption site heterogeneity decreases, and thus the adsorption on the crop residue-derived black carbon becomes more linear. Comparison with Other Geosorbents. Figure 4 compares the sorption data of the two antibiotics between mBCacid, Naþmontmorillonite clay, bulk soil, and the humic acids extracted from the soil. Sulfamethoxazole and tetracycline again manifest 5584

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Figure 4. Adsorption isotherms plotted as adsorbed concentration (q, on unit mass basis) vs aqueous-phase concentration (Ce) at equilibrium for bulk soil (0), acid-treated maize-residue-derived black carbon (Δ), Naþ-montmorillonite (O), and extracted soil humic acids (b) (measured at single concentration with six replicate samples). (a) Sulfamethoxazole. (b) Tetracycline.

very different sorption patterns. First, the disparities in sorption affinity between mBCacid and other sorbents are much larger for sulfamethoxazole (more than 5 orders of magnitude) than for tetracycline (only about 1 order of magnitude). Furthermore, compared with tetracycline sulfamethoxazole exhibits considerably lower sorption to Naþ-montmorillonite clay and bulk soil. The measured Kd values for sorption to Naþ-montmorillonite clay and bulk soil are in the order of 100 L/kg and 100; L/kg for sulfamethoxazole, but in the order of 103
105 L/kg and 102
103 L/kg for tetracycline, respectively. A similar trend is observed for humic acids
the measured Kd values from singleconcentration sorption is 450 ( 40 L/kg (standard deviation calculated from six replicate samples) for sulfamethoxazole and 3600 ( 800 L/kg for tetracycline (Note the equilibrium aqueous-phase concentrations are nearly identical between the two antibiotics). The very high sorption affinity of tetracycline can be ascribed to its extraordinarily strong complexing ability. Under the tested pH conditions (5.0 ( 0.2), tetracycline is predominantly a neutral, internal zwitterion, which contains various polar functional groups (phenol, alcohol, amine, and ketone) and charged moieties to enable strong complexation and cationexchange reactions with clay minerals and humic substances.3,21
23,26 However, sulfamethoxazole only has a limited number of complexing groups/moieties, and moreover, under the tested pH conditions a significant portion (20%) of sulfamethoxazole is anionized, and may thus invoke repulsive electrostatic interactions with the same negatively charged clay minerals (mainly due to isomorphous substitution) and humic substances (due to dissociation of carboxyl groups). More research is needed to examine the pH dependence of antibiotic adsorption on crop residue-derived black carbon. Based on the comparison of sorption isotherms, it can be derived that black carbon plays an important role in sulfamethoxazole sorption to soil, but makes negligible contribution to tetracycline sorption to soil. The contributions of black carbon to the overall sorption to bulk soil can be estimated using the measured sorption data for bulk soil and black carbon (mBCacid) and the soil black carbon content (0.34%, ref 32). The estimate is within a range of 30
97% for most of the data points of sulfamethoxazole, but only approximately 3% for all data points of tetracycline. Note that the estimate would be lowered (particularly for tetracycline) if adsorption on the intrinsic minerals associated with the black carbon is taken into account. For tetracycline, the clay fraction is apparently the most important sorption component. The sorption contribution of clay fraction estimated by the same methods is 58
76% over the examined concentration range.

Implication. The key factors and underlying mechanisms that control adsorption of environmental antibiotics on black carbon in soil need to be fully understood to ensure better prediction of the fate of these contaminants. It appears that the relative importance of black carbon in the antibiotic sorption to soil heavily relies on the complexing ability of the antibiotic molecule with other sorbent components (including intrinsic minerals associated with the crop residue-derived black carbon and clays and humic substances in soil). Furthermore, depending on the molecular size of the antibiotic adsorbate, significant pore effect (micropore filling or size exclusion) may occur and strongly affect the adsorption affinity to the crop residue-derived black carbon. Undoubtedly, more research should be warranted in the future to investigate the adsorption properties of other classes of pharmaceutical antibiotics on environmental black carbon in consideration of the very diverse electronic and molecular structures of these chemicals.

’ ASSOCIATED CONTENT

bS

Supporting Information. Table S1 summarizes selected physicochemical properties of sorbates. Table S2 summarizes surface compositions of minor elements of crop residue-derived black carbon determined by XPS. Table S3 summarizes mineral compositions of crop residue-derived black carbon determined by XRF. Table S4 summarizes Freundlich model parameters and distribution coefficients for sorption data. Figure S1 shows sorbate chemical structures and molecular sizes. Figure S2 presents adsorption kinetics for adsorption to crop residuederived black carbon. Figure S3 shows TEM images of crop residue-derived black carbon. Figure S4 presents ζ-pH relationships of crop residue-derived black carbon. Figure S5 presents Raman spectra of demineralized crop residue-derived black carbon and pure graphite. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*Phone: þ86 025 8968-0372; fax: þ86 025 8968-0372; e-mail: [email protected].

’ ACKNOWLEDGMENT This study was supported by the National Science Foundation of China (Grants 20637030, 20777031, and 21077049) and the Jiangsu Province Science Foundation of China (BK2009248) for financial support. 5585

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