Influence of Perfluorooctanoic Acid on the Transport and Deposition

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Influence of Perfluorooctanoic Acid on the Transport and Deposition Behaviors of Bacteria in Quartz Sand Dan Wu,† Meiping Tong,*,† and Hyunjung Kim*,‡ †

The Key Laboratory of Water and Sediment Sciences, Ministry of Education, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, P. R. China ‡ Department of Mineral Resources and Energy Engineering, Chonbuk National University, Baekje-daero, Deokjin-gu, Jeonju-si, Jeollabuk-do 561-756, Republic of Korea S Supporting Information *

ABSTRACT: The significance of perfluorooctanoic acid (PFOA) on the transport and deposition behaviors of bacteria (Gram-negative Escherichia coli and Gram-positive Bacillus subtilis) in quartz sand is examined in both NaCl and CaCl2 solutions at pH 5.6 by comparing both breakthrough curves and retained profiles with PFOA in solutions versus those without PFOA. All test conditions are found to be highly unfavorable for cell deposition regardless of the presence of PFOA; however, 7%−46% cell deposition is observed depending on the conditions. The cell deposition may be attributed to micro- or nanoscale roughness and/or to chemical heterogeneity of the sand surface. The results show that, under all examined conditions, PFOA in suspensions increases cell transport and decreases cell deposition in porous media regardless of cell type, presence or absence of extracellular polymeric substances, ionic strength, and ion valence. We find that the additional repulsion between bacteria and quartz sand caused by both acid−base interaction and steric repulsion as well as the competition for deposition sites on quartz sand surfaces by PFOA are responsible for the enhanced transport and decreased deposition of bacteria with PFOA in solutions.

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INTRODUCTION Perfluoroalkyl acids (PFAAs), with surface activity and thermal and acid resistance, have been widely used as raw materials for many products such as stain repellents, food packaging, and firefighting foams.1 The industrial-scale applications of PFAAs over the past few decades have inevitably released PFAAs into the environment. Thus, significant amounts of PFAAs have been detected around the world in sediment, sludge, municipal wastewater, coastal water, and even tap water.2,3 For instance, in natural water systems, PFAA concentrations vary from pg/L to μg/L, but their amounts in some wastewaters are at mg/L to low g/L levels, or up to 10 orders of magnitude higher than those found in natural aquatic systems.4,5 Because of their wide distribution and bioaccumulation in the environment, PFAAs are proposed to be persistent organic pollutants and significant attention is now directed toward understanding their potential environmental and human health impacts.6,7 For example, their toxicity of PFAAs has already been reported.6,7 Because PFAAs are water-soluble and contain hydrophobic chains and hydrophilic functional groups, recent studies have focused on the interaction between PFAAs (i.e., perfluorooctanesulfonates (PFOS) and perfluorooctanoic acid (PFOA)) and colloids present or released into the natural aquatic environment.8−10 For instance, Tang et al.8 showed that due to nonelectrostatic interactions, PFOS adsorption onto © XXXX American Chemical Society

silica is only marginally affected by pH, ionic strength, and calcium ions. Wang et al.9 reported that PFOS and PFOA adsorbed onto alumina with the maximum adsorption capacities of 0.252 and 0.157 μg/m2, respectively, at pH 4.3. Li et al.10 very recently found that because of the adsorption onto Ag nanoparticle surfaces, the presence of perfluorocarboxylic acids (PFCAs) can decrease the dissolution, aggregation, and generation of reactive oxygen species, and the toxicity of Ag nanoparticles. In addition, Tess et al.11 found that the aggregation of bacterial cells and the production of extracellular polymeric substances (EPS) increased at relatively high concentrations of PFAAs (>2 mg/L), demonstrating that PFAAs can potentially influence the surface properties of bacteria. All these results indicate that PFAAs act as highly surface-active organics in their interactions. These surface properties indicate that the presence of PFAAs in subsurface or groundwater systems influences the fate and transport of the concerned bacteria. Specifically, although the significance of different physical, chemical, and biological factors (such as grain shape and size,12,13 fluid conditions,13 solution ionic strength Received: November 8, 2015 Revised: January 25, 2016 Accepted: February 11, 2016

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DOI: 10.1021/acs.est.5b05496 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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an inverted fluorescent Ti-E microscope (Nikon, Japan) under bright field. The stock concentration is typically around 109− 1010 cells/mL, which is diluted to obtain the target influent concentration of 1.5 × 107 ± 10% cells/mL. Preparation of PFOA Suspension. The PFOA (SigmaAldrich, St. Louis, MO) stock solution was prepared by dissolving ∼10 mg of PFOA powder in 100 mL of Milli-Q water (Q-Gard1, Millipore Inc., Billerica, MA). The target concentration of the PFOA solution was 100 μg/L, which was determined using a Waters Acquity ultraperformance HPLC/ MS/MS system equipped with a 150 × 2.1 mm2 ZORBAX Extend-C18 column. Porous Media. The porous medium used for the bacterial transport experiments was quartz sand (ultrapure with 99.80% SiO2; Sinopharm Chemical Reagent Co., Ltd.) with sizes ranging from 417 to 600 μm (with a median diameter of 510 μm). The quartz sand was cleaned by sequentially soaking in concentrated HCl and then in concentrated NaOH for at least 24 h. Following each cleaning step, the quartz sand was thoroughly rinsed with deionized water. The quartz sand was dried overnight at 105 °C, followed by baking at 850 °C for 8 h. The clean sand was stored under vacuum until use. Column Experiments. The cylindrical Plexiglas columns (10 cm long and 2 cm inner diameter) were wet-packed with clean quartz sand. Prior to packing, the clean quartz sand was rehydrated by boiling in Milli-Q water for at least 1 h. After the rehydrated quartz sand was cooled, the columns were packed by adding wet quartz sand in small increments (∼1 cm) with mild vibration of the column to minimize any layering or air entrapment. A single 140-mesh stainless steel screen was placed at each end of the column. The porosity of the packed column was approximately 0.42. After packing, the columns were pre-equilibrated with 20 pore volumes of Milli-Q water and at least ten pore volumes of bacteria-free salt solutions at the desired ionic strength. Following pre-equilibration, three pore volumes of suspended bacteria with and without PFOA suspensions were injected into the column, followed by elution with five pore volumes of salt solution (without bacteria and PFOA) at the same ionic strength. For selected experiments, prior to the injection of bacteria suspensions, the columns were pre-equilibrated with three pore volumes of PFOA solutions (100 μg/L) at the desired ionic strength, followed by the introduction of two pore volumes of salt solution at the same ionic strength, to elute the suspended PFOA. The suspensions and solutions were injected into the columns in the up-flow mode by using a syringe pump (Harvard PHD 2000, Harvard Apparatus Inc., Holliston, MA). The pore water velocity for all experiments was set to 4 m/day (0.43 mL/min) to represent fluid velocities in coarse aquifer sediments. The transport experiments were conducted in both NaCl (10 and 25 mM ionic strength) and CaCl2 (1.2 and 5 mM ionic strength) solutions at pH 5.6 to avoid any complexity originated from the chemical species in buffer solution. All water used in these experiments was autoclaved for sterility. Column effluent samples were collected in sterilized glass culture tubes. The collected bacteria and reservoir samples were preserved using formaldehyde (2%) and were refrigerated at 4 °C prior to measuring the cell concentration (usually finished within 10 days). After the transport experiment, the sediment was extruded from the column under gravity and dissected into 10 segments (each 1 cm long). The retained bacteria were desorbed from the sediment segments into specified volumes of sterilized Milli-Q water with 4% formaldehyde and by shaking

and composition,14,15 nutrient conditions,16 bacterial cell type and motility,17,18 bacterial growth phase,19 and surface macromolecules20,21) have been previously demonstrated to strongly affect the transport and deposition of bacteria in porous media, the influence of PFAAs, which are emerging contaminants in the environment, on the transport and deposition of bacteria has never been explored. Furthermore, recent studies22,23 have reported that the competition for deposition sites created by other inorganic or organic colloids on the sand surface, which normally originate in the sand chemical heterogeneity under natural conditions (i.e., unfavorable conditions), significantly influences bacterial transport. PFOA is also expected to affect cell retention in sand columns, although no study has yet addressed this issue. Thus, the present study systematically investigates the effects of PFAAs on the transport and deposition of bacteria in packed porous media under environmentally relevant solution conditions. PFOA, one of the most toxic and widely found PFAAs in the natural environment, is used as the model PFAA, and the cell types E. coli and B. subtilis are used to model Gramnegative and Gram-positive cell types, respectively. Packed column experiments are conducted both with and without PFOA in bacteria suspensions in both monovalent and divalent salt solutions. Furthermore, possible mechanisms by which PFOAs affect the transport of bacteria are proposed and discussed.

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MATERIALS AND METHODS Cell Culture and Preparation. E. coli and B. subtilis, which are widely dispersed in the natural environment,24,25 were used in this study to represent Gram-negative and Gram-positive strains, respectively. We chose these two different types of bacteria since they have different cell membrane structure,20 which might cause different transport behavior with PFOA. E. coli and B. subtilis were cultivated in a Luria Broth growth medium (16 h at 37 °C while shaking at 200 rpm) and in a Tryptic Casein Soy Agar growth medium (30 °C while shaking at 200 rpm for 32 h), respectively, until they reached the stationary growth phase. The cells were harvested by centrifugation (4000g for 8 min at 4 °C). More details about the cell harvest protocols are available in our previous study26 and in the Supporting Information (SI). To remove EPS from the cells, the cation exchange resin (CER) technique was used. The CER treatment is clearly explained in our previous publications.23,26 Briefly, CER (Dowex Marathon C, 20−50 mesh, sodium form, Fluka 91973), which was soaked in Milli-Q water overnight prior to use, was added to the cells at a dosage of 2.5 g/g bacterial mass. The bacteria−CER suspension was then stirred at 600 rpm for 2.5 h at 4 °C, following which the suspension was allowed to settle for 3 min to separate the CER. The cell suspension was then transferred to a centrifugation tube. After harvest, the cell suspensions (with and without EPS) were collected by centrifugation at 8000g for 20 min at 4 °C. Note that this treatment method is widely accepted to be effective and has been used in many previous studies.20,27 The tests conducted for verifying the effectiveness of this method are described in the SI, and the information on the composition and amount of EPS associated with the cells used in the present study is available elsewhere.20 The prepared stock cell concentration (both untreated and CER-treated bacterial cell suspension) was determined using a counting chamber (Buerker-Tuerk Chamber, Marienfeld Laboratory Glassware, Germany) with B

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A132 is the Hamaker constant for substances “1” and “2” in the presence of medium “3” and can be determined from the Hamaker constant of each material. The detailed calculation of A132 based on surface free energy information is given in the SI. The calculation of κ and ΔGAB is also provided in SI. Steric Interaction. In a system with brush-layered colloids, the classic DLVO model often fails to fully explain the interactions detected experimentally because of the presence of steric forces caused by brush layers on two interacting colloids or at the colloid−solid substrate interface.19,32 Thus, to improve accuracy, steric interactions are frequently considered. They can be calculated by using33

at 350 rpm for 15 min. To obtain the cell concentration in both the effluent samples and the supernatant samples from the recovery of retained bacteria, each sample was directly counted using a counting chamber with an inverted fluorescent Ti-E microscope under bright field. The overall recovery (mass balance) of cells for each transport experiment is provided in Table S1. The protocol for obtaining mass balance is provided in the SI. Measurement of Contact Angle and Zeta Potential. The bacteria suspensions with and without PFOA were filtered through 0.45-μm acetate cellulose membranes by using vacuum filtration to form cell lawns for measuring the contact angle. After filtration, a piece of membrane was cut off and air-dried for 10 min. A contact angle analyzer (Dataphysics Co., Germany) was used to measure the contact angle of the bacteria both with and without PFOA against water, diiodomethane, and glycerol by using the sessile drop technique.15,28 The reported contact angles under all examined conditions were the average of 10 replicated measurements. The zeta potentials of bacteria and quartz sand were measured under all experimental conditions with and without PFOA by using a Zetasizer Nano ZS90 instrument (Malvern Instruments, UK). The detailed procedure for this measurement is available in previous studies.20,27 The electrophoretic mobility measurements were repeated 9−12 times. Calculation of Extended Derjaguin−Landau−Verwey−Overbeek (XDVLO) Interaction Energy. The traditional Derjaguin−Landau−Verwey−Overbeek (DLVO) theory considers apolar Lifshitz−van der Waals (LW) attraction and electrical double layer (EL) repulsion as a function of distance. However, when a liquid is polar, another category of noncovalent interactions is quantitatively more dominant than either LW or EL interactions; namely, the polar Lewis acid− base (AB) or electron acceptor/donor interactions, which were first reported by Lewis in 1923. van Oss et al.29 considered that AB should be used in calculating interactions among biopolymers, cells, and/or particles. Thus, the XDLVO theory containing LW, EL, and AB was used in the present study to calculate the interactions between bacteria and quartz sand. The equations describing the total interaction, which includes the LW, EL, and AB interactions, between bacteria and quartz sand (sphere-plate geometry) are30,31 ΦTotal = ΦLW + Φ EL + Φ AB ΔGLW = −

−1 A132 r ⎛ 14h ⎞ ⎜1 + ⎟ λ ⎠ 6h ⎝

Fsilica − cell(h) =

(5)

ΦSteric(h) = −

RESULTS AND DISCUSSION Influence of PFOA on Transport and Deposition of Cells in Monovalent and Divalent Solution. To understand the effects of PFOA on the transport of bacteria in monovalent and divalent solutions, we analyzed transport experiments involving a model Gram-negative strain E. coli and Gram-positive strain B. subtilis both with and without PFOA in suspensions. The experiments were conducted in NaCl and CaCl2 solutions at two ionic strengths (10 and 25 mM for NaCl, and 1.2 and 5.0 mM for CaCl2), respectively. The results showed that the breakthrough curves of both E. coli and B. subtilis at the higher ionic strength are lower than those acquired at lower ionic strength regardless of ion type, both with and without PFOA (Figures 1 and 2, a and c), which is consistent with the less negative cell zeta potential observed at higher ionic strength (Table S2), and thus, is qualitatively consistent with the DLVO theory, as presented in Figure S1. Similar observations were also reported previously.35,36 Although the trend in cell deposition as a function of ionic strength apparently follows the interaction energy profile, the predicted energy barrier seems insurmountable for cell deposition onto the sand surface, which indicates that the conditions are highly unfavorable for all conditions tested. Surface roughness and/or chemical heterogeneity on the sand surface could be plausible explanations; these two are widely recognized as the main factors causing the discrepancy between the theoretical predictions and experimental observations of colloid deposition under unfavorable conditions.37,38 For instance, microscale roughness can physically trap the cells when the roughness exceeds the colloid radius.39 Nanoscale roughness can also significantly reduce the energy barrier, and under some conditions, the energy barrier can be eliminated entirely.37,40 Additionally, chemical heterogeneity (e.g., metal oxide) on the collector surface allows colloid deposition in the presence of the energy barrier.41,42 Note that all of these factors are sensitive to the diffuse layer thickness, which affects the electrostatic interaction area (zone of influence), which in turn

(1)

(2)

⎪

⎪

⎛h − h⎞ ΔG AB = 2πrλABΔGhAB exp⎜ 0 ⎟ 0 ⎝ λAB ⎠

(6)

■

⎪

⎪

∫ F(h)dhh ≤ 2L

where Fsilica‑cell is the steric force between silica sand and bacteria, Φsteric is the steric interaction energy, s is the average distance between the anchoring sites, and L is the thickness of the brush layer. On the basis of previous work, the values used here for L and s are ∼134 and ∼2.2 nm,33 respectively.

⎧ ⎡ 1 + exp( −κh) ⎤ ΔGEL = πrεε0⎨2ζbζs ln⎢ ⎥ + (ζb2 + ζs2) h 1 exp( ) − − κ ⎦ ⎣ ⎩ ⎫ ln[1 + exp( −2κh)]⎬ ⎭

5/4 ⎤ ⎛ h ⎞7/4 16πκTLr ⎡ ⎛⎜ 2L ⎞⎟ ⎜ ⎟ ⎢ ⎥ + − 7 5 12 ⎝ 2L ⎠ ⎥⎦ 35s 3 ⎢⎣ ⎝ h ⎠

(3)

(4)

where h is the separation distance, r is the mean bacterial radius, λ is the characteristic wavelength of the interaction (usually taken as 100 nm), ε0 is the dielectric permittivity of vacuum (8.854 × 10−12 C V−1 m−1), ε is the dielectric constant of water (78.5), λAB is the decay length of water (1 nm), and h0 is the distance of the closest approach (0.158 nm).31 The quantity C

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chemical heterogeneity likely contribute to cell deposition since both factors are affected by ionic strength. Directly comparing the breakthrough curves of E. coli and B. subtilis with PFOA against those without PFOA shows that the breakthrough curves with PFOA (Figures 1 and 2, a and c, solid symbols) are higher than those without PFOA (Figure 1, a and c, open symbols). This holds true at both ionic strengths in NaCl and CaCl2 solutions. These results clearly demonstrate that the presence of PFOA increases cell transport in packed quartz sand regardless of the ionic strength and ion type used in this study. To examine whether the presence of PFOA in suspensions influences the deposition of bacteria in quartz sand, we acquired the retained profiles of E. coli and B. subtilis both with and without PFOA in cell suspensions in both NaCl and CaCl2 solutions (Figures 1and 2, b and d). As expected from mass balance consideration (Table S1), the retained profiles are the inverse of the plateaus of breakthrough curves. Under all ionic strengths examined in NaCl and CaCl2 solutions, the retained concentrations of E. coli and B. subtilis with PFOA are lower than those without PFOA. This observation demonstrates that the presence of PFOA decreases the deposition of bacteria in quartz sand under all ionic strength conditions regardless of the cell and ion type. Comparison of the retained profiles of E. coli and B. subtilis in the presence of PFOA versus those in the absence of PFOA shows that, under all ionic strengths, the decreased cell retention induced by the presence of PFOA in suspension occurs across the entire column. Therefore, the overall shapes of the retained profiles of E. coli and B. subtilis with PFOA are similar to those without PFOA. This observation implies that, although the presence of PFOA in suspension decreases the retention of both cell types in porous media under all ionic strengths tested in NaCl and CaCl2 solutions, the PFOA present in suspensions might not alter the deposition mechanisms of E. coli and B. subtilis in quartz sand. Effect of PFOA on Transport and Deposition of Treated Cells (without EPS). EPS secreted by cells during their growth play important roles in the transport and deposition of bacteria.45,46 To investigate whether enhanced cell transport due to the presence of PFOA holds true for bacteria without EPS on cell surfaces, we conducted transport experiments with CER-treated bacteria (i.e., bacteria for which EPS were removed from the surfaces) both with and without PFOA in solutions (Figure 3). We selected 25 mM NaCl and 5 mM CaCl2 as representative test conditions for E. coli and B. subtilis, respectively, to better capture the deposition trend for treated cells because the transport trend of untreated cells with PFOA versus without PFOA is very similar regardless of the cell strain and ionic strength. With no PFOA in suspensions, the breakthrough curve of cells without EPS (Figure 3, open triangles) is higher than that with EPS on cell surfaces (Figures 1 and 2, open squares), indicating that the removal of EPS from cell surfaces enhances cell transport. Similar observations were reported previously.20,47 A more important observation is that, similar to the untreated cells, the breakthrough curve for treated cells with PFOA present in suspensions (Figure 3, solid squares) is also higher than that without PFOA in suspensions (Figure 3, open squares). This observation clearly shows that the presence of PFOA in solutions also enhances the transport behavior of EPS-removed bacteria. Moreover, the retained profile of treated bacteria in the presence of PFOA is lower than that in the absence of PFOA, which indicates that PFOA

Figure 1. Breakthrough curves (left) and retained profiles (right) for untreated E. coli (a and b) and untreated B. subtilis (c and d) in the absence (open symbols) and presence of PFOA (solid symbols) in cell suspensions in both 10 and 25 mM NaCl solutions at pH 5.6. Error bars represent standard deviations from replicate experiments (n = 2).

Figure 2. Breakthrough curves (left) and retained profiles (right) for (a and b) untreated E. coli and (c and d) untreated B. subtilis in the absence (open symbols) and presence of PFOA (solid symbols) in cell suspensions in both 1.2 and 5 mM CaCl2 solutions at pH 5.6. Error bars represent standard deviations from replicate experiments (n = 2).

is sensitive to the ionic strength.43,44 To better understand the observed trend as a function of ionic strength in the presence of PFOA, PFOA transport and sorption tests were carried out in quartz sand at 10 mM and 25 mM NaCl solution; all other conditions were same as the bacterial column tests. The results in Figure S2 show greater PFOA sorption at higher ionic strength, indicating that sorption sites on quartz sand increase with increasing ionic strength. Note that the sorption sites are likely chemical heterogeneity on quartz sand since the main mechanism of PFOA sorption is known as electrostatic interaction.8 In addition, the results indicates that the PFOA injection time is not enough to fully saturate the sorption sites; thus, it is reasonable to conclude that both roughness and D

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might control the transport and deposition behaviors of these two representative bacteria with PFOA present in suspensions. Although PFOA does not induce obvious changes in both zeta potentials and cell size, PFOA present in suspensions might still interact with cell surfaces. An adsorption test indeed reveals that PFOA adsorbs to cell surfaces (Figure S3). Thus, to check whether the interaction of PFOA with cell surfaces contributes to the increased cell transport obtained with the PFOA copresent in suspensions, transport experiments were conducted in quartz sand with E. coli cell suspension premixed with 100 μg/L PFOA, yet from which the suspended PFOA was filtered out by 0.22-μm nylon membranes under vacuum. The breakthrough curves of cells with the removal of suspended PFOA (Figure S4, solid symbols) are equivalent to those without PFOA in suspensions (Figure S4, open symbols). These observations show that, although PFOA interacts with bacteria, the interaction does not change the transport and deposition behaviors of bacteria in quartz sand. Therefore, we can reasonably conclude that the interaction of PFOA with cell surfaces is not likely to contribute to the increased transport and decreased deposition of bacteria induced by the copresence of PFOA. Previous studies also found that the interaction of humic acid with cell surfaces did not contribute to increased bacteria transport with humic acid present in cell suspensions.23 Alteration in the Surface Properties of Quartz Sand. To understand whether the presence of PFOA influences the surface properties of quartz sand, we investigated the zeta potentials of quartz sand both with and without PFOA under all ionic strengths examined for both NaCl and CaCl2 solutions. Table S2 shows that, in both NaCl and CaCl2 solutions, the presence of PFOA in solutions slightly changed the zeta potentials of quartz sand. Specifically, under all examined conditions, the zeta potentials of quartz sand with PFOA were slightly more negative relative to those without PFOA in suspensions. Note that previous studies also found that, in the presence of PFOS or PFOA, the zeta potentials of clay particles and carbon nanotubes became more negative.48,49 As a result, the more negative zeta potentials of quartz sand obtained with PFOA in suspensions in the current study would lead to a decrease in the electrostatic interaction area due to the expansion of a diffuse double layer. Thereby, a slightly increased cell transport may be obtained when PFOA is copresent in cell suspensions. However, steric repulsion cannot be ruled out in this case since PFOA can adsorb both cell and sand surface, which generates brush layers onto both surfaces. A more quantitative analysis with additional column tests and interaction energy calculation is given below. Competition of Deposition Sites by PFOA. To test whether PFOA adsorption onto quartz sand (i.e., competition of deposition sites by PFOA) leads to increased cell transport (decreased cell deposition) in quartz sand, additional transport experiments were conducted which involved precovering the deposition sites on the quartz sand by PFOA (pretreating the columns with three pore volumes of 100 μg/L PFOA solutions). If the presence of PFOA in cell suspensions blocks sites for bacteria deposition on quartz sand (by adsorption onto quartz sand surfaces), pretreatment of the columns with PFOA solutions prior to injecting the bacteria suspension would allow deposition sites to be preferably occupied by PFOA, resulting in less favorable sites for bacteria deposition. Higher breakthrough curves and lower retained profiles of bacteria relative to those without pretreatment (without PFOA in suspensions)

Figure 3. (a) Breakthrough curves and (b) retained profiles for CERtreated E. coli and B. subtilis in the absence (open symbols) and presence (solid symbols) of PFOA in cell suspensions in 25 mM NaCl and 5 mM CaCl2 solutions at pH 5.6, respectively. Error bars represent standard deviations from replicate experiments (n = 2).

present in cell suspensions also decreases the retention of bacteria without EPS on surfaces in porous media. Mechanisms of Enhanced Transport and Decreased Deposition of Cells by PFOA. Altered Sizes and Surface Properties of Bacteria. To examine whether cell size changes due to the presence of PFOA in suspensions, cell size was measured both with and without PFOA in solutions by using an inverted microscope (Ti-E, Nikon, Japan). The sizes of at least 60 cells were measured for each sample, and the results showed that, for all cell types, the bacterial sizes in the presence of PFOA are equivalent to those in the absence of PFOA (data not shown). To further determine the effects of PFOA on cell size, the size distribution of both E. coli and B. subtilis (also, cells without EPS under representative conditions) in the absence and presence of PFOA in NaCl (10 and 25 mM) and CaCl2 (1.2 and 5 mM) solutions was acquired using dynamic light scattering (Zetasizer Nano, ZS90), and the results are presented in Table S3. Similar to microscope observations, dynamic light scattering measurements also show that, for both E. coli and B. subtilis (regardless of the presence or absence of EPS), bacteria size with PFOA is equivalent to that without PFOA in solutions. This observation further confirms that the addition of PFOA in bacterial suspension does not induce changes in individual cell size. Thus, the change in cell size is highly unlikely to contribute to the increased transport and decreased deposition of bacteria when PFOA is present in suspensions. To check whether the presence of PFOA influences the surface properties of bacteria, the cell zeta potential was measured both with and without PFOA in both NaCl and CaCl2 solutions. For both cell types, zeta potentials of bacteria in the presence of PFOA were similar to those in the absence of PFOA under all solution conditions examined (Table S2). This result shows that the presence of PFOA has no obvious effect on the electrokinetic properties of cell surfaces although the PFOA adsorption occurs to cell surfaces (Figure S3). Clearly, the increased cell transport induced by PFOA is not likely caused by changes in the cell zeta potential. Other mechanisms E

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caused by site competition from PFOA; other mechanisms induced by the presence of PFOA also contribute to the increased bacteria transport. One plausible explanation is the steric repulsion between bacteria and quartz sand because the adsorption of PFOA onto both bacteria and quartz sand occurs and generates brush layers on both sides (Figure S3).50,51 However, our adsorption test results show that the residual PFOA that is not adsorbed onto cells or sand coexists in pore space (Figure S3), and its role is not clear. Thus, to rule out the effect of the nonadsorbed PFOA, transport experiments were conducted in PFOA-pretreated sand with E. coli cell suspension premixed with 100 μg/L PFOA, yet from which the suspended PFOA was filtered out by 0.22-μm nylon membranes under vacuum. The breakthrough curve with the removal of suspended PFOA (Figure S4, open symbols) is equivalent to that with residual PFOA (Figure S4, solid symbols), supporting that steric repulsion is a sole factor contributing to the increased cell transport. Further quantitative discussion on this steric repulsion is given by the calculation of the interaction energy in the next section. Because site competition by suspended PFOA and steric repulsion by adsorbed PFOA are all present when PFOA are copresent in cell suspensions, whether the columns are pretreated with or without PFOA does not affect the transport and deposition of bacteria (with PFOA in cell suspension). Thereby, when PFOA is present in cell suspension, comparable breakthrough curves and retained profiles are observed for columns without (Figure 4, open triangles) and with the pretreatment of quartz sand with PFOA (Figure 4, solid triangles). Interaction Force between Bacteria and Quartz Sand. Although both the zeta potentials and bacteria size with PFOA are comparable to those without PFOA present in solutions (Tables S2 and S3), the zeta potentials of quartz sand in the presence of PFOA are slightly more negative than those in the absence of PFOA (Table S2). Moreover, the contact angle of bacteria with PFOA in suspensions differs slightly from that without PFOA (Table S4), resulting in a different Hamaker constant (Table S4), which in turn influences the LW. As described in the previous section, steric repulsion is also considered in the presence of PFOA in cell suspension. The presence of steric repulsion in the presence of PFOA is well supported by the higher breakthrough curves observed in treated bacteria with PFOA in suspension (Figure 3a, solid squares and Table S1) compared with untreated bacteria (Figure 1a, solid triangles and Table S1)which is consistent with the adsorption test results (Figure S3), which indicate that greater PFOA adsorption occurs for treated bacteria relative to untreated bacteria. Previous studies also reported that the density of the adsorbed brush layers influences the steric repulsive force.50,51 The result of interaction energy calculation at 10 mM NaCl is presented in Figure 5 as a representative since a similar trend is observed in other conditions (Figure S1). The clear difference in the total interaction energy between the presence and absence of PFOA indicates that the addition of PFOA in cell suspensions increases the repulsive interaction between bacteria and quartz sand. This also explains the greater cell breakthrough for the case with PFOA in suspension yet without sand pretreatment with PFOA compared to that with only the pretreatment (Figure 4 and Table S1). Environmental Implications. The presence of PFOA increases bacterial transport, and the underlying mechanism controlling the enhanced transport is very complex because

would thus be observed for columns pretreated with PFOA. On the basis of this hypothesis, pretreatment experiments were conducted under high ionic strength conditions (25 mM NaCl for E. coli and 5 mM CaCl2 for B. subtilis), where greater retention occurs to precisely detect the effect of pretreatment. Recall that cell strain does not affect the deposition mechanism, as shown in Figures 1 and 2, regardless of the salt type. Thus, different representative conditions were selected for each cell type. Interestingly, for both Gram-negative E. coli and Grampositive B. subtilis, the breakthrough curves for columns pretreated with PFOA yet without PFOA present in suspensions (Figure 4a and c, solid squares) are higher than

Figure 4. Breakthrough curves (left) and retained profiles (right) for (a and b) untreated E. coli and (c and d) untreated B. subtilis in the absence (squares) and presence (triangles) of PFOA in cell suspensions both with (solid symbols) and without (open symbols) the pretreatment of the quartz sand with three pore volumes of 100 μg/L PFOA solutions. The data without pretreatment of quartz sand with PFOA (open symbols) were replotted from Figures 1 and 2. Error bars represent standard deviations from replicate experiments (n = 2).

those without pretreatment with PFOA (i.e., without PFOA in cell suspension; see Figure 4, open squares). Accordingly, lower retained profiles are observed for columns pretreated with PFOA yet without PFOA present in suspensions (Figure 4b and d, solid squares). These observations show that, on quartzsand surfaces, PFOA does compete for deposition sites with bacteria. Clearly, site blocking (site competition) by PFOA contributes to the enhanced transport and decreased deposition with PFOA in suspensions. Note that if the increased cell transport were caused solely by the site competition of PFOA, equivalent breakthrough curves and retained profiles would be observed for columns pretreated with PFOA yet without PFOA present in suspensions and for columns without pretreatment yet with PFOA in cell suspensions. However, for both cell types, breakthrough curves with PFOA in suspensions without pretreatment (Figure 4, open triangles) are higher than those with pretreatment yet without PFOA in cell suspensions (Figure 4, solid squares). Accordingly, lower retained profiles are obtained for columns without pretreatment yet with PFOA in suspensions. The increased cell transport and reduced cell deposition is not solely F

DOI: 10.1021/acs.est.5b05496 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Nature Science Foundation of China under Grants 41422106 and 21177002.

Figure 5. Interaction energy between bacteria and quartz sand in the absence (dashed line) and presence (solid line) of PFOA in cell suspension.

bacterial deposition in the presence of PFOA is not controlled by a sole factor but rather by coupled roles of suspended and adsorbed PFOA; in other words, increased repulsion and deposition competition. Furthermore, these PFOAs and bacteria are expected to respond similarly to changes in the solution environment in terms of adsorption and deposition (e.g., greater adsorption or deposition with increasing ionic strength) as observed in studies that use similar types of organic matter,23 which actually leads to further complexity. Nonetheless, the concentration of PFOA used in this study is 100 μg/L, which is relevant to natural conditions, particularly to areas that can be influenced by sewage wastewater leakage.4,5 Therefore, if these organic compounds are released into the soil environment, the PFOA is expected to interact strongly with various colloidal contaminants (e.g., toxic nanoparticles and pathogens) and eventually facilitate their transport beyond that predicted by conventional models (e.g., filtration theory) because they are strong surface-active compounds, as shown in previous studies48,49 as well as by our adsorption results. Thus, to further understand the role of PFOA in the transport and deposition of bacteria, we should focus on elucidating the role of transport and sorption of PFOA, PFOA and bacteria concentration, the presence of other materials (i.e., nanoparticles and NOMs), and the presence of naturally occurring oxides and hydroxides on sand surfaces.

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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.5b05496. Mass balances (Table S1); zeta potentials for bacteria and quartz sand (Table S2); cell size (Table S3); contact angles for bacteria with and without PFOA (Table S4); Interaction energy profiles between E. coli and quartz sand with and without PFOA (Figure S1); PFOA transport behavior in quartz sand (Figure S2); PFOA adsorption fraction onto cells (Figure S3); breakthrough curves for PFOA adsorbed bacteria with and without nonadsorbed PFOA in PFOA-pretreated sand (Figure S4); additional materials and methods (PDF)

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DOI: 10.1021/acs.est.5b05496 Environ. Sci. Technol. XXXX, XXX, XXX−XXX