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Inhibited transport of graphene oxide nanoparticles in granular quartz sand coated with Bacillus subtilis and Pseudomonas putida biofilms
Chemosphere 169 (2017) 1e8
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Inhibited transport of graphene oxide nanoparticles in granular quartz sand coated with Bacillus subtilis and Pseudomonas putida biofilms Jian-Zhou He a, d, Deng-Jun Wang b, Huan Fang c, d, Qing-Long Fu a, d, Dong-Mei Zhou a, * a
Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China Department of Plant and Soil Sciences, University of Delaware, Newark, DE 19716, United States c State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China d University of Chinese Academy of Sciences, Beijing 100049, China b
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Effect of biofilms on the transport of GONPs was systematically examined. XMCT was used to quantitatively characterize the pore structures of packed columns. Biofilms reduced the porosity and narrowed the pore sizes of sand columns. The presence of biofilms provides favorable sites for GONPs retention/ attachment.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 March 2016 Received in revised form 30 October 2016 Accepted 1 November 2016
Increasing production and use of graphene oxide nanoparticles (GONPs) boost their wide dissemination in the subsurface environments where biofilms occur ubiquitously, representative of the physical and chemical heterogeneities. This study aimed at investigating the influence of Gram-positive Bacillus subtilis (BS) and Gram-negative Pseudomonas putida (PP) biofilms on the transport of GONPs under different ionic strengths (0.1, 0.5, and 1.0 mM CaCl2) at neutral pH 7.2 in water-saturated porous media. Particularly, the X-ray micro-computed tomography was used to quantitatively characterize the pore structures of sand columns in the presence and absence of biofilms. Our results indicated that the presence of biofilms reduced the porosity and narrowed down the pore sizes of packed columns. Transport experiments in biofilm-coated sand showed that biofilms, irrespective of bacterial species, significantly inhibited the mobility of GONPs compared to that in cleaned sand. This could be due to the Ca2þ complexation, increased surface roughness and charge heterogeneities of collectors, and particularly enhanced physical straining caused by biofilms. The two-site kinetic retention model-fitted value of maximum solid-phase concentration (Smax2) for GONPs was higher for biofilm-coated sand than for cleaned sand, demonstrating that biofilms act as favorable sites for GONPs retention. Our findings presented herein are important to deepen our current understanding on the nature of particle-collector interactions. © 2016 Elsevier Ltd. All rights reserved.
Handling Editor: Chang-Ping Yu Keywords: Graphene oxide nanoparticles Biofilm Transport Porous media Computed tomography Modeling
1. Introduction * Corresponding author. E-mail address: [email protected] (D.-M. Zhou). http://dx.doi.org/10.1016/j.chemosphere.2016.11.040 0045-6535/© 2016 Elsevier Ltd. All rights reserved.
Graphene oxide, a layered carbonaceous nanomaterial, is composed of graphene sheets and oxygen-containing functional
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J.-Z. He et al. / Chemosphere 169 (2017) 1e8
groups such as epoxide, carbonyl, carboxyl, hydroxyl, and phenol (Dikin et al., 2007; Dreyer et al., 2010). In the past decade, graphene oxide nanoparticles (GONPs) have received exploding attention in many fields (e.g., biomedicine, nanoelectronics, sensors and conductive films) attributable to their unique structures and extraordinary physiochemical properties (Eda et al., 2008; Fugetsu et al., 2010; Berlin et al., 2011; Zhang et al., 2011). Nonetheless, an increasing number of studies demonstrated that GONPs are toxic to human, animal, and bacteria (Liu et al., 2011; Vallabani et al., 2011; Wang et al., 2011a; Gurunathan et al., 2013). For instance, GONPs exhibited dose-dependent toxicity to human fibroblast cells and mice by inducing cell apoptosis and lung granuloma formation (Wang et al., 2011a). Liu et al. (2011) also found GONPs showed high antibacterial activity towards Escherichia coli, which was ascribed to the membrane and oxidation stress. As the knowledge of GONPs potential risks to environment and human health remains unsound yet, a thorough understanding of the fate and transport of GONPs is critical for their benign use and risk assessment and management. GONPs display high solubility and stability in aquatic environment (Mkhoyan et al., 2009; Chowdhury et al., 2013), where biofilms are ubiquitous, representative of the physical and chemical heterogeneities in riverbank sediments or groundwater aquifers. To date, several studies have documented that biofilms play an important role on the fate and transport of engineered nanoparticles (ENPs) in granular aquatic matrixes (Tong et al., 2010; Lerner et al., 2012; Tripathi et al., 2012; Jiang et al., 2013; Xiao and Wiesner, 2013; Mitzel and Tufenkji, 2014; He et al., 2015). Findings of Tripathi et al. (2012) on the transport of four types of ENPs with different particle sizes and surface chemistries revealed that the four ENPs exhibited increased retention in the biofilmladen packed bed. Similarly, Lerner et al. (2012) reported enhanced retention of zerovalent iron nanoparticles (nZVI) in the presence of Pseudomonas aeruginosa biofilm on sand grains. Very recently, we compared the transport behaviors of GONPs mediated by biofilm and extracellular polymeric substance (EPS) in watersaturated sand columns. Our findings indicated that EPS exhibited negligible influence on GONPs transport due to effects of hydration effect and steric repulsion, whereas enhanced retention of GONPs was observed in biofilm-coated sand. We speculated that the greater retention of GONPs in the presence of biofilm is likely due to the increased surface roughness and physical straining. However, since the real three-dimensional (3D) structure of biofilms developed in porous media is still poorly understood, our explanations regarding the role of biofilm on ENPs transport are ambiguous without any direct evidence. During the past several decades, the X-ray micro-computed tomography (XMCT) technique has been successfully employed to visualize and quantify 3D microstructure of porous materials (Flannery et al., 1987). The advantages of this technique are nondestructive and time-effective compared with the traditional s, 1992). Systematic anamethods, e.g., mercury porosimetry (Fie lyses of images acquired by XMCT scanning can provide new information on pore space of specimen with respect to variables, such as soil bulk density (Petrovic et al., 1982), porosity (Zhou et al., 2013), and solutes breakthrough (Clausnitzer and Hopmans, 2000) in porous media. Researchers (Davit et al., 2011; Iltis et al., 2011; du Roscoat et al., 2014) have successfully visualized the 3D biofilms in porous media via XMCT technique. Thus, XMCT-based method is anticipated to provide novel and unique insights into the morphology of granular medium where ENPs remain direct contacts with bacterial biofilm. The overarching objective of this work was to examine the influence of biofilm on the transport of GONPs in saturated sand columns under three different ionic strengths (ISs, 0.1, 0.5 and 1.0 mM CaCl2) at neutral pH 7.2. Two representative bacteria, i.e.,
Gram-positive Bacillus subtilis (BS) and Gram-negative Pseudomonas putida (PP) were selected as model biofilms. To our knowledge, the XMCT technique was, for the first time, applied to unravel the effect of biofilms on the fate and transport of GONPs in porous media. Our findings will advance the current knowledge of the role of biofilm in GONPs transport in porous media, and thus deepen our understanding on the nature of particle-collector interactions in the subsurface environments. 2. Materials and methods 2.1. Preparation of GONPs influent suspensions The GONPs were obtained from Nanjing XFNANO Materials Tech Co., Ltd. (Nanjing, China). The manufacturer reported that the purity of GONPs were >99% (atomic force microscopy image is provided in Fig. S1, Supplementary Information). Upon receipt, the GONPs stock solution (2.0 mg mL1) was stored at 4 C. Twenty mg L1 of GONPs influents with varied ionic strengths (ISs) in calcium chloride (CaCl2) (Analytical grade, Sinopharm Co., Ltd., China) were created by diluting aliquots of the GONPs stock solution to the electrolyte solutions (0.1, 0.5, and 1.0 mM CaCl2). The resulting suspension was then mixed thoroughly followed by sonicating at 45 kHz, 100 W (KQ-300VDE, Kunshan Sonicator Co., China) over 1 h prior to the column transport experiments. All electrolyte solutions and GONPs influents were prepared using sterilized deionized (DI) water (18.2 MU cm, Millipore, Inc., USA). The pH of GONPs influents was adjusted to 7.2 using 0.1 M NaOH. 2.2. Column transport experiments Column experiments were performed in the absence and presence of biofilms formed by Bacillus subtilis (BS) and Pseudomonas putida (PP) using glass chromatography column (Shanghai Huxi Glassware Co., China) with 2.6-cm inner diameter and 20-cm in length (Zhou et al., 2011). Quartz sands (Sinopharm Chemical Reagent Co., Ltd., China) with sizes ranging from 600 to 710 mm were used as porous media for column transport experiments. Before use, the sand was thoroughly cleaned following the method of Zhou et al. (2011). To pack the vertically-oriented column, granular sands autoclaved at 121 C for 30 min were carefully added in 1e2 cm increments and then gently vibrated to eliminate any layering or air bubbles (Wang et al., 2012a). For biofilm-coated sand condition, the column was wet-packed with autoclaved sands premixed with bacterial suspension using the procedure described in our recent study (He et al., 2015) and also provided in S1, Supplementary Information (SI). Before initiating transport experiments, the packed columns were fully equilibrated with several pore volumes (PVs) of GONPsfree background electrolyte (pH 7.2) in an upward mode to establish steady hydrodynamic and chemical condition (Wang et al., 2011b). Subsequently, 3.5 PVs of the prepared GONPs influents (20 mg L1) at the desired ISs (0.1, 0.5, and 1.0 mM CaCl2) were introduced into the column using a peristaltic pump (YZП-15, Baoding Longer Precision Pump Co., Ltd., China) at a flow rate of 1.0 mL min1, followed by background electrolyte elution for 4 PVs. Column effluents were automatically collected into 15-mL sterile glass tubes at regular intervals using a fraction collector (BS-100A, Huxi Analytical Instrument Factory Co., Ltd, China), and the concentration of GONPs was immediately determined with UV/Vis spectrophotometer at the wavelength of 228 nm (He et al., 2015). A calibration curve was pre-established by diluting the 20 mg L1 GONPs influent, which was linear within the range of 0e20 mg L1 (Fig. S2, R2 > 0.999).
J.-Z. He et al. / Chemosphere 169 (2017) 1e8
2.3. Characterization of GONPs and sand collectors Several methods were used to characterize the physicochemical properties of GONPs and sand collectors that likely influence GONPs transport in porous media. Morphological property of GONPs was examined with transmission electron microscopy (TEM), and the samples were prepared by drying a droplet of GONPs suspension (20 mg L1) onto a copper TEM grid (JEM-2100, JEOL, Japan). Stability of GONPs influents was also determined by monitoring the light absorption over the time frame of the column transport experiments (3 h) and the results revealed that the GONPs influents were stable under investigated ISs (Figs. S3 and SI). The z-potential and hydrodynamic diameter were measured using a NanoBrook 90Plus PALS analyzer (Brookhaven Instruments, US). 2.4. XMCT scanning and image processing An industrial Phoenix Nanotom X-ray micro-computed tomography facility (XMCT, GE, Sensing and Inspection Technologies, GmbH, Wunstorf, Germany) was used to characterize the pore structure of columns packed with cleaned and biofilm-coated sands. The prepared column was mounted on a rotary stage and scanned at a voltage of 110 kV and an electrical current of 100 mA from different angles at same intervals. The final slices were stored in 8-bit format, which means each voxel had a value between 0 and 255 representing the attenuation coefficient of the corresponding material. The resulting voxel size was 15 15 15 mm3. A region of interest (ROI) was selected from the central part of columns to avoid artifacts at the boundary region. The image stacks were cropped to an ROI of 600 600 800 voxels, representing a volume of 9 9 12 mm3. Image processing and visualization were conducted with the open-source software ImageJ. Media filter and segmentation were conducted first. Pore size distribution (PSD) was obtained by morphological “opening” operations. Briefly, pore smaller than a certain size was removed by erosion followed by dilation using a spherical structuring element, which is called “opening”. By changing the size of the structuring element, the PSD could be derived. A detailed description about this method was reported by Schlüter et al. (2011).
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are presented in Table 1. The calculated z-potentials of GONPs were all negative under examined pH value, in accordance with the previous literature (Stoller et al., 2008) considering that the isoelectric point (IEP) was 3 for graphene oxide. The z-potentials progressively became less negative with increasing ISs, which is in agreement with the anticipated influence of electrostatic double layer (EDL) compression (Elimelech et al., 1995). For example, the zpotential of GONPs decreased from 28.3 to 17.9 mV when the IS was increased from 0.1 to 1.0 mM (Table 1). Likewise, the same decreasing trend of z-potentials was observed for sand grains in response to increasing ISs. The presence of biofilms (i.e. BS and PP) decreased the absolute surface potential of cleaned sand to some extent, consistent with the findings documented in previous publications (Tripathi et al., 2012; He et al., 2015). For example, the zpotential of cleaned sand was 32.9 mV, while the values of BS biofilm and PP biofilm-coated sand were declined to 25.1 and 24.1 mV, respectively, in 0.1 mM CaCl2 at pH 7.2 (Table 1). The effect of solution chemistry on GONPs aggregation was also examined using dynamic light scattering (DLS) and TEM. The averaged hydrodynamic diameter (Dh) of GONPs was found to increase from 296 to 698 nm when the IS was increased from 0.1 to 1.0 mM in CaCl2 (Table 1). Additionally, DLS size change of GONPs over the time frame of the column transport experiments (i.e., 3 h) is shown in Fig. S4 in SI, which indicates that GONPs influents were relatively stable with slight ascending in DLS sizes for both 0.1 and 0.5 mM CaCl2, whereas the DLS sizes increased gradually from initial 698 nm to final 1356 nm at the investigated duration for 1.0 mM CaCl2 case. As depicted in Fig. 1, the representative TEM micrographs showed that in DI water and 0.1 mM CaCl2, the GONPs flakes were well dispersed, mostly as irregularly shaped thin flakes with few wrinkles. In contrast, at 0.5 mM CaCl2, the TEM image clearly showed GONPs flakes started to overlap and aggregate together. Particularly, significant aggregations of GONPs occurred at IS of 1.0 mM CaCl2. The aggregates were much darker in color, indicating the stacking of multiple GONPs flakes. The above observations demonstrated that high IS decreased the stability of GONPs influents, which is well-documented in the literature (Lanphere et al., 2013; Liu et al., 2013; Qi et al., 2014). 3.2. Transport of GONPs in cleaned and biofilm-coated sand
2.5. Mathematical modeling An inert tracer (bromide) experiment was conducted to obtain the pore-water velocity and dispersion coefficient, by fitting tracer breakthrough curves using the CXTFIT code (Toride et al., 1999). A one-dimensional form of the convection-dispersion equation (CDE) with two types of kinetic retention sites (Schijven and Sim unek, 2002; Bradford et al., 2003) was used to simulate the GONPs transport in the column experiments. The two-site kinetic retention model has been successfully employed to simulate the transport of GONPs in saturated quartz sand covered with iron oxides, biofilms, and extracellular polymeric substances (Wang et al., 2012a, b; He et al., 2015). For the cleaned sand column in this study, site 1 and site 2 are the surface locations of quartz sand and metal (iron or aluminum) oxide impurity, respectively; whereas, they are cleaned sand and biofilm surface location, respectively, in biofilm-coated sand column. Detailed model description is given in SI S2. 3. Results and discussion 3.1. Properties of GONPs and sand collectors Properties of GONPs influents and quartz sands in the presence and absence of biofilms at various ISs (0.1e1.0 mM CaCl2 at pH 7.2)
Fig. 2a, b and 2c present the breakthrough curves (BTCs) of GONPs in the absence and presence of biofilms, under varied solution ISs (0.1e1.0 mM CaCl2) at pH 7.2. The BTCs are plotted as normalized effluent concentration (C/C0) versus PVs. GONPs broke through at approximately 1.0 PV with the exceptions of BS biofilm and PP biofilm-coated sand columns at IS ¼ 1.0 mM. The value of C/ C0 increased gradually and did not reach a steady peak plateau. The observed asymmetric BTCs were inconsistent with the prediction by classical filtration theory (Yao et al., 1971). These results are indicative of blocking behavior, i.e., decreasing deposition rates with time. Fig. 2a shows the BTC for GONPs transport in cleaned sand in 0.1e1.0 mM CaCl2. Increasing the ionic strengths reduced the maximum effluent concentration of GONPs; that is, the value of C/ C0 dramatically decreased from 0.99 to 0.36 when ISs increased from 0.1 to 1.0 mM CaCl2. Similar results were observed in recent studies (Feriancikova and Xu, 2012; Lanphere et al., 2013; Liu et al., 2013; Qi et al., 2014). These overall phenomena can be attributed to the consistently decreased z-potential (less negative) and increased DLS sizes (Table 1), induced by increasing ISs. In comparison to cleaned sand, Fig. 2b and c shows the presence of BS biofilm and PP biofilm significantly enhanced the retention of GONPs under all experimental conditions. The normalized effluent concentrations (C/C0) were all correspondingly lower than that of
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Table 1 Properties of GONPs influents and quartz sand coated with or without biofilms, as well as the calculated height of repulsive maximum energy barrier (Fmax) and depth of attractive secondary minimum (Fmin2) according to the DLVO theory. IS (mM)
DLSa (nm)
z-potential (mV)
FbGONPs-Cleaned
FcGONPs-BS (kT)
FdGONPs-PP (kT)
(kT)
0.1 0.5 1.0
296 322 698
GONPs
Cleaned sand
BS biofilm-coated
PP biofilm-coated
Fmax
Fmin2
Fmax
Fmin2
Fmax
Fmin2
28.3 ± 1.8 22.2 ± 1.5 17.9 ± 1.9
32.9 ± 0.4 28.4 ± 0.7 28.4 ± 1.0
25.1 ± 0.8 22.0 ± 0.7 17.4 ± 0.1
24.1 ± 2.5 16.8 ± 2.6 13.5 ± 2.1
339 209 302
NAe 0.068 0.35
254 160 176
NA 0.072 0.40
241 111 120
NA 0.077 0.43
a
Average hydrodynamic diameters of GONPs, measured by DLS. Interaction energy between GONPs and cleaned, BS biofilm, or PP biofilm-coated sand, respectively, in the unit of kT (where k is the Boltzmann constant and T is the absolute temperature). e Not Applicable. b,c, and d
Fig. 1. Representative TEM images of GONPs under different ISs.
GONPs transport in cleaned sand under same solution chemistry. Similar findings were recently reported for other ENPs (e.g., ZnO nanoparticles and nZVI) transport (Lerner et al., 2012; Jiang et al., 2013). However, no discernible differences on GONPs transport were observed between BS biofilm and PP biofilm tests, which is likely due to the similar physical structures of two biofilms (discussed in Section 3.3). For example, the magnitude of C/C0 for GONPs transport in BS biofilm- and PP biofilm-coated sands ranged from 0.89 to 0.01 and from 0.89 to 0.06, respectively, with IS increasing from 0.1 to 1.0 mM CaCl2. The two-site kinetic retention model assuming Langmuirian blocking on site 2 provided a good description of BTCs (see Fig. 2 and R2 in Table 2). Table 2 summarizes the fitted parameters of k1, k1d, k2 and Smax2, as well as the Pearson's correlation coefficient (R2). The values of k2 and Smax2 all increased with ascending ionic strengths for cleaned, BS biofilm- and PP biofilm-coated sands, suggesting that mechanism controlling GONPs retention near the column inlet is sensitive to solution ionic strengths (Wang et al., 2012a, b; He et al., 2015). Meanwhile, the fitted values of Smax2 tended to increase due to the presence of BS biofilm and PP biofilm. In particular, Smax2 is proportional to the fraction of surface areas that is favorable for retention (Bradford et al., 2009; Wang et al., 2012a). These observations suggest that the presence of biofilms, irrespective of bacteria species, provide the favorable sites for GONPs retention/attachment.
3.3. Mechanisms of reduced transport of GONPs by biofilms 3.3.1. DLVO interaction energy As discussed in Section 3.1, the GONPs and sand collector surface were both negatively charged under investigated solution chemistries (Table 1). Therefore, the deposition of the negatively charged GONPs onto the cleaned, BS biofilm-, and PP biofilm-coated sands is considered to be unfavorable; namely, GONPs experience repulsive electrostatic double layer (EDL) interactions as it approaches the sand surfaces. A sphere-plate configuration was used to estimate the total interaction energy (the sum of the attractive van der Waals (VDW) and the EDL interactions) based on the classical DerjaguinLandau-Verwey-Overbeek (DLVO) theory (Derjaguin and Landau, 1941; Verwey and Overbeek, 1948). Details are given in SI S3. Table 1 summarizes the parameter values calculated based on the classical DLVO theory and Fig. 3 presents the detailed interaction energy profiles. The data in Table 1 and Fig. 3 indicated that strong primary energy barriers existed (over 111 kT, k is the Boltzmann constant and T is the absolute temperature) for all conditions tested, which impaired GONPs to deposit on the sand surfaces in the primary energy well. A slight increase of Fmax for the three conditions was observed when IS increased from 0.5 to 1.0 mM CaCl2. This is most likely due to the significant increase in DLS sizes of GONPs (from 322 to 698 nm), which would outperform the effect of z-potentials resulting from the changes in ISs. Similar
J.-Z. He et al. / Chemosphere 169 (2017) 1e8
1.0
0.1 mM 0.1 mM-fitted 0.5 mM 0.5 mM-fitted 1.0 mM 1.0 mM-fitted
(a)
0.8
C/C0
0.6 0.4 0.2 0.0 0
1
2
3
4
5
6
7
8
PV
0.1 mM 0.1 mM-fitted 0.5 mM 0.5 mM-fitted 1.0 mM 1.0 mM-fitted
(b)
1.0 0.8
C/C0
0.6 0.4 0.2 0.0 0
1
2
3
4
5
6
7
8
PV
1.0
0.1 mM 0.1 mM-fitted 0.5 mM 0.5 mM-fitted 1.0 mM 1.0 mM-titted
(c)
0.8
C/C0
0.6 0.4 0.2 0.0 0
1
2
3
4
5
6
7
8
PV Fig. 2. Observed (symbols) and fitted (lines) breakthrough curves of GONPs in cleaned (a), BS biofilm- (b), and PP biofilm- (c) coated sand columns under different ISs (pH 7.2). Error bars represent the standard deviations.
findings have been frequently reported in the literature (Fang et al., 2013; Lanphere et al., 2013; Liu et al., 2013). Additionally, the predicted depth of attractive secondary minimum (ca. 0.068 to 0.43 kT) was relatively shallow, demonstrating that deposition of GONPs in the secondary minimum (Fmin2) is anticipated to be negligible. Fig. S5 also confirmed this that only a negligible amount (0.8%e6.5%) of retained GONPs was recovered during Phrase 3 when the ionic strength was reduced to zero, i.e., the secondary minimum was eliminated in the presence of DI water (Franchi and O'Melia, 2003). Thus, based on the interpretation of classical DLVO interactions, GONPs are not expected to deposit on sand surfaces, although the attractive secondary minimum is substantially likely involved in GONPs deposition in previous literature. The noted
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disagreement between the experimental BTCs and the DLVO prediction suggest that other factors are contributable to the retention of GONPs in the presence of biofilms under various solution chemistries. 3.3.2. Surface properties It is reported that natural organic matter (NOM) contains hydroxyl, carboxyl, and amino functional groups (Schulten and Schnitzer, 1993; Leenheer, 2007). Previous study showed that GO exhibited specific interactions with NOM via functional group association under electrostatically unfavorable condition (Chowdhury et al., 2014b). Likewise, BS and PP bacterial surfaces have identical functional groups, i.e., carboxyl, amino, phosphate, and hydroxyl related moieties (Jiang et al., 2004; Cao, 2013), which are similar to those of NOM. Hence, it is anticipated that more specific interactions occurred between GONPs and biofilms compared to cleaned sands that only include relatively ‘inert’ silanol group. GONPs interact with biofilms via H-bonds, Lewis acidbase, and p-p interactions (Hartono et al., 2009). Moreover, divalent cations (e.g., Ca2þ) destabilized GO in the presence of NOM due to charge screening and obvious bridging effect (i.e., GO-MetalNOM complexation) (Chowdhury et al., 2014b, 2015). In our study, the value of C/C0 for GONPs was much lower in 1.0 mM CaCl2 than that obtained in 50 mM NaCl (C/C0: 0.01 vs 0.24; IS: 1.0 mM vs 50 mM) (He et al., 2015) for BS biofilm-coated condition. This is largely ascribed to strong complexation between GONPs and biofilms in the presence of divalent Ca2þ. Similar findings were reported in the literature (Wang et al., 2011b; Jiang et al., 2013; Chowdhury et al., 2014a). Also, surface heterogeneities (e.g., physical roughness and charge heterogeneity) of colloids and collectors have been documented to play a vital role on colloid transport under unfavorable attachment conditions (Siegrist and Gujer, 1985; Tufenkji and Elimelech, 2005; Morales et al., 2009; Shen et al., 2013; Torkzaban and Bradford, 2016). Our recent work (He et al., 2015) revealed that biofilms developed by BS and PP bacteria used in the present study increased the physical roughness of sand collector with inhomogeneous coverage, which is consistent with the depiction of biofilm by Mitzel and Tufenkji (2014). Surface roughness created low flow velocity region (Vaidyanathan and Tien, 1988; Wang et al., 2011c), where GONPs experienced less hydrodynamic forces and torques and flow vortices. Thus, surface roughness is expected to result in greater retention of GONPs in biofilm-coated sand, consistent with recent publications (Tong et al., 2010; Lerner et al., 2012; Jiang et al., 2013). On the other hand, due to the heterogeneously covered quartz sand by biofilms (Fig. S6), coupled with more negative z-potentials of sand collectors than that of biofilms (Table 1), it is reasonable to suspect that charge heterogeneity is highly likely to affect GONPs transport. In addition, surface charge heterogeneity in the colloid population substantively exists. Wang et al. (2012c) tested this by measuring the z-potentials of Alizarin red S-labeled hydroxyapatite nanoparticle (ARS-nHAP) before and after filtering ARS-nHAP through 1-mm pore diameter glass fiber filters. They found that the z-potentials of ARS-nHAP became progressively more negative after filtration, and concluded the fraction of the ARS-nHAP population with lower z-potentials was assumed to attach preferentially at the column inlet, whereas the remaining nanoparticles experienced a slower attachment rate and greater transport potential. Similarly, a reduction in z-potentials induced by biofilm coatings would effectively decrease the repulsive interaction and increase the attractive interaction between GONPs (especially for those with less charge) and biofilms than that between GONPs and cleaned sand. These provide a plausible explanation on the enhanced GONPs retention in biofilm-coated sand.
Table 2 Summary of fitted parameters obtained from the two-site kinetic retention model based on the breakthrough curve data of GONPs, in the absence and presence of biofilms at various ISs at pH 7.2. Sand type
IS (mM)
k1a (min1)
k1db (min1)
k2c (min1)
Cleaned
0.1 0.5 1.0 0.1 0.5 1.0 0.1 0.5 1.0
1.81 1.60 0.52 1.10 1.26 1.50 0.89 2.33 7.86
1.33 1.22 0.51 0.87 0.96 1.22 0.46 1.12 7.77
9.18 4.49 1.11 4.51 5.88 2.47 7.05 8.29 2.60
BS biofilm-coated
PP biofilm-coated
a b c d e
103 102 101 102 102 101 103 102 101
Smax2d (mg g1)
R2e
0.06 1.09 2.44 0.53 1.46 118.43 0.75 1.92 25.24
0.999 0.999 0.970 0.995 0.993 0.920 0.998 0.998 0.865
First-order retention rate coefficient on site 1. First-order detachment rate coefficient on site 1. First-order retention rate coefficient on site 2. Maximum solid-phase retained concentration of GONPs on site 2. Pearson's correlation coefficient.
350
(a) 0.1 mM CaCl2
Interaction Energy (kT)
300
0.5 mM CaCl2
250
1.0 mM CaCl2
200 150 100 50 0 0
20
40
60
80
100
h (nm)
Interaction Energy (kT)
350
(b)
300
0.1 mM CaCl2
250
0.5 mM CaCl2 1.0 mM CaCl2
200 150 100 50 0 0
20
40
60
80
100
h (nm)
350
(c)
Interaction Energy (kT)
300
0.1 mM CaCl2
250
0.5 mM CaCl2 1.0 mM CaCl2
200 150 100
3.3.3. Physical straining In addition to the above mechanisms that may result in the enhanced retention of GONPs in biofilm-coated sand, physical straining, reported in many previous studies (Bradford et al., 2005, 2007; Jiang et al., 2013) is also likely to play an appreciable role in inhibiting GONPs transport in this study. It is documented that biofilms grown inside the column occupied the pore vacancy, yielding a reduction in void space (Dupin and McCarty, 2000; Liu et al., 2008). To test this hypothesis, the XMCT was used to characterize the pore sizes and porosities of packed columns before and after the biofilm formation. We extracted sub-volumes of size 600 600 800 voxels (i.e., 9 9 12 mm3) from the central part of each image for further analysis. It should be mentioned that although only PP biofilm-coated column was analyzed using XMCT, the procedure used for coating biofilm onto sand surface was wellestablished and warranted the reproducibility as per our recent work (He et al., 2015). Therefore, it is reasonable to expect that BS biofilm grown inside the column would have similar effect on the pore size distribution and cumulative porosity as PP biofilm did. Fig. 4 shows the resultant visualization of microstructure for cleaned and PP biofilm-coated sand columns. While the overall variation of micro-pore structure between selected columns cannot be visually detected (the pores discussed here were excluded those with sizes smaller than 15 mm due to resolution limitation), Fig. 5 clearly presents the difference in pore size distribution and cumulative porosity between cleaned and PP biofilm-coated sand columns. Close inspection of Fig. 5 indicated that the bulk porosity was 0.44 and 0.39 for cleaned and PP biofilm-coated conditions, respectively. Pore size distribution showed clear evidence of unimodal pattern, with pores smaller than 59.7 mm slightly increased and those larger than 59.7 mm significantly decreased in PP biofilm-coated sand as compared to the cleaned sand. In general, a lower micro-porosity is expected to result in a less mobility of water and GONPs in biofilm-coated sand. It should be noted that while the discernible pore scale is > 15 mm which is 2-orders of magnitude larger than the DLS sizes of GONPs under all the investigated solution chemistries, our findings directly prove that grown biofilm on sand surfaces would reduce the porosity and narrowed the pore sizes, thereby greatly inducing physical straining. This interprets the enhanced retention of GONPs in the presence of biofilms.
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4. Conclusions
0 0
20
40
60
80
100
h (nm) Fig. 3. Calculated DLVO interaction energy between GONPs and cleaned (a), BS biofilm- (b), and PP biofilm- (c) coated sand as a function of separation distance (h) at various ISs (pH 7.2).
In this research, the role of biofilms, developed from Bacillus subtilis (BS, Gram-positive) and Pseudomonas putida (PP, Gramnegative) strains, on the transport of GONPs in three different ionic strengths (0.1, 0.5, and 1.0 mM CaCl2) at pH 7.2 was
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Fig. 4. Representative 2D and 3D visualizations of pore structures for cleaned (upper) and PP biofilm-coated (lower) sand columns.
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Effective pore diameter (um) Fig. 5. Effective pore size distribution and cumulative porosity of pore structures for a selected region (9 mm 9 mm 12 mm) within the cleaned and PP biofilm-coated sand columns.
systematically unraveled. Reduced transport of GONPs occurred at higher ISs due primarily to the decrease in their z-potentials and increase in their DLS sizes. The presence of biofilms (i.e., BS and PP) inhibited the mobility of GONPs in porous media. Physicochemical characterizations of the biofilms revealed that biofilms grown on sand surfaces decreased the z-potentials and increased the degrees of surface roughness and charge heterogeneity of collectors, and reduced the porosity and narrowed the pore sizes of packed columns, which altogether contributed to the inhibited transport of GONPs in the presence of biofilms. The experimental BTCs of GONPs were well described using a two-site kinetic retention model, and the BS biofilm and PP biofilm provided favorable retention sites for GONPs. In addition, the XMCT technique is quite promising to capture the complex microstructure and quantify parameter changes induced by biofilm growth, which will significantly provide new insights in the fate and transport of ENPs in porous media. Acknowledgments This work was supported by the National Natural Science
Foundation of China (41430752 and 41125007) and the National Basic Research and Development Program of China (2013CB934303). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.chemosphere.2016.11.040. References Berlin, J.M., Yu, J., Lu, W., Walsh, E.E., Zhang, L., Zhang, P., Chen, W., Kan, A.T., Wong, M.S., Tomson, M.B., 2011. Engineered nanoparticles for hydrocarbon detection in oil-field rocks. Energy Environ. Sci. 4, 505e509. Bradford, S.A., Kim, H.N., Haznedaroglu, B.Z., Torkzaban, S., Walker, S.L., 2009. Coupled factors influencing concentration-dependent colloid transport and retention in saturated porous media. Environ. Sci. Technol. 43, 6996e7002. Bradford, S.A., Simunek, J., Bettahar, M., Tadassa, Y.F., van Genuchten, M.T., Yates, S.R., 2005. Straining of colloids at textural interfaces. Water Resour. Res. 41, W10404. Bradford, S.A., Simunek, J., Bettahar, M., van Genuchten, M.T., Yates, S.R., 2003. Modeling colloid attachment, straining, and exclusion in saturated porous media. Environ. Sci. Technol. 37, 2242e2250. Bradford, S.A., Torkzaban, S., Walker, S.L., 2007. Coupling of physical and chemical mechanisms of colloid straining in saturated porous media. Water Res. 41, 3012e3024. Cao, Y., 2013. Interaction Mechanisms of Extraceller Polymeric Substances from Bacteria with Soil Soilds Interface and its Environmental Effects. Ph.D. Dissertation. Huazhong Agricultural University, Wuhan, P. R. China. Chowdhury, I., Duch, M.C., Mansukhani, N.D., Hersam, M.C., Bouchard, D., 2013. Colloidal properties and stability of graphene oxide nanomaterials in the aquatic environment. Environ. Sci. Technol. 47, 6288e6296. Chowdhury, I., Duch, M.C., Mansukhani, N.D., Hersam, M.C., Bouchard, D., 2014a. Deposition and release of graphene oxide nanomaterials using a quartz crystal microbalance. Environ. Sci. Technol. 48, 961e969. Chowdhury, I., Duch, M.C., Mansukhani, N.D., Hersam, M.C., Bouchard, D., 2014b. Interactions of graphene oxide nanomaterials with natural organic matter and metal oxide surfaces. Environ. Sci. Technol. 48, 9382e9390. Chowdhury, I., Mansukhani, N.D., Guiney, L.M., Hersam, M.C., Bouchard, D., 2015. Aggregation and stability of reduced graphene oxide: complex roles of divalent cations, pH, and natural organic matter. Environ. Sci. Technol. 49, 10886e10893. Clausnitzer, V., Hopmans, J., 2000. Pore-scale measurements of solute breakthrough using microfocus X-ray computed tomography. Water Resour. Res. 36, 2067e2079. rino, M., Davit, Y., Iltis, G., Debenest, G., Veran-Tissoires, S., Wildenschild, D., Ge Quintard, M., 2011. Imaging biofilm in porous media using X-ray computed microtomography. J. Microsc. 242, 15e25. Derjaguin, B.V., Landau, L.D., 1941. Theory of the stability of strongly charged lyophobic sols and the adhesion of strongly charged particles in solutions of
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Inhibited transport of graphene oxide nanoparticles in granular quartz sand coated with Bacillus subtilis and Pseudomonas putida biofilms Jian-Zhou He a, d, Deng-Jun Wang b, Huan Fang c, d, Qing-Long Fu a, d, Dong-Mei Zhou a, * a
Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China Department of Plant and Soil Sciences, University of Delaware, Newark, DE 19716, United States c State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China d University of Chinese Academy of Sciences, Beijing 100049, China b
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Effect of biofilms on the transport of GONPs was systematically examined. XMCT was used to quantitatively characterize the pore structures of packed columns. Biofilms reduced the porosity and narrowed the pore sizes of sand columns. The presence of biofilms provides favorable sites for GONPs retention/ attachment.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 March 2016 Received in revised form 30 October 2016 Accepted 1 November 2016
Increasing production and use of graphene oxide nanoparticles (GONPs) boost their wide dissemination in the subsurface environments where biofilms occur ubiquitously, representative of the physical and chemical heterogeneities. This study aimed at investigating the influence of Gram-positive Bacillus subtilis (BS) and Gram-negative Pseudomonas putida (PP) biofilms on the transport of GONPs under different ionic strengths (0.1, 0.5, and 1.0 mM CaCl2) at neutral pH 7.2 in water-saturated porous media. Particularly, the X-ray micro-computed tomography was used to quantitatively characterize the pore structures of sand columns in the presence and absence of biofilms. Our results indicated that the presence of biofilms reduced the porosity and narrowed down the pore sizes of packed columns. Transport experiments in biofilm-coated sand showed that biofilms, irrespective of bacterial species, significantly inhibited the mobility of GONPs compared to that in cleaned sand. This could be due to the Ca2þ complexation, increased surface roughness and charge heterogeneities of collectors, and particularly enhanced physical straining caused by biofilms. The two-site kinetic retention model-fitted value of maximum solid-phase concentration (Smax2) for GONPs was higher for biofilm-coated sand than for cleaned sand, demonstrating that biofilms act as favorable sites for GONPs retention. Our findings presented herein are important to deepen our current understanding on the nature of particle-collector interactions. © 2016 Elsevier Ltd. All rights reserved.
Handling Editor: Chang-Ping Yu Keywords: Graphene oxide nanoparticles Biofilm Transport Porous media Computed tomography Modeling
1. Introduction * Corresponding author. E-mail address: [email protected] (D.-M. Zhou). http://dx.doi.org/10.1016/j.chemosphere.2016.11.040 0045-6535/© 2016 Elsevier Ltd. All rights reserved.
Graphene oxide, a layered carbonaceous nanomaterial, is composed of graphene sheets and oxygen-containing functional
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groups such as epoxide, carbonyl, carboxyl, hydroxyl, and phenol (Dikin et al., 2007; Dreyer et al., 2010). In the past decade, graphene oxide nanoparticles (GONPs) have received exploding attention in many fields (e.g., biomedicine, nanoelectronics, sensors and conductive films) attributable to their unique structures and extraordinary physiochemical properties (Eda et al., 2008; Fugetsu et al., 2010; Berlin et al., 2011; Zhang et al., 2011). Nonetheless, an increasing number of studies demonstrated that GONPs are toxic to human, animal, and bacteria (Liu et al., 2011; Vallabani et al., 2011; Wang et al., 2011a; Gurunathan et al., 2013). For instance, GONPs exhibited dose-dependent toxicity to human fibroblast cells and mice by inducing cell apoptosis and lung granuloma formation (Wang et al., 2011a). Liu et al. (2011) also found GONPs showed high antibacterial activity towards Escherichia coli, which was ascribed to the membrane and oxidation stress. As the knowledge of GONPs potential risks to environment and human health remains unsound yet, a thorough understanding of the fate and transport of GONPs is critical for their benign use and risk assessment and management. GONPs display high solubility and stability in aquatic environment (Mkhoyan et al., 2009; Chowdhury et al., 2013), where biofilms are ubiquitous, representative of the physical and chemical heterogeneities in riverbank sediments or groundwater aquifers. To date, several studies have documented that biofilms play an important role on the fate and transport of engineered nanoparticles (ENPs) in granular aquatic matrixes (Tong et al., 2010; Lerner et al., 2012; Tripathi et al., 2012; Jiang et al., 2013; Xiao and Wiesner, 2013; Mitzel and Tufenkji, 2014; He et al., 2015). Findings of Tripathi et al. (2012) on the transport of four types of ENPs with different particle sizes and surface chemistries revealed that the four ENPs exhibited increased retention in the biofilmladen packed bed. Similarly, Lerner et al. (2012) reported enhanced retention of zerovalent iron nanoparticles (nZVI) in the presence of Pseudomonas aeruginosa biofilm on sand grains. Very recently, we compared the transport behaviors of GONPs mediated by biofilm and extracellular polymeric substance (EPS) in watersaturated sand columns. Our findings indicated that EPS exhibited negligible influence on GONPs transport due to effects of hydration effect and steric repulsion, whereas enhanced retention of GONPs was observed in biofilm-coated sand. We speculated that the greater retention of GONPs in the presence of biofilm is likely due to the increased surface roughness and physical straining. However, since the real three-dimensional (3D) structure of biofilms developed in porous media is still poorly understood, our explanations regarding the role of biofilm on ENPs transport are ambiguous without any direct evidence. During the past several decades, the X-ray micro-computed tomography (XMCT) technique has been successfully employed to visualize and quantify 3D microstructure of porous materials (Flannery et al., 1987). The advantages of this technique are nondestructive and time-effective compared with the traditional s, 1992). Systematic anamethods, e.g., mercury porosimetry (Fie lyses of images acquired by XMCT scanning can provide new information on pore space of specimen with respect to variables, such as soil bulk density (Petrovic et al., 1982), porosity (Zhou et al., 2013), and solutes breakthrough (Clausnitzer and Hopmans, 2000) in porous media. Researchers (Davit et al., 2011; Iltis et al., 2011; du Roscoat et al., 2014) have successfully visualized the 3D biofilms in porous media via XMCT technique. Thus, XMCT-based method is anticipated to provide novel and unique insights into the morphology of granular medium where ENPs remain direct contacts with bacterial biofilm. The overarching objective of this work was to examine the influence of biofilm on the transport of GONPs in saturated sand columns under three different ionic strengths (ISs, 0.1, 0.5 and 1.0 mM CaCl2) at neutral pH 7.2. Two representative bacteria, i.e.,
Gram-positive Bacillus subtilis (BS) and Gram-negative Pseudomonas putida (PP) were selected as model biofilms. To our knowledge, the XMCT technique was, for the first time, applied to unravel the effect of biofilms on the fate and transport of GONPs in porous media. Our findings will advance the current knowledge of the role of biofilm in GONPs transport in porous media, and thus deepen our understanding on the nature of particle-collector interactions in the subsurface environments. 2. Materials and methods 2.1. Preparation of GONPs influent suspensions The GONPs were obtained from Nanjing XFNANO Materials Tech Co., Ltd. (Nanjing, China). The manufacturer reported that the purity of GONPs were >99% (atomic force microscopy image is provided in Fig. S1, Supplementary Information). Upon receipt, the GONPs stock solution (2.0 mg mL1) was stored at 4 C. Twenty mg L1 of GONPs influents with varied ionic strengths (ISs) in calcium chloride (CaCl2) (Analytical grade, Sinopharm Co., Ltd., China) were created by diluting aliquots of the GONPs stock solution to the electrolyte solutions (0.1, 0.5, and 1.0 mM CaCl2). The resulting suspension was then mixed thoroughly followed by sonicating at 45 kHz, 100 W (KQ-300VDE, Kunshan Sonicator Co., China) over 1 h prior to the column transport experiments. All electrolyte solutions and GONPs influents were prepared using sterilized deionized (DI) water (18.2 MU cm, Millipore, Inc., USA). The pH of GONPs influents was adjusted to 7.2 using 0.1 M NaOH. 2.2. Column transport experiments Column experiments were performed in the absence and presence of biofilms formed by Bacillus subtilis (BS) and Pseudomonas putida (PP) using glass chromatography column (Shanghai Huxi Glassware Co., China) with 2.6-cm inner diameter and 20-cm in length (Zhou et al., 2011). Quartz sands (Sinopharm Chemical Reagent Co., Ltd., China) with sizes ranging from 600 to 710 mm were used as porous media for column transport experiments. Before use, the sand was thoroughly cleaned following the method of Zhou et al. (2011). To pack the vertically-oriented column, granular sands autoclaved at 121 C for 30 min were carefully added in 1e2 cm increments and then gently vibrated to eliminate any layering or air bubbles (Wang et al., 2012a). For biofilm-coated sand condition, the column was wet-packed with autoclaved sands premixed with bacterial suspension using the procedure described in our recent study (He et al., 2015) and also provided in S1, Supplementary Information (SI). Before initiating transport experiments, the packed columns were fully equilibrated with several pore volumes (PVs) of GONPsfree background electrolyte (pH 7.2) in an upward mode to establish steady hydrodynamic and chemical condition (Wang et al., 2011b). Subsequently, 3.5 PVs of the prepared GONPs influents (20 mg L1) at the desired ISs (0.1, 0.5, and 1.0 mM CaCl2) were introduced into the column using a peristaltic pump (YZП-15, Baoding Longer Precision Pump Co., Ltd., China) at a flow rate of 1.0 mL min1, followed by background electrolyte elution for 4 PVs. Column effluents were automatically collected into 15-mL sterile glass tubes at regular intervals using a fraction collector (BS-100A, Huxi Analytical Instrument Factory Co., Ltd, China), and the concentration of GONPs was immediately determined with UV/Vis spectrophotometer at the wavelength of 228 nm (He et al., 2015). A calibration curve was pre-established by diluting the 20 mg L1 GONPs influent, which was linear within the range of 0e20 mg L1 (Fig. S2, R2 > 0.999).
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2.3. Characterization of GONPs and sand collectors Several methods were used to characterize the physicochemical properties of GONPs and sand collectors that likely influence GONPs transport in porous media. Morphological property of GONPs was examined with transmission electron microscopy (TEM), and the samples were prepared by drying a droplet of GONPs suspension (20 mg L1) onto a copper TEM grid (JEM-2100, JEOL, Japan). Stability of GONPs influents was also determined by monitoring the light absorption over the time frame of the column transport experiments (3 h) and the results revealed that the GONPs influents were stable under investigated ISs (Figs. S3 and SI). The z-potential and hydrodynamic diameter were measured using a NanoBrook 90Plus PALS analyzer (Brookhaven Instruments, US). 2.4. XMCT scanning and image processing An industrial Phoenix Nanotom X-ray micro-computed tomography facility (XMCT, GE, Sensing and Inspection Technologies, GmbH, Wunstorf, Germany) was used to characterize the pore structure of columns packed with cleaned and biofilm-coated sands. The prepared column was mounted on a rotary stage and scanned at a voltage of 110 kV and an electrical current of 100 mA from different angles at same intervals. The final slices were stored in 8-bit format, which means each voxel had a value between 0 and 255 representing the attenuation coefficient of the corresponding material. The resulting voxel size was 15 15 15 mm3. A region of interest (ROI) was selected from the central part of columns to avoid artifacts at the boundary region. The image stacks were cropped to an ROI of 600 600 800 voxels, representing a volume of 9 9 12 mm3. Image processing and visualization were conducted with the open-source software ImageJ. Media filter and segmentation were conducted first. Pore size distribution (PSD) was obtained by morphological “opening” operations. Briefly, pore smaller than a certain size was removed by erosion followed by dilation using a spherical structuring element, which is called “opening”. By changing the size of the structuring element, the PSD could be derived. A detailed description about this method was reported by Schlüter et al. (2011).
3
are presented in Table 1. The calculated z-potentials of GONPs were all negative under examined pH value, in accordance with the previous literature (Stoller et al., 2008) considering that the isoelectric point (IEP) was 3 for graphene oxide. The z-potentials progressively became less negative with increasing ISs, which is in agreement with the anticipated influence of electrostatic double layer (EDL) compression (Elimelech et al., 1995). For example, the zpotential of GONPs decreased from 28.3 to 17.9 mV when the IS was increased from 0.1 to 1.0 mM (Table 1). Likewise, the same decreasing trend of z-potentials was observed for sand grains in response to increasing ISs. The presence of biofilms (i.e. BS and PP) decreased the absolute surface potential of cleaned sand to some extent, consistent with the findings documented in previous publications (Tripathi et al., 2012; He et al., 2015). For example, the zpotential of cleaned sand was 32.9 mV, while the values of BS biofilm and PP biofilm-coated sand were declined to 25.1 and 24.1 mV, respectively, in 0.1 mM CaCl2 at pH 7.2 (Table 1). The effect of solution chemistry on GONPs aggregation was also examined using dynamic light scattering (DLS) and TEM. The averaged hydrodynamic diameter (Dh) of GONPs was found to increase from 296 to 698 nm when the IS was increased from 0.1 to 1.0 mM in CaCl2 (Table 1). Additionally, DLS size change of GONPs over the time frame of the column transport experiments (i.e., 3 h) is shown in Fig. S4 in SI, which indicates that GONPs influents were relatively stable with slight ascending in DLS sizes for both 0.1 and 0.5 mM CaCl2, whereas the DLS sizes increased gradually from initial 698 nm to final 1356 nm at the investigated duration for 1.0 mM CaCl2 case. As depicted in Fig. 1, the representative TEM micrographs showed that in DI water and 0.1 mM CaCl2, the GONPs flakes were well dispersed, mostly as irregularly shaped thin flakes with few wrinkles. In contrast, at 0.5 mM CaCl2, the TEM image clearly showed GONPs flakes started to overlap and aggregate together. Particularly, significant aggregations of GONPs occurred at IS of 1.0 mM CaCl2. The aggregates were much darker in color, indicating the stacking of multiple GONPs flakes. The above observations demonstrated that high IS decreased the stability of GONPs influents, which is well-documented in the literature (Lanphere et al., 2013; Liu et al., 2013; Qi et al., 2014). 3.2. Transport of GONPs in cleaned and biofilm-coated sand
2.5. Mathematical modeling An inert tracer (bromide) experiment was conducted to obtain the pore-water velocity and dispersion coefficient, by fitting tracer breakthrough curves using the CXTFIT code (Toride et al., 1999). A one-dimensional form of the convection-dispersion equation (CDE) with two types of kinetic retention sites (Schijven and Sim unek, 2002; Bradford et al., 2003) was used to simulate the GONPs transport in the column experiments. The two-site kinetic retention model has been successfully employed to simulate the transport of GONPs in saturated quartz sand covered with iron oxides, biofilms, and extracellular polymeric substances (Wang et al., 2012a, b; He et al., 2015). For the cleaned sand column in this study, site 1 and site 2 are the surface locations of quartz sand and metal (iron or aluminum) oxide impurity, respectively; whereas, they are cleaned sand and biofilm surface location, respectively, in biofilm-coated sand column. Detailed model description is given in SI S2. 3. Results and discussion 3.1. Properties of GONPs and sand collectors Properties of GONPs influents and quartz sands in the presence and absence of biofilms at various ISs (0.1e1.0 mM CaCl2 at pH 7.2)
Fig. 2a, b and 2c present the breakthrough curves (BTCs) of GONPs in the absence and presence of biofilms, under varied solution ISs (0.1e1.0 mM CaCl2) at pH 7.2. The BTCs are plotted as normalized effluent concentration (C/C0) versus PVs. GONPs broke through at approximately 1.0 PV with the exceptions of BS biofilm and PP biofilm-coated sand columns at IS ¼ 1.0 mM. The value of C/ C0 increased gradually and did not reach a steady peak plateau. The observed asymmetric BTCs were inconsistent with the prediction by classical filtration theory (Yao et al., 1971). These results are indicative of blocking behavior, i.e., decreasing deposition rates with time. Fig. 2a shows the BTC for GONPs transport in cleaned sand in 0.1e1.0 mM CaCl2. Increasing the ionic strengths reduced the maximum effluent concentration of GONPs; that is, the value of C/ C0 dramatically decreased from 0.99 to 0.36 when ISs increased from 0.1 to 1.0 mM CaCl2. Similar results were observed in recent studies (Feriancikova and Xu, 2012; Lanphere et al., 2013; Liu et al., 2013; Qi et al., 2014). These overall phenomena can be attributed to the consistently decreased z-potential (less negative) and increased DLS sizes (Table 1), induced by increasing ISs. In comparison to cleaned sand, Fig. 2b and c shows the presence of BS biofilm and PP biofilm significantly enhanced the retention of GONPs under all experimental conditions. The normalized effluent concentrations (C/C0) were all correspondingly lower than that of
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Table 1 Properties of GONPs influents and quartz sand coated with or without biofilms, as well as the calculated height of repulsive maximum energy barrier (Fmax) and depth of attractive secondary minimum (Fmin2) according to the DLVO theory. IS (mM)
DLSa (nm)
z-potential (mV)
FbGONPs-Cleaned
FcGONPs-BS (kT)
FdGONPs-PP (kT)
(kT)
0.1 0.5 1.0
296 322 698
GONPs
Cleaned sand
BS biofilm-coated
PP biofilm-coated
Fmax
Fmin2
Fmax
Fmin2
Fmax
Fmin2
28.3 ± 1.8 22.2 ± 1.5 17.9 ± 1.9
32.9 ± 0.4 28.4 ± 0.7 28.4 ± 1.0
25.1 ± 0.8 22.0 ± 0.7 17.4 ± 0.1
24.1 ± 2.5 16.8 ± 2.6 13.5 ± 2.1
339 209 302
NAe 0.068 0.35
254 160 176
NA 0.072 0.40
241 111 120
NA 0.077 0.43
a
Average hydrodynamic diameters of GONPs, measured by DLS. Interaction energy between GONPs and cleaned, BS biofilm, or PP biofilm-coated sand, respectively, in the unit of kT (where k is the Boltzmann constant and T is the absolute temperature). e Not Applicable. b,c, and d
Fig. 1. Representative TEM images of GONPs under different ISs.
GONPs transport in cleaned sand under same solution chemistry. Similar findings were recently reported for other ENPs (e.g., ZnO nanoparticles and nZVI) transport (Lerner et al., 2012; Jiang et al., 2013). However, no discernible differences on GONPs transport were observed between BS biofilm and PP biofilm tests, which is likely due to the similar physical structures of two biofilms (discussed in Section 3.3). For example, the magnitude of C/C0 for GONPs transport in BS biofilm- and PP biofilm-coated sands ranged from 0.89 to 0.01 and from 0.89 to 0.06, respectively, with IS increasing from 0.1 to 1.0 mM CaCl2. The two-site kinetic retention model assuming Langmuirian blocking on site 2 provided a good description of BTCs (see Fig. 2 and R2 in Table 2). Table 2 summarizes the fitted parameters of k1, k1d, k2 and Smax2, as well as the Pearson's correlation coefficient (R2). The values of k2 and Smax2 all increased with ascending ionic strengths for cleaned, BS biofilm- and PP biofilm-coated sands, suggesting that mechanism controlling GONPs retention near the column inlet is sensitive to solution ionic strengths (Wang et al., 2012a, b; He et al., 2015). Meanwhile, the fitted values of Smax2 tended to increase due to the presence of BS biofilm and PP biofilm. In particular, Smax2 is proportional to the fraction of surface areas that is favorable for retention (Bradford et al., 2009; Wang et al., 2012a). These observations suggest that the presence of biofilms, irrespective of bacteria species, provide the favorable sites for GONPs retention/attachment.
3.3. Mechanisms of reduced transport of GONPs by biofilms 3.3.1. DLVO interaction energy As discussed in Section 3.1, the GONPs and sand collector surface were both negatively charged under investigated solution chemistries (Table 1). Therefore, the deposition of the negatively charged GONPs onto the cleaned, BS biofilm-, and PP biofilm-coated sands is considered to be unfavorable; namely, GONPs experience repulsive electrostatic double layer (EDL) interactions as it approaches the sand surfaces. A sphere-plate configuration was used to estimate the total interaction energy (the sum of the attractive van der Waals (VDW) and the EDL interactions) based on the classical DerjaguinLandau-Verwey-Overbeek (DLVO) theory (Derjaguin and Landau, 1941; Verwey and Overbeek, 1948). Details are given in SI S3. Table 1 summarizes the parameter values calculated based on the classical DLVO theory and Fig. 3 presents the detailed interaction energy profiles. The data in Table 1 and Fig. 3 indicated that strong primary energy barriers existed (over 111 kT, k is the Boltzmann constant and T is the absolute temperature) for all conditions tested, which impaired GONPs to deposit on the sand surfaces in the primary energy well. A slight increase of Fmax for the three conditions was observed when IS increased from 0.5 to 1.0 mM CaCl2. This is most likely due to the significant increase in DLS sizes of GONPs (from 322 to 698 nm), which would outperform the effect of z-potentials resulting from the changes in ISs. Similar
J.-Z. He et al. / Chemosphere 169 (2017) 1e8
1.0
0.1 mM 0.1 mM-fitted 0.5 mM 0.5 mM-fitted 1.0 mM 1.0 mM-fitted
(a)
0.8
C/C0
0.6 0.4 0.2 0.0 0
1
2
3
4
5
6
7
8
PV
0.1 mM 0.1 mM-fitted 0.5 mM 0.5 mM-fitted 1.0 mM 1.0 mM-fitted
(b)
1.0 0.8
C/C0
0.6 0.4 0.2 0.0 0
1
2
3
4
5
6
7
8
PV
1.0
0.1 mM 0.1 mM-fitted 0.5 mM 0.5 mM-fitted 1.0 mM 1.0 mM-titted
(c)
0.8
C/C0
0.6 0.4 0.2 0.0 0
1
2
3
4
5
6
7
8
PV Fig. 2. Observed (symbols) and fitted (lines) breakthrough curves of GONPs in cleaned (a), BS biofilm- (b), and PP biofilm- (c) coated sand columns under different ISs (pH 7.2). Error bars represent the standard deviations.
findings have been frequently reported in the literature (Fang et al., 2013; Lanphere et al., 2013; Liu et al., 2013). Additionally, the predicted depth of attractive secondary minimum (ca. 0.068 to 0.43 kT) was relatively shallow, demonstrating that deposition of GONPs in the secondary minimum (Fmin2) is anticipated to be negligible. Fig. S5 also confirmed this that only a negligible amount (0.8%e6.5%) of retained GONPs was recovered during Phrase 3 when the ionic strength was reduced to zero, i.e., the secondary minimum was eliminated in the presence of DI water (Franchi and O'Melia, 2003). Thus, based on the interpretation of classical DLVO interactions, GONPs are not expected to deposit on sand surfaces, although the attractive secondary minimum is substantially likely involved in GONPs deposition in previous literature. The noted
5
disagreement between the experimental BTCs and the DLVO prediction suggest that other factors are contributable to the retention of GONPs in the presence of biofilms under various solution chemistries. 3.3.2. Surface properties It is reported that natural organic matter (NOM) contains hydroxyl, carboxyl, and amino functional groups (Schulten and Schnitzer, 1993; Leenheer, 2007). Previous study showed that GO exhibited specific interactions with NOM via functional group association under electrostatically unfavorable condition (Chowdhury et al., 2014b). Likewise, BS and PP bacterial surfaces have identical functional groups, i.e., carboxyl, amino, phosphate, and hydroxyl related moieties (Jiang et al., 2004; Cao, 2013), which are similar to those of NOM. Hence, it is anticipated that more specific interactions occurred between GONPs and biofilms compared to cleaned sands that only include relatively ‘inert’ silanol group. GONPs interact with biofilms via H-bonds, Lewis acidbase, and p-p interactions (Hartono et al., 2009). Moreover, divalent cations (e.g., Ca2þ) destabilized GO in the presence of NOM due to charge screening and obvious bridging effect (i.e., GO-MetalNOM complexation) (Chowdhury et al., 2014b, 2015). In our study, the value of C/C0 for GONPs was much lower in 1.0 mM CaCl2 than that obtained in 50 mM NaCl (C/C0: 0.01 vs 0.24; IS: 1.0 mM vs 50 mM) (He et al., 2015) for BS biofilm-coated condition. This is largely ascribed to strong complexation between GONPs and biofilms in the presence of divalent Ca2þ. Similar findings were reported in the literature (Wang et al., 2011b; Jiang et al., 2013; Chowdhury et al., 2014a). Also, surface heterogeneities (e.g., physical roughness and charge heterogeneity) of colloids and collectors have been documented to play a vital role on colloid transport under unfavorable attachment conditions (Siegrist and Gujer, 1985; Tufenkji and Elimelech, 2005; Morales et al., 2009; Shen et al., 2013; Torkzaban and Bradford, 2016). Our recent work (He et al., 2015) revealed that biofilms developed by BS and PP bacteria used in the present study increased the physical roughness of sand collector with inhomogeneous coverage, which is consistent with the depiction of biofilm by Mitzel and Tufenkji (2014). Surface roughness created low flow velocity region (Vaidyanathan and Tien, 1988; Wang et al., 2011c), where GONPs experienced less hydrodynamic forces and torques and flow vortices. Thus, surface roughness is expected to result in greater retention of GONPs in biofilm-coated sand, consistent with recent publications (Tong et al., 2010; Lerner et al., 2012; Jiang et al., 2013). On the other hand, due to the heterogeneously covered quartz sand by biofilms (Fig. S6), coupled with more negative z-potentials of sand collectors than that of biofilms (Table 1), it is reasonable to suspect that charge heterogeneity is highly likely to affect GONPs transport. In addition, surface charge heterogeneity in the colloid population substantively exists. Wang et al. (2012c) tested this by measuring the z-potentials of Alizarin red S-labeled hydroxyapatite nanoparticle (ARS-nHAP) before and after filtering ARS-nHAP through 1-mm pore diameter glass fiber filters. They found that the z-potentials of ARS-nHAP became progressively more negative after filtration, and concluded the fraction of the ARS-nHAP population with lower z-potentials was assumed to attach preferentially at the column inlet, whereas the remaining nanoparticles experienced a slower attachment rate and greater transport potential. Similarly, a reduction in z-potentials induced by biofilm coatings would effectively decrease the repulsive interaction and increase the attractive interaction between GONPs (especially for those with less charge) and biofilms than that between GONPs and cleaned sand. These provide a plausible explanation on the enhanced GONPs retention in biofilm-coated sand.
Table 2 Summary of fitted parameters obtained from the two-site kinetic retention model based on the breakthrough curve data of GONPs, in the absence and presence of biofilms at various ISs at pH 7.2. Sand type
IS (mM)
k1a (min1)
k1db (min1)
k2c (min1)
Cleaned
0.1 0.5 1.0 0.1 0.5 1.0 0.1 0.5 1.0
1.81 1.60 0.52 1.10 1.26 1.50 0.89 2.33 7.86
1.33 1.22 0.51 0.87 0.96 1.22 0.46 1.12 7.77
9.18 4.49 1.11 4.51 5.88 2.47 7.05 8.29 2.60
BS biofilm-coated
PP biofilm-coated
a b c d e
103 102 101 102 102 101 103 102 101
Smax2d (mg g1)
R2e
0.06 1.09 2.44 0.53 1.46 118.43 0.75 1.92 25.24
0.999 0.999 0.970 0.995 0.993 0.920 0.998 0.998 0.865
First-order retention rate coefficient on site 1. First-order detachment rate coefficient on site 1. First-order retention rate coefficient on site 2. Maximum solid-phase retained concentration of GONPs on site 2. Pearson's correlation coefficient.
350
(a) 0.1 mM CaCl2
Interaction Energy (kT)
300
0.5 mM CaCl2
250
1.0 mM CaCl2
200 150 100 50 0 0
20
40
60
80
100
h (nm)
Interaction Energy (kT)
350
(b)
300
0.1 mM CaCl2
250
0.5 mM CaCl2 1.0 mM CaCl2
200 150 100 50 0 0
20
40
60
80
100
h (nm)
350
(c)
Interaction Energy (kT)
300
0.1 mM CaCl2
250
0.5 mM CaCl2 1.0 mM CaCl2
200 150 100
3.3.3. Physical straining In addition to the above mechanisms that may result in the enhanced retention of GONPs in biofilm-coated sand, physical straining, reported in many previous studies (Bradford et al., 2005, 2007; Jiang et al., 2013) is also likely to play an appreciable role in inhibiting GONPs transport in this study. It is documented that biofilms grown inside the column occupied the pore vacancy, yielding a reduction in void space (Dupin and McCarty, 2000; Liu et al., 2008). To test this hypothesis, the XMCT was used to characterize the pore sizes and porosities of packed columns before and after the biofilm formation. We extracted sub-volumes of size 600 600 800 voxels (i.e., 9 9 12 mm3) from the central part of each image for further analysis. It should be mentioned that although only PP biofilm-coated column was analyzed using XMCT, the procedure used for coating biofilm onto sand surface was wellestablished and warranted the reproducibility as per our recent work (He et al., 2015). Therefore, it is reasonable to expect that BS biofilm grown inside the column would have similar effect on the pore size distribution and cumulative porosity as PP biofilm did. Fig. 4 shows the resultant visualization of microstructure for cleaned and PP biofilm-coated sand columns. While the overall variation of micro-pore structure between selected columns cannot be visually detected (the pores discussed here were excluded those with sizes smaller than 15 mm due to resolution limitation), Fig. 5 clearly presents the difference in pore size distribution and cumulative porosity between cleaned and PP biofilm-coated sand columns. Close inspection of Fig. 5 indicated that the bulk porosity was 0.44 and 0.39 for cleaned and PP biofilm-coated conditions, respectively. Pore size distribution showed clear evidence of unimodal pattern, with pores smaller than 59.7 mm slightly increased and those larger than 59.7 mm significantly decreased in PP biofilm-coated sand as compared to the cleaned sand. In general, a lower micro-porosity is expected to result in a less mobility of water and GONPs in biofilm-coated sand. It should be noted that while the discernible pore scale is > 15 mm which is 2-orders of magnitude larger than the DLS sizes of GONPs under all the investigated solution chemistries, our findings directly prove that grown biofilm on sand surfaces would reduce the porosity and narrowed the pore sizes, thereby greatly inducing physical straining. This interprets the enhanced retention of GONPs in the presence of biofilms.
50
4. Conclusions
0 0
20
40
60
80
100
h (nm) Fig. 3. Calculated DLVO interaction energy between GONPs and cleaned (a), BS biofilm- (b), and PP biofilm- (c) coated sand as a function of separation distance (h) at various ISs (pH 7.2).
In this research, the role of biofilms, developed from Bacillus subtilis (BS, Gram-positive) and Pseudomonas putida (PP, Gramnegative) strains, on the transport of GONPs in three different ionic strengths (0.1, 0.5, and 1.0 mM CaCl2) at pH 7.2 was
J.-Z. He et al. / Chemosphere 169 (2017) 1e8
7
Fig. 4. Representative 2D and 3D visualizations of pore structures for cleaned (upper) and PP biofilm-coated (lower) sand columns.
0.5
Clean sand column PP biofilm-coated column
0.06
0.4
Porosity
0.05 0.3
0.04 0.03
0.2
0.02 0.1
0.01 0.00
Cumulative porosity
0.07
0
100
200
300
400
0.0
Effective pore diameter (um) Fig. 5. Effective pore size distribution and cumulative porosity of pore structures for a selected region (9 mm 9 mm 12 mm) within the cleaned and PP biofilm-coated sand columns.
systematically unraveled. Reduced transport of GONPs occurred at higher ISs due primarily to the decrease in their z-potentials and increase in their DLS sizes. The presence of biofilms (i.e., BS and PP) inhibited the mobility of GONPs in porous media. Physicochemical characterizations of the biofilms revealed that biofilms grown on sand surfaces decreased the z-potentials and increased the degrees of surface roughness and charge heterogeneity of collectors, and reduced the porosity and narrowed the pore sizes of packed columns, which altogether contributed to the inhibited transport of GONPs in the presence of biofilms. The experimental BTCs of GONPs were well described using a two-site kinetic retention model, and the BS biofilm and PP biofilm provided favorable retention sites for GONPs. In addition, the XMCT technique is quite promising to capture the complex microstructure and quantify parameter changes induced by biofilm growth, which will significantly provide new insights in the fate and transport of ENPs in porous media. Acknowledgments This work was supported by the National Natural Science
Foundation of China (41430752 and 41125007) and the National Basic Research and Development Program of China (2013CB934303). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.chemosphere.2016.11.040. References Berlin, J.M., Yu, J., Lu, W., Walsh, E.E., Zhang, L., Zhang, P., Chen, W., Kan, A.T., Wong, M.S., Tomson, M.B., 2011. Engineered nanoparticles for hydrocarbon detection in oil-field rocks. Energy Environ. Sci. 4, 505e509. Bradford, S.A., Kim, H.N., Haznedaroglu, B.Z., Torkzaban, S., Walker, S.L., 2009. Coupled factors influencing concentration-dependent colloid transport and retention in saturated porous media. Environ. Sci. Technol. 43, 6996e7002. Bradford, S.A., Simunek, J., Bettahar, M., Tadassa, Y.F., van Genuchten, M.T., Yates, S.R., 2005. Straining of colloids at textural interfaces. Water Resour. Res. 41, W10404. Bradford, S.A., Simunek, J., Bettahar, M., van Genuchten, M.T., Yates, S.R., 2003. Modeling colloid attachment, straining, and exclusion in saturated porous media. Environ. Sci. Technol. 37, 2242e2250. Bradford, S.A., Torkzaban, S., Walker, S.L., 2007. Coupling of physical and chemical mechanisms of colloid straining in saturated porous media. Water Res. 41, 3012e3024. Cao, Y., 2013. Interaction Mechanisms of Extraceller Polymeric Substances from Bacteria with Soil Soilds Interface and its Environmental Effects. Ph.D. Dissertation. Huazhong Agricultural University, Wuhan, P. R. China. Chowdhury, I., Duch, M.C., Mansukhani, N.D., Hersam, M.C., Bouchard, D., 2013. Colloidal properties and stability of graphene oxide nanomaterials in the aquatic environment. Environ. Sci. Technol. 47, 6288e6296. Chowdhury, I., Duch, M.C., Mansukhani, N.D., Hersam, M.C., Bouchard, D., 2014a. Deposition and release of graphene oxide nanomaterials using a quartz crystal microbalance. Environ. Sci. Technol. 48, 961e969. Chowdhury, I., Duch, M.C., Mansukhani, N.D., Hersam, M.C., Bouchard, D., 2014b. Interactions of graphene oxide nanomaterials with natural organic matter and metal oxide surfaces. Environ. Sci. Technol. 48, 9382e9390. Chowdhury, I., Mansukhani, N.D., Guiney, L.M., Hersam, M.C., Bouchard, D., 2015. Aggregation and stability of reduced graphene oxide: complex roles of divalent cations, pH, and natural organic matter. Environ. Sci. Technol. 49, 10886e10893. Clausnitzer, V., Hopmans, J., 2000. Pore-scale measurements of solute breakthrough using microfocus X-ray computed tomography. Water Resour. Res. 36, 2067e2079. rino, M., Davit, Y., Iltis, G., Debenest, G., Veran-Tissoires, S., Wildenschild, D., Ge Quintard, M., 2011. Imaging biofilm in porous media using X-ray computed microtomography. J. Microsc. 242, 15e25. Derjaguin, B.V., Landau, L.D., 1941. Theory of the stability of strongly charged lyophobic sols and the adhesion of strongly charged particles in solutions of
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