Different roles of silica nanoparticles played in virus transport in saturated and unsaturated porous media

Environmental Pollution 259 (2020) 113861

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Different roles of silica nanoparticles played in virus transport in saturated and unsaturated porous media* Yunqi Qin a, b, Zong Wen a, b, Wenjing Zhang a, b, *, Juanfen Chai a, b, Dan Liu a, b, Shengyu Wu a, b a b

Key Laboratory of Groundwater Resources and Environment, Ministry of Education, Jilin University, Changchun, 130021, China College of New Energy and Environment, Jilin University, Changchun, 130021, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 3 June 2019 Received in revised form 14 December 2019 Accepted 19 December 2019 Available online 26 December 2019

Because of the complexity of contaminants infiltrating groundwater, it is necessary to study the cotransport of contaminants in the vadose and saturated zones. To investigate the role of inorganic colloids in the transport of biocolloids through porous media, a series of experiments were performed using columns packed with sand. The Escherichia coli phage (E. coli phage) was used as the model virus and silica as the model colloid in this study. The model virus exhibited a higher degree of attachment when compared with silica under similar experimental conditions. Under unsaturated flow conditions, the degree of virus retention was higher than in the corresponding saturated flow case, regardless of the presence of silica. Mass recovery and breakthrough curve data showed that silica hindered virus transport in saturated porous media. The model virus exhibited a higher degree of retention in the presence of silica. This could be related to pore structure changes caused by aggregated virus-silica particles located within the pores of the sand. Conversely, the suspended virus retained at the airwater interface provided new retention sites for other colloids; the retention was observed to be higher in the presence of colloidal silica in the saturated columns. In the corresponding unsaturated experiments, silica was observed to play the opposite function with respect to virus transport, which demonstrated that silica facilitated virus transport in the presence of unsaturated porous media. Capillary forces were stronger than the virus-silica interactions, and inhibited the aggregation of particles. Suspended silica competes with the virus for sorption sites because of a high affinity for the airwater interface. This competition inhibits virus retention by electrostatic repulsion of like-charged particles, and concomitantly facilitates virus transport under unsaturated conditions. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Virus Silica Co-transport Column experiments

1. Introduction Nano-sized pathogenic contaminants that enter surface water bodies and groundwater systems through unmanaged wastewater discharge and irrigation pose a great risk to human health (Anders and Chrysikopoulos, 2008; You et al., 2005). The movement of pathogenic contaminants from the earth surface to groundwater occurs via the vadose zone (Bellou et al., 2015; Seetha et al., 2015; Torkzaban et al., 2006b). The infiltration of contaminants results in severely contaminated soils and groundwater, and causes great

* This paper has been recommended for acceptance by Sarah Harmon. * Corresponding author. College of New Energy and Environment, Jilin University, Changchun, 130021, China. E-mail address: [email protected] (W. Zhang).

https://doi.org/10.1016/j.envpol.2019.113861 0269-7491/© 2019 Elsevier Ltd. All rights reserved.

harm to ecological and human health. In addition, pathogenic viruses possess the same physicochemical properties as colloids (large specific surface areas and electrical doubleelayers) that can affect the movement of contaminants in the subsurface environment (Chen et al., 2018; Walshe et al., 2010; Zhang et al., 2017). Therefore, to protect groundwater resources and human health, it is essential that the transport behavior of pathogenic viruses, as well as their co-transport with other contaminants through porous media, is better understood. Complexity of contaminant migration in aquifer is mainly due to different kinds of particles or solute, and various migration environments, which will have an obviously impact on the migration of contaminants. Many contaminants in aqueous media are readily adsorbed/attached onto colloidal particles, which often act as carriers (Katzourakis and Chrysikopoulos, 2014). Previous research has focused on the co-transport of viruses and colloids though

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fractured and porous media as a function of various colloid types (Bellou et al., 2015; Syngouna et al., 2017), virus types (Syngouna et al., 2013), moisture content (Syngouna and Chrysikopoulos, 2015), and hydrochemical conditions (Walshe et al., 2010). Several mathematical models have been developed to describe the co-transport of colloids and viruses in porous media (Katzourakis and Chrysikopoulos, 2014, 2015; Seetha et al., 2015). Of particular importance is the migrationmechanisms of both virusesevarious colloids and colloidsevarious viruses are more complex in the vadose zone than in saturated porous media (Kim et al., 2010; Zhang et al., 2010). Rainfall, snowmelt, and human activities (e.g., irrigation and artificial recharge) can result in the redistribution and remobilization of contaminants by transient flow in the vadose zone, thereby increasing the risk of groundwater contamination (Wei et al., 2010). Moisture content appears to exert the greatest control on colloid transport and retention in porous media (Flury and Aramrak, 2017; Kamrani et al., 2018). In addition to retention mechanisms (e.g., straining, blocking, and ripening) in saturated porous media, other potential retention sites in the gaseous phase in unsaturated porous media have also been discussed by Mitropoulou et al. (2013). Torkzaban et al. (2006b) suggested that transient flow conditions and variable water saturation may result in the continuous redistribution of colloids between the solidewater interface (SWI), the airewater interface (AWI), and the airewateresolid (AWS) interface. Colloid attachment to the AWI is often considered to be irreversible because of the electrostatic and capillary forces that hold the colloids at the interface (Bai et al., 2017). Capillary forces are known to be important for colloid attachment at the AWI, as well as for film straining (Syngouna and Chrysikopoulos, 2015). In fact, the co-transport mechanism of two or more particles become more complicated, which is due to the change of the interaction between particle-particle and the interaction between particleseinterface (Seetha et al., 2015). Katzourakis and Chrysikopoulos (2014) indicated that viruses can be suspended in the aqueous phase, attached onto suspended colloid sand the solid matrix, and attached onto colloids previously attached on the solid matrix. It is necessary to account for the role of colloids in virus transport which can lead to serious underestimation or overestimation of the travel distances of groundwater pathogenic. This type of research not only explores the mechanisms of contaminant co-transport, but also provides a theoretical basis for the pollution remediation that is required. Highly dispersible colloidal silica is commonly used to enhance the mobility of strongly absorbed contaminants (Li et al., 2019). This paper mainly focuses on the influence of silica on the transport and retention behavior of viruses in water-saturated and unsaturated porous media under a steady flow rate. The specific objectives were to: (1) examine the effect of silica on virus activation and on the stability of virus-silica systems; (2) explore the influence of silica on the transport of viruses in water-saturated and unsaturated porous media; and (3) identify the main deposition mechanisms of the virus-silica system in porous media with different water saturations. This study will serve as a useful reference for the protection of groundwater supplies from pathogenic contamination and for the assessment of pathogen risk in groundwater for other colloids. A co-transport model of virusesecolloids and the effect of extended DLVO theory, capillary interactions between viruses-colloids, the virus-colloid sorption rate, and other virus-various colloid interactions will be addressed in future research. 2. Materials and methods 2.1. Preparation of viral and silica suspensions The phage vB_EcoM-ep3 used in this study was taken from

sewage and artificial lakes in the Changchun area (Zhang et al., 2017). The host bacterium of phage vB_EcoM-ep3 was E. coli O786, which was purified by the College of Veterinary Medicine, Jilin University (Lv et al., 2015). The method used to incubate the E. coli phage has been described in previous studies (Zhang et al., 2017). Viral suspensions were prepared by diluting virus stock suspensions with sterile deionized (DI) water. Coliphage concentrations have been reported to range widely in polluted waters (e.g., in sewage water the coliphage concentration may range from 10 to 107 pfu/mL) (Snowdon et al., 1989; Syngouna et al., 2013). In the present study, the initial viral suspension concentration was ~106 pfu/mL, and was used to evaluate virus transport behavior through a sand column. Inorganic colloidal suspensions were prepared using commercial silicon dioxide (Aladdin Reagents). Silica microspheres (5.59% aqueous dispersion) were diluted with DI water to achieve the desired silica suspension concentration (10 and 20 mg/L) (Zhou et al., 2017b). In addition, sterile DI water was used as the aqueous solvent for the experiments to ensure that the resultant conditions did not interfere with virus viability/inactivation and to eliminate the influence of other factors on the experiment (Chrysikopoulos and Syngouna, 2012). 2.2. Virus-silica interactions The inactivation of viruses in the presence and absence of silica was studied in batch experiments. The experimentation and data are listed in Supplementary Material Table S2. The experiment was conducted at a set temperature of 10
C to reflect the subsurface environment, and the longest transport experiment period was 10 h. Schijven and Hassanizadeh (2000) indicated that temperature is the most important factor that influences the inactivation of viruses. Inactivation is virus-specific and almost independent of adsorption. The inactivation of E. coli phages can be ignored according to the results of a series of inactivation experiments conducted by the College of Veterinary Medicine, Jilin University (Lv et al., 2015; Zhang et al., 2017). Batch experiments in the presence of silica indicated that no significant virus inactivation was expected under the present experimental conditions. 2.3. Porous media The average grain diameter of the natural sand used was 0.425 mm. The sand was collected from an artificial recharge site (Tai’an, China). The natural sand composition was determined as: 9.44% Al2O3, 13.26% Fe2O3, and 77.3% SiO2 (Li et al., 2019). The estimated porosity of the porous media, measured by mass, ranged from 0.38 to 0.40. To remove impurities from the surface, the sand was washed in HNO3 (70%) and NaOH (0.1 M) for 4 h. Thereafter, the sand was rinsed thoroughly with DI water until the pH of the water was neutral. The prepared sand was dried in an oven at 121
C for 20 min and then stored in screw-cap sterile beakers until required. 2.4. Column experiments A schematic of the equipment is shown in Fig. 1. All experiments were performed using a Plexiglas column with a length of 15 cm and an internal diameter of 5 cm. For the saturated column experiments, suspensions were introduced vertically from the top of the column using a peristaltic pump. Because of the relatively small size of the viruses used in this study, the influence of gravity was assumed to be negligible (Chrysikopoulos and Syngouna, 2014). For the unsaturated column experiments, two peristaltic pumps at the column inlet and outlet were used to regulate the column moisture content and to control the downward flow rate. To prepare the unsaturated column

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For the concentration of virus-silica complex, the concentration of the mixed suspension was tested to ensure mixture formation in suspension based on previously measured particle sizes (virus, silica, and virus-silica). Then, the concentration of the mixed suspension (CT) was tested using the double-layer overlay method. The 2.5 ml mixed suspension was passed through the filter membrane (particle size ¼ 450 nm, virus size ¼ 321.8 nm, complex size > 500 nm). The filtered suspension contains suspended viruses and silica. The double-layer overlay method has selectivity. Thus, the concentration of the filtered suspension can be considered as the suspended virus concentration (Cv). The complex concentration (Cc) ¼ CTCv. The suspended virus concentration tests were done in triplicate and the results were averaged. 3. Transport data analysis Fig. 1. Schematic diagram of the experimental setup.

conditions, an initially saturated column was drained for ~4 h. The target moisture content (80% water saturation) was obtained by making the outflow rate 5% higher than the inflow rate (Esfandyari et al., 2015). The moisture saturation percentage was calculated from the ratio of q (water-filled porosity) to the total porosity. Two time-domain reflectometry (TDR) probes (Soilmoisture Equipment Corp., Santa Barbara, CA) were used to measure water saturation. The capillary pressure head was measured using two miniature stainless steel tensiometers (Chemiquip Products Corp., West New York, NJ) (Torkzaban et al., 2006a). The tensiometer and TDR probe data were collected and monitored using a computer. For the single particle transport experiments, the colloid suspensions (viral or silica) were pumped through the column for three pore volumes (PVs, stage І), followed by sterile DI water for 10 PVs (stage ІІ). For the co-transport experiments, a mixed suspension of viruses (106 pfu/mL) and silica nanoparticles (10 and 20 mg/L) was injected simultaneously. The constant flow rate was 5 ml/min. The movement of groundwater under natural conditions is slow; the high pore water velocities employed in the present study represent site remediation processes under forced flow conditions (Syngouna et al., 2017). Effluent samples were taken at 20 min intervals (samples were collected at 1 h intervals for later experiments) using an automatic fraction collector (Huxi analytical instrument Corp., Shanghai Huxi, CBS-A100). The entire packed column and glassware used for the experiments were sterilized in an autoclave at 121
C for 20 min. A potassium iodide (KI) tracer solution (3 mg/L) was used for tracer experiments. The tracer solution was substituted for the colloids and used to define the water flow characteristics in the columns. 2.5. Sample analysis The E. coli phage, vB_EcoM-ep3, was assayed using the doublelayer agar method (Chem, 1959). This method can effectively determine the titer of bacteriophages, and the counting accuracy meets the requirements of this study. The details of this method have been documented by Zhang et al. (2017). The optical density of the colloidal silica was analyzed at a wavelength of 340 nm (Fujita and Kobayashi, 2016), using a UV spectrophotometer (UV-1800, SHIMZU, Japan), to monitor the colloidal silica concentrations in the effluent throughout the experiment. The colloidal silica concentrations were determined using the procedures outlined by Wang et al. (2016). The KI concentration in the effluent was determined every 5 min using a UV spectrophotometer and a wavelength of 280 nm (Liu et al., 2016).

3.1. The classical colloid filtration theory The classical colloid filtration theory (CFT) was used to quantitatively compare the attachment of viruses, silica, and virus-silica systems at the media surface in the laboratory-scale transport experiments. Details of the CFT calculations can be found in the Supplementary Material. 3.2. Mathematical model for colloid transport and deposition A mathematical model was used to describe the simultaneous transport (co-transport) of viruses and colloids in homogeneous porous media with uniform flow. The model accounts for the migration of individual virus transport and virus transport in the presence of silica under saturated and unsaturated conditions. Details of the model are provided in the Supplementary Material. 4. Results and discussion 4.1. Characterization of the virus The virus was characterized using a transmission electron microscope (Lv et al., 2015) and is shown in the Supplementary Material (Fig. S1). The individual virus has a hexagon head (diameter of 53 ± 2 nm) and a long tail (107 ± 3 nm). The virus was characterized using anatomic force microscope (AFM) as shown in Fig. 2. To obtain statistics on the individual virus particle diameter, two representative regions were selected for analysis, and are shown in Fig. 2a. The spherical particles were of nonuniform size and the diameters were mainly in the order of 89 ± 2 nm. It was hypothesized that the differences were caused by the retractable tail, which results in virus morphologies being altered to a spherical particle when results are compared with SEM images. The wettability of the virus was investigated using DSA100 contact angle measurements. Results show that the virus used in this study was hydrophilic, and that the contact angle (left:66.8, right:66.26) < 90
. An isoelectric point for the virus of about 4.37 was obtained using the method described by Zhu et al. (2015). Details of the contact angle and isoelectric point measurements for the virus are given in the Supplementary Material. 4.2. The hydrodynamic sizes and zeta potentials of the colloid The average hydrodynamic sizes and zeta potentials of the virus, silica, and virus-silica system were measured using a Malvern Zetasizer. The results are given in Fig. 3 and the Supplementary Material (Table S1). The hydrodynamic size of the virus used in this study was 321.8 nm, as shown in Fig. 3a, which suggested aggregation of the

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Fig. 2. (a) Two-dimensional topographic AFM image of the virus on the micasurface; (b) Three-dimensional topographic AFM image; (c) Section analysis along the white line in (a).

Fig. 3. Particle size distribution for the virus and virus-colloidal silica systems at different colloid concentrations.

virus in the viral suspension. The zeta potential of virus was 24.70 mV. The colloid absolute zeta potential, which was <30 mV, was considered typical for an unsteady state (Tourinho et al., 2012). Thus, the negatively-charged virus zeta potential indicated that the system was in an unsteady state, which can also be used to explain the aggregation of the virus particles observed in

the suspension. The physical and chemical properties of silica have been previously investigated by our group (Wang et al., 2016; Zhou et al., 2017a). The previous electrokinetic measurements revealed that the zeta potential of silica was negatively-charged across various pH and IS conditions. Wang et al. (2016) reported that the zeta potential was 27.4 mV and the hydrodynamic size was

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372.4 nm for a 20 mg/L colloidal silica suspension at pH 7.4. In the virus-silica system (Fig. 3b and c), the hydrodynamic size is increased and there is only one peak, which suggests the aggregation of virus-silica particles in mixed suspension. Silica particles were easily bound to the virus particles in a co-existent system, which resulted in an increased particle size. The hydrodynamic size ranged from 513.4 nm to 692.5 nm when the silica concentration in the suspension increased from 10 to 20 mg/L. This implies that increasing the silica concentration results in a higher binding capacity of the virus. When compared with the non-silica system, the absolute zeta potential of the virus-silica system (aggregated particles) exhibited an indistinct increasing trend. The zeta potential values ranged from 26.13 ± 1.45 mV to27.83 ± 2.15 mV as the silica concentration in the suspension

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increased from 10 to 20 mg/L. The silica concentration was observed to exhibit a negligible effect on the zeta potential of the virus-silica system. The absolute zeta potential of the particles was <30 mV and the aggregated particles were in an unsteady state condition. 4.3. Transport experiments Normalized breakthrough data collected from the transport experiments in the presence of the tracer (KI), virus, and silica, as a function of PV, under saturated (q ¼ 100%) and unsaturated (q ¼ 80%) conditions, are presented in Fig. 4. The corresponding transport experiment data analysis is listed in Table 1 and fitted parameters were shown in Table 2.

Fig. 4. Breakthrough curves (BTCs) for the tracer (KI), virus, and silica in saturated and unsaturated columns.

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Table 1 Column experiment conditions and calculated results. Experiment

Initial concentration

Transport experiment Virus 106 pfu/mL Virus 106 pfu/mL Silica 10 mg/L Silica 10 mg/L Co-transport experiment Virus-Silica (106 pfu/mL)-(10 Virus-Silica (106 pfu/mL)-(10 Virus-Silica (106 pfu/mL)-(20 Virus-Silica (106 pfu/mL)-(20

mg/L) mg/L) mg/L) mg/L)

q (%)

Mr1 (%)

Mr2 (%)

Retention (%)

a

100 80 100 80

55.65 32.47 74.01 48.49

3.40 0.74 10.80 9.09

40.95 66.79 15.20 42.42

1.55 2.18 3.89 1.02

   

101 101 102 101

8.19 1.94 2.17 9.52

   

102 102 102 102

100 80 100 80

47.13 40.34 41.43 47.74

12.47 11.33 12.85 4.79

40.40 48.33 45.72 47.48

1.37 1.79 1.62 2.03

   

101 101 101 101

7.23 1.16 8.56 1.13

   

102 102 103 102

katt (1/s)

q is the moisture content under experimental condition; Mr1(Stage I) is the relative mass recovery during the virus injection process; Mr2(Stage II) is the relative mass recovery during the sterile deionized (DI) water washing process; a is the particle attachment efficiency; and katt is the attachment rate coefficient.

Table 2 Fitted values of model parameters for the experimental data. Experiment

Concentration

Transport experiment Virus 106 pfu/mL Virus 106 pfu/mL Silica 10 mg/L Silica 10 mg/L Co-transport experiment Virus-Silica (106 pfu/mL)-(10 Virus-Silica (106 pfu/mL)-(10 Virus-Silica (106 pfu/mL)-(20 Virus-Silica (106 pfu/mL)-(20

mg/L) mg/L) mg/L) mg/L)

Va

qb

Dx

k1

k2

R2

4.62 3.85 4.62 3.85

100 80 100 80

0.57 0.38 0.57 0.38

0.13 0.23 0.12 0.27

0.0001 0.0001 0.0001 0.0090

0.81 0.82 0.95 0.95

4.62 3.85 4.62 3.85

100 80 100 80

0.65 0.38 0.65 0.38

0.16 0.17 0.20 0.15

0.0036 0.0001 0.0001 0.0001

0.63 0.75 0.51 0.68

Dx is the dispersion coefficient (cm2 min1); k1 is attachment coefficients (1/s); k2 is detachment coefficients (1/s); R2 is regression linear parameters. a V is the Darcian velocity (cm min1) defined as following: q ¼ Q/S with Q the total flow and S the section of the column. We can then estimate the pore water velocity (Vm) in the mobile region as follows: Vm ¼ q/qm. b The water content (q) was determined as the ratio of the water volume in the column Vw to the total volume of the column:q ¼ Vw/Vt。Vw is the volume occupied by water in the column, Vt is the total volume of the column. These volumes were estimated by weighting.

The tracer hysteresis reached a peak concentration, shown in Fig. 4b, with decreasing moisture content, indicating that the additional AWI introduces complexity to the water flow path in unsaturated columns (Fujita and Kobayashi, 2016). Furthermore, non-uniform wetting results in a heterogeneous water distribution, which induces preferential flow under unsaturated flow conditions (Kamrani et al., 2018). As shown in Fig. 4, virus and silica retention in saturated conditions was less than that in unsaturated conditions. This could have been caused by the influence of additional mechanisms in unsaturated conditions. When compared with the saturated conditions, the regions of stagnant flow are enhanced within the pore structure as water saturation decreases (Torkzaban et al., 2006a); this allows additional virus particles to remain in the sand column. In the present study, the colloid particles, the sand surface, and the AWI exhibited a negative charge when the pH of the solution was 7.4 (Li and Somasundaran, 1991; Torkzaban et al., 2006a; Yang et al., 2001). Thus, the electric repulsion force between these particles and the interfaces (SWI, AWI) inhibit virus deposition. While a degree of retention was observed, possibly as a result of non-DLVO Lewis acid-base interactions, hydrogen bonds may be partially responsible for the observed retention (Wang et al., 2016). Capillary potential forces are significantly larger than the electric doublelayer repulsive forces, and thus can move the colloid to within the vicinity of the grain surface (Syngouna and Chrysikopoulos, 2015), and result in higher colloid retention in unsaturated columns. Wang et al. (2012) reported that surface roughness, mainly in the form of large valleys on sand grains, can locally increase the

energy barrier as well as the depth of the secondary energy minima (DLVO), which would allow additional retention of particles in the secondary energy minima. Wan and Tokunaga, 1997 and Torkzaban et al. (2008) indicated that the deposition of colloids increased with decreasing water content, and that this can be attributed to pore and film straining. Furthermore, viruses are too small in size to cause straining. CFT was used to predict the behavior of colloid particles during transport processes. Table 1 shows the a, katt, and Mr of particles for both transport and co-transport experiments under saturated conditions and unsaturated conditions. The katt values were 8.19  102 and 1.94  102 for the viruses that passed though the saturated and unsaturated sand columns, respectively. The values indicate that the retention capacity of the viruses on the SWI increased as water saturation decreased, which suggests that attachment on the AWI and film straining may be the retention mechanisms for viruses in the unsaturated column. Silica particles exhibited poor attachment to solid surfaces, as shown in Table 1. The observed higher silica retention when the water saturation was 80% was principally related to the silica particles being trapped at the stagnation region of the pore space (Fujita and Kobayashi, 2016). When the transport behavior of the virus (biocolloid) and silica (inorganic colloid) though the columns (Fig. 4) are compared, the virus exhibits higher attachment under both saturated and unsaturated conditions. Because bio-colloids are living organisms, they exhibit a more complex transport behavior when compared with inorganic colloids. The deposition mechanisms of bio-colloidal viruses in porous media are dependent on colloid stability as well as biological characteristics (Chattopadhyay and Puls, 2000; Sen, 2011). Colloid surface roughness may be a reason for the increased attachments of viruses when compared with silica nanoparticles (Chou et al., 2015; Dylla-Spears et al., 2017). The virus used in this study has a isometrically hexagonal head and a contractile tail (Lv et al., 2015) and Shen et al. (2019), which indicates that protruding asperities on viruses can decrease interaction energy barriers and primary minimum depths, and also decrease adhesion. The spherical silica particles used in this study have a smooth surface, which causes reduced attachment of silica when compared with viruses. In addition, Syngouna and Chrysikopoulos (2011) indicated that in their study, grain surface area, angularity, and roughness may have contributed to physicochemical filtration and bio-colloid retention. 4.4. Co-transport experiments The normalized breakthrough data of the virus collected from co-transport experiments, as a function of PV, under both saturated and unsaturated conditions, are presented in Fig. 5. The

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Fig. 5. BTCs of the virus-silica systems as a function of silica concentration in saturated and unsaturated columns.

corresponding data analysis values for the virus from the cotransport experiments are listed in Table 1 and fitted parameters were shown in Table 2. The main purpose of the experiment was to explore the effect of the presence of silica on virus migration. Thus, Mr represents the summed viral concentration (suspended virus and virus-silica particles) of the effluent examples. As would be expected, the virus BTCs occur earlier in the presence of silica for the saturated experiments (within 0.5 PV), while the corresponding BTCs are retarded for the unsaturated experiments (within 1 PV). These observations are also related to then onuniform wetting conditions, as discussed in Section 4.3. As shown in Table 1, the mass recovery of the virus in unsaturated conditions was higher than that in the saturated columns, regardless of the presence of silica. Additionally, silica appears to play the opposite role in virus transport under saturated and unsaturated conditions (Fig. 5). For the saturated experiments, Mr1 for the virus was 55.65%, 47.13%, and 41.43%, when the silica concentration was 0, 10, and 20 mg/L, respectively. The results demonstrate that the presence of silica in the suspensions hinders virus migration through sand columns, and that virus transport decreased as a function of silica concentration. However, the peak values of the BTCs fluctuate greatly in the presence of silica in saturated conditions (Fig. 5a and b). This represents an obvious difference from the BTCs in the absence of silica under the same conditions. It is speculated that the fluctuating BTCs are related to the migration behavior of both the free virus and the attached virus (virus-silica aggregation particles). As discussed in Section 4.2, virus-silica particle systems were unstable when zeta potentials <30 mV. Several colloid-virus particles

may be detached because of hydrodynamic shear (Zhang et al., 2017). The migration of the suspended virus was faster than the virus-silica particles though the saturated sand columns. Therefore, the different arrival times of the suspended virus and the virussilica particles at the outflow may have caused slight fluctuations in the BTCs for the saturated experiments. This demonstrates that straining caused by aggregated particles was probably derived from the dominant mechanism for particle retention during the initial transport period. Two co-transport experiments were carried out under the same experimental conditions to verify this supposition and to evaluate the transport behavior of the suspended virus and virus-silica particles in co-transport. As shown in Fig. 6, the mass recovery of virus-silica particles was less than that of the virus suspension under saturated conditions. The parallel experiments for the co-transport experiments are shown in Fig. 5. For the experiment using only viruses under saturated conditions, the a was 1.55  101 and katt was 8.19  102. In contrast, when only silica was used in the experiment under the same experimental conditions, the values of a (3.89  102) and katt (2.17  103) were significantly lower. The calculation results suggest that the virus is more likely to be retained on the surface of the sand under the same simulated conditions. The fitted attachment coefficients k1 (Table 2) include attachment to both solidwater and air-water interfaces. However, the simulation results could not permit to identify in which kind of interface virus is more or less retained. Besides, silica is assumed to be a type of medium surface; that is, viruses affected by the presence of silica attached on the silica surface. As shown in Table 2, higher k1 values were obtained in the presence of silica compared to the absence of silica

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Fig. 6. Transport behaviors of the suspended virus and virus-silica particles in the cotransport experiments.

for the virus experiments. This suggests that the presence of silica increases viral deposition, in accordance with the observed BTCs at column scale. Although repulsive colloid-colloid interactions may inhibit retention, viruses with positively charged tails could act as retention sites for colloids. The virus tail structure (tail tube and tail fiber) has a net positive charge, while the colloidal virus has a negative charge as a whole (Zhang et al., 2017). This phenomenon might be caused by the negatively charged head playing a larger role than the positively charged tail (Penrod et al., 1996). Thus, retained viruses may act as new retention sites for other suspended colloids and lead to enhanced retention. Zhang et al. (2010) indicated that aggregated particles located within the small pores alter the pore structure. Additionally, silica-virus particles clogged the pores, which may have promoted straining. In co-transport column experiments, the virus adsorption mechanism varies depending on the virus, and is significantly influenced by the colloid characteristics (Bellou et al., 2015; Katzourakis and Chrysikopoulos, 2014; Syngouna and Chrysikopoulos, 2016). The saturated co-transport experiments, conducted by Chowdhury et al. (2012), suggested that higher human adenovirus retention occurred in the presence of clay colloids and TiO2 NPs because of substantial aggregation or hetero-aggregation. The degree of aggregation may increase during an initial pseudo-equilibrium period. However, the particles subsequently gradually detach, which is consistent with the observations made in this study. For the unsaturated experiments, the virus Mr1 values were 32.47%, 40.43%, and 47.74% when the silica concentration was 0, 10, and 20 mg/L, respectively. Lower virus retention in the presence of silica suggested that silica facilitates virus transport under unsaturated conditions. Fujita and Kobayashi (2016) reported that silica particles trapped in the straining regions and retention at the AWI are the main retention mechanisms for unsaturated columns.

Capillary forces are several orders of magnitude larger than the virus-silica interactions under the unsaturated transport process. Silica-virus particles may be detached by capillary forces from the suspended virus and silica. It can be speculated that suspended silica and the virus are the main components in the transport process. Suspended silica competes with the virus for sorption sites during the transport process. The studies by Kobayashi et al. (2005) suggested that the repulsive force between silica particles (pH 7.4 solution) is sufficiently large, and consequently the lateral interaction forces between the deposited silica particles and the suspended silica particles inhibit further silica deposition. The occupation of retention sites (AWI) by silica during the early injection stage in unsaturated column experiments inhibits virus retention by electrostatic repulsions of like-charged particles (Zhang et al., 2010), which facilitates virus transport under unsaturated conditions. The order in which the virus and silica attach to the interface may affect the deposition of the two particles because of the heterogeneous surface charge of the virus. As shown in Fig. 5, virus retention decreased as a function of silica concentration in the suspension for the co-transport column experiments. The influence of silica concentration on virus transport is related to the AWI because silica occupies a higher degree of the retention sites. Conversely, the calculated a for the virus was 2.18  101and 1.79  101 when the silica concentration was 0 and 10 mg/L, respectively, which indicates that the presence of silica also competes with the virus for sorption sites on the sand grains. However, the calculated a value for the virus was 2.03  101when the silica concentration was 20 mg/L, which may be related to the deposited viruses acting as new sorption sites for suspended virus particles. As shown in Table 2, lower k1 values were obtained in the presence of silica compared to the absence of silica for the virus experiments, in accordance with the observed BTCs at column scale. During the sterile DI water washing process, there was no significant release of the virus, which suggests an irreversible virus deposition process at the interfaces. This irreversible process may be related to the virus attaching tightly at the interfaces because of the capillary potential energy, which is several orders of magnitude greater than the DLVO potential energy (Syngouna and Chrysikopoulos, 2015). To validate our analysis, the media (after virus, silica, and virus-silica transport experiments) were analyzed using SEM, and the results are shown in the Supplementary Material (Fig. S5). The SEM observations show that the majority of the deposited particles were in a state of aggregation under saturated conditions, but in a dispersed state under unsaturated conditions. These observations also indicate that capillary forces may inhibit the clustering of particles. It is difficult to distinguish between the particles of silica and viruses of aggregation under co-transport. Consequently, the SEM images were only used to represent the dispersion of particles at the interface of the virus, silica, and virussilica particles under different saturation conditions. In unsaturated co-transport experiments conducted by Syngouna and Chrysikopoulos (2015), clay particles (KGa-1b) hindered the transport of fX174 under saturated conditions, while the system facilitated the transport of fX174 under unsaturated conditions, which is in agreement with the results presented in the present study for virus and silica systems. The authors concluded that KGa-1b possess a greater hydrophobicity (Chrysikopoulos and Syngouna, 2012), and a stationary AWI under steady-state flow conditions in the presence of a strong force, and can overcome colloidal aggregation with settling dominating colloid dispersion and mobility in porous media (Shang et al., 2009; Thorsten et al., 2014). The silica used in the present study exhibits hydrophobic interactions, which can explain the observations that silica facilities virus transport in unsaturated sand columns and inhibits virus transport in saturated sand columns.

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5. Conclusions The influence of silica NPs and water saturation on virus transport in porous media was examined in this study. Water saturation was observed to have the greatest relative impact on the virus, silica, and virus-silica systems in sand columns. The data from the transport experiments indicated that non-uniform wetting results in an obvious virus and silica hysteresis, with peak concentrations being a function of decreasing moisture content. Virus instability is considered to result in larger particle aggregates during the migration process, thus resulting in a higher degree of retention when compared with silica. Silica particles are principally retained at the AWI and the straining region under unsaturated conditions. The data from the co-transport experiments revealed that silica hindered virus transport in the saturated sand columns, but facilitated virus transport in the unsaturated sand columns. In the saturated co-transport experiments, the virus-silica systems resulted in a high degree of particle aggregation during the migration process, with the particles being located at the pores. This concomitantly alters the pore structure, and consequently results in larger virus retention. In the unsaturated co-transport experiments, silica competes with the virus for sorption sites at the AWI. The occupation of retention sites by silica at the AWI during the early stages of injection in the unsaturated column experiments inhibits virus retention through the electrostatic repulsion of like-charged particles, and thus facilitates virus transport. This study investigated virus transport and deposition mechanisms though porous media in the presence of silica NPs, and provides a platform for assessing the fate, transport, and risk of viruses in the presence of NPs. Acknowledgments This work was supported by the National Natural Science Foundation of China (41877175), Natural Science Foundation of Jilin province, China (20190201112JC) and the 111 Project, China [B16020]. The authors appreciate the editors and reviewers who provided valuable advice that greatly improved this paper. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.envpol.2019.113861. References Anders, R., Chrysikopoulos, C.V., 2008. Transport of viruses through saturated and unsaturated columns packed with sand. Transp. Porous Media 76 (1), 121e138. Bai, H., Cochet, N., Pauss, A., Lamy, E., 2017. DLVO, hydrophobic, capillary and hydrodynamic forces acting on bacteria at solid-air-water interfaces: their relative impact on bacteria deposition mechanisms in unsaturated porous media. Colloids Surfaces B Biointerfaces 150, 41e49. Bellou, M.I., Syngouna, V.I., Tselepi, M.A., Kokkinos, P.A., Paparrodopoulos, S.C., Vantarakis, A., Chrysikopoulos, C.V., 2015. Interaction of human adenoviruses and coliphages with kaolinite and bentonite. Sci. Total Environ. 517, 86e95. Chattopadhyay, S., Puls, R.W., 2000. Forces dictating colloidal interactions between viruses and soil. Chemosphere 41 (8), 1279. Chem, A., 1959. Interscience publishers. Anal. Chem. 22 (4057), 139e140. Chen, F.M., Yuan, X.M., Song, Z.F., Xu, S.P., Yang, Y.S., Yang, X.Y., 2018. Gram-negative Escherichia coli promotes deposition of polymer-capped silver nanoparticles in saturated porous media. Environ. Sci. Nano 5 (6), 1495e1505. Chou, K.S., Chen, X.Y., Lai, I.H., 2015. Surface roughness on adhesion of silver colloids to a polyimide substrate. J. Adhes. 92 (6), 151006111658005. Chowdhury, I., Cwiertny, D.M., Walker, S.L., 2012. Combined factors influencing the aggregation and deposition of nano-TiO2 in the presence of humic acid and bacteria. Environ. Sci. Technol. 46 (13), 6968e6976. Chrysikopoulos, C.V., Syngouna, V.I., 2012. Attachment of bacteriophages MS2 and FX174 onto kaolinite and montmorillonite: extended-DLVO interactions. Colloids Surfaces B Biointerfaces 92 (92), 74e83.

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