Influence of Bisphenol A on the transport and deposition behaviors of bacteria in quartz sand

Accepted Manuscript Influence of Bisphenol A on the transport and deposition behaviors of bacteria in quartz sand Dan Wu, Lei He, Ruonan Sun, Meiping Tong, Hyunjung Kim PII:

S0043-1354(17)30368-8

DOI:

10.1016/j.watres.2017.05.011

Reference:

WR 12890

To appear in:

Water Research

Received Date: 23 December 2016 Revised Date:

28 April 2017

Accepted Date: 6 May 2017

Please cite this article as: Wu, D., He, L., Sun, R., Tong, M., Kim, H., Influence of Bisphenol A on the transport and deposition behaviors of bacteria in quartz sand, Water Research (2017), doi: 10.1016/ j.watres.2017.05.011. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Influence of Bisphenol A on the Transport and Deposition Behaviors

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of Bacteria in Quartz Sand

Dan Wu†, Lei He†, Ruonan Sun†, Meiping Tong†,∗∗, and Hyunjung Kim†† †. The Key Laboratory of Water and Sediment Sciences, Ministry of Education;

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College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, P. R. China

.Department of Mineral Resources and Energy Engineering, Chonbuk

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National University, Baekje-daero, Deokjin-gu, Jeonju-si,Jeollabuk-do

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54896, Republic of Korea

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Corresponding author: Tel: +86 10 62756491; Fax: +86 10 62756526; E-mail address: [email protected] (M. Tong)

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Abstract The influence of Bisphenol A (BPA) on the transport and deposition behaviors of

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bacteria in quartz sand was examined in both NaCl (10 and 25 mM) and CaCl2

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solutions (1.2 and 5 mM) by comparing the breakthrough curves and retained profiles

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of cell with BPA in suspensions versus those without BPA. Gram-negative

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Escherichia coli and Gram-positive Bacillus subtilis were employed as model cells in

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the present study. The extended Derjaguin-Landau-Verwey-Overbeek interaction

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energy calculation revealed that the presence of BPA in cell suspensions led to a lower

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repulsive interaction between the cells and the quartz sand. This suggests that,

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theoretically, increased cell deposition on quartz sand would be expected in the

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presence of BPA. However, under all examined solution conditions, the presence of

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BPA in cell suspensions increased transport and decreased deposition of bacteria in

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porous media regardless of cell type, ionic strength, ion valence, the presence or

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absence of extracellular polymeric substances. We found that competition by BPA

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through hydrophobicity for deposition sites on the quartz sand surfaces was the sole

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contributor to the enhanced transport and decreased deposition of bacteria in the

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presence of BPA.

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Keywords: Bacteria Transport; Biophenol A; Site competition; Quartz sand;

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Interaction force.

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1.

Introduction Bisphenol A (BPA) is widely used in various products such as epoxy resins,

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polycarbonate plastics, food cans, and dental composites/sealants (Staples et al., 1998).

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The extensive application of BPA in various types of production leads to the high BPA

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level in industrial effluents (Fukazawa et al., 2001; Lee and Peart, 2000) and landfill

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leachate in various countries (Asakura et al., 2004; Kalmykova et al., 2013; Kurata et

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al., 2008; Schwarzbauer et al., 2002; Yamamoto et al., 2001). For instance, Fukazawa

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et al. (Fukazawa et al., 2001) found that the concentration of BPA was 370 µg/L in the

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effluents of 8 paper recycling plants. The BPA concentrations in landfill leachate in

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Japan were found to reach 17200 µg/L (Asakura et al., 2004; Kurata et al., 2008;

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Yamamoto et al., 2001). Exceptionally high leachate concentration of BPA

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(4200-25000 µg/L) has also been found in Germany (Schwarzbauer et al., 2002). As a

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result, the ubiquitous presence of BPA in natural water systems has also been

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worldwide recognized (Bhatnagar and Anastopoulos, 2017; Corrales et al., 2015;

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Huang et al., 2012; Im and Loffler, 2016; Lee et al., 2013; Wang et al., 2011a; Zhang

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et al., 2017). For example, previous study (Huang et al., 2012) has reported the

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presence of a few BPA hotpots in mainland China, Hong Kong and Taiwan with the

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concentrations of BPA that were over tens of µg/L or µg/g in water bodies and in river

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sediments, respectively. Corrales et al. (Corrales et al., 2015) found that the

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concentration of BPA reached 56 µg/L in surface water. Due to the increasing demand

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for BPA and BPA-based materials, it is expected that BPA pollution in natural

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environment will concomitantly become more and more serious in the near future

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(Huang et al., 2012), which definitely will increase the BPA concentration in natural

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environment.

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cytotoxicity, genotoxicity, reproductive toxicity, and neurotoxicity, the presence of

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BPA in the environment may be harmful to humans and animals (Chen et al., 2016).

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Therefore, the fate of BPA in natural environments has drawn significant attention.

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Since it contains toxic effects, including endocrine disruption,

Previous studies have found that BPA could interact with colloids such as clays

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(Park et al., 2014) and humic acids (Lim et al., 2014), as well as sediments (Sun and

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Zhou, 2014), in the natural environment. For instance, Park et al. (Park et al., 2014)

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found that through hydrophobic interaction, BPA interacted strongly with different

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types of clay fabricated from montmorillonite. Sun and Zhou (Sun and Zhou, 2014)

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reported that nonspecific hydrophobic interaction was the dominant interaction

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between BPA and organic matter in sediments. Therefore, once released into natural

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systems, BPA is also highly likely to interact with porous media and biological

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colloids such as bacteria in the natural environment. The surface properties of the

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porous media and/or the bacteria might be altered by BPA, which may affect the

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transport and deposition behaviors of bacteria in porous media.

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The fate and transport of bacteria in porous media is significant for a wide range

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of water and soil related treatment applications such as riverbank filtration (Weiss et

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al., 2005), in-situ bioremediation of contaminated soil (Sayler and Ripp, 2000), and

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land disposal of effluents from treated sewage and wastewater (Stagnitti, 1999). Over

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recent decades, factors such as grain size and shape (Bradford et al., 2007; Syngouna

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and Chrysikopoulos, 2012), surface coating on the grain collector (Dong et al., 2014; 4

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(Kim et al., 2009; Magal et al., 2011), ion types (Bradford et al., 2007; Wang et al.,

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2011b), fluid conditions (Syngouna and Chrysikopoulos, 2012; Walshe et al., 2010;

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Wang et al., 2013), nutrient conditions (Han et al., 2013; Haznedaroglu et al., 2008),

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bacteria cell types (Bolster et al., 2010; Haznedaroglu et al., 2009; Zhao et al., 2014),

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mobility (De Kerchove and Elimelech, 2008; Haznedaroglu et al., 2010), and surface

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macromolecules

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shown to influence the transport behavior of bacteria in porous media. Colloids

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present in natural environments, such as humic acid (Foppen et al., 2008; Yang et al.,

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2012a; Zhao et al., 2014), clay particles (Vasiliadou and Chrysikopoulos, 2011; Yang

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et al., 2012b; Zhao et al., 2012), and hematite (Yang et al., 2016), as well as

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nanoparticles released into the environment, such as carbon nanotubes (Yang et al.,

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2013) and TiO2 (Battin et al., 2009; Chowdhury et al., 2012b), have also been

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documented to affect the transport behavior of bacteria in porous media. Very recent

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study (Wu et al., 2016) reported that perfluorooctanoic acid at low concentration (100

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µg/L) can also alter the transport and deposition of bacteria in quartz sand. Although

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the interaction of BPA with colloids and sediments has been investigated, the

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significance of BPA on the transport behavior of bacteria in porous media yet has

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never been explored; it thus requires investigation.

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(Kim et al., 2009; Liu et al., 2007; Tong et al., 2010) have been

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Therefore, the present study was designed to investigate the effects and

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mechanisms of BPA on the transport and deposition of bacteria in packed porous

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media

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Gram-negative

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as model cells. Bacteria transport experiments were conducted both with and without

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BPA in cell suspensions at different ionic strength conditions in both monovalent and

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divalent salt solutions. The breakthrough curves and retained profiles of bacteria with

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and without BPA in suspensions were compared under all experimental conditions.

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Possible mechanisms by which BPA affect the transport of bacteria are proposed and

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discussed.

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Materials and Methods

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2.1. Cell Culture and Preparation

E. coli and B. subtilis, which are widely present in the natural environment (Chen

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et al., 2010; Garcia-Armisen and Servais, 2004), were used as model strains in this

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study. E. coli was cultivated in a Luria Broth growth medium (16 h at 37 °C while

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shaking at 200 rpm), whereas B. subtilis was cultivated in a Tryptic Casein Soy Agar

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growth medium (30 °C while shaking at 200 rpm for 32 h), until they both reached the

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stationary growth phase. The cells were harvested by centrifugation (4000 g for 8 min

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at 4 °C). More details regarding the cell harvest protocols are available in our previous

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study (Tong et al., 2010) and in the Supplementary Materials. To remove extracellular

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polymeric substances (EPS) from the cell surfaces, the cation exchange resin (CER)

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technique was used. The CER treatment is clearly explained in our previous

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publications (Long et al., 2009; Wu et al., 2016; Yang et al., 2012a), which could also

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be found in the Supplementary Materials.

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ACCEPTED MANUSCRIPT The concentration of the stock cell solutions (both untreated and CER-treated

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bacterial cell suspension) were counted using a counting chamber (Buerker-Tuerk

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Chamber, Marienfeld Laboratory Glassware, Germany) with an inverted fluorescent

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Ti-E microscope (Nikon, Japan) under a bright field. The stock concentration was

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typically approximately 109–1010 cells/mL. The solution was diluted to obtain the

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target influent concentration of 1.5 × 107 ± 10% cells/mL.

2.2. Preparation of BPA Suspension

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The BPA (Sigma-Aldrich, St. Louis, USA) stock solution was prepared by

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dissolving ~10 mg of BPA powder in 100 mL methanol (HPLC grade). The

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concentration of BPA was determined using a Water Acquity ultra-performance

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HPLC/MS/MS system equipped with a 150 × 2.1 mm2 ZORBAX Extend-C18 column.

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The experimental concentration of BPA was set to be 100 µg/L. Preliminary transport

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experiments (investigating the effects of methanol on bacteria transport behavior)

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showed that breakthrough curves and retained profiles in the presence of methanol

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were equivalent to those without methanol (Figure S1), indicating that methanol had

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no significant influence on the transport behavior of bacteria in porous media.

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2.3. Porous Media

The porous media used for bacteria transport experiments were quartz sand

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(ultrapure with 99.80% SiO2) (Hebeizhensheng Mining Ltd., Shijiazhuang, P.R. China)

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with sizes ranging from 417 to 600 µm. The quartz sand was cleaned by concentrated 7

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sand was washed with deionized water until the pH was neutral. Subsequently, the

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sand was dried overnight at 105 °C, followed by baking at 850 °C for 8 h. The clean

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sand was stored under vacuum until use.

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2.4. Column Experiments

The quartz sand was wet-packed into cylindrical Plexiglass columns (10 cm

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length and 2 cm inner diameter). Mild vibration of the column was required to

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minimize air entrapment. A 140-mesh screen was placed at each end of the column to

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prevent the loss of sand particles. The final porosity of the packed column was

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approximately 0.42.

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After packing, the columns were firstly equilibrated by using twenty pore

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volumes of Milli-Q water and then by ten pore volumes of salt solutions at the desired

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ionic strength and pH. Following pre-equilibration, three pore volumes of bacteria

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suspensions (with and without BPA suspensions) were injected into the column,

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followed by elution with five pore volumes of bacteria-free salt solution at the same

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ionic strength. The suspension and salt solutions were injected in an up-flow

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orientation at 4 m/day (0.43 mL/min) using a syringe pump (Harvard PHD 2000,

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Harvard Apparatus Inc., Holliston, USA). In selected experiments, three pore volumes

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of BPA were injected prior to the addition of the bacteria suspension, followed by two

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pore volumes of salt solution at the desired condition to elute the unattached BPA. The

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transport experiments were conducted in both NaCl (10 and 25 mM ionic strength)

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and CaCl2 (1.2 and 5 mM ionic strength) solutions without pH adjustment (pH~6.3) to

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avoid any influence of chemical species in the buffer solution. All water used in these

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experiments was sterilized by autoclaving. During the transport experiments, samples of the column effluent were collected

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in 10 mL centrifuge tubes at the desired time intervals. After the transport experiment,

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the sediment was extruded from the column under gravity and dissected into 10

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segments (each 1 cm long) for sample concentration analysis. To obtain the cell

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concentration in both the effluent samples and the recovery of retained bacteria, each

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sample was directly counted using a counting chamber with an inverted fluorescent

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Ti-E microscope under a bright field. The overall recovery (mass balance) of cells for

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each transport experiment is provided in Table S1. The protocol for obtaining the

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mass balance is provided in the Supplementary Materials.

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2.5. Measurement of Zeta Potential

A Zetasizer Nano ZS90 (Malvern Instruments, UK) was used to determine the

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zeta potential of bacteria and quartz sand in the presence and absence of BPA in NaCl

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(10 and 25 mM) and CaCl2 solutions (1.2 and 5 mM) (Table S2). Each measurement

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was performed at least 9–12 times. The detailed procedure has been reported in

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previous studies (Tong et al., 2010; Yang et al., 2012a).

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2.6. Measurement of surface thermodynamics Prior to the measurement of the contact angles, the bacteria suspension was 9

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cell lawns. The BPA wafers were compressed using a powder compressing machine

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(769YP-15A, Tianjin). The contact angles were measured by the sessile drop

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technique (Ong et al., 1999; Wang et al., 2011b). All the contact angles were measured

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against an apolar liquid, diiodomethane, and two polar liquids, water and glycerol,

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using an OCAH200 contact angle analyzer (Dataphysics Co., Germany). The reported

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contact angles under all examined conditions were the average of at least 10 replicated

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measurements (Table S3).

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An extended Derjaguin–Landau–Verwey–Overbeek (XDLVO) approach is used

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to describe interaction energies between spherical particles and rough surfaces

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(Vanoss, 1993). Interactions between bacteria and quartz sand with and without BPA

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should be considered Lifshitz–van der Waals (LW), Lewis acid–base (AB), and

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electrostatic double layer interactions (EL). Therefore, the total interaction can be

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calculated as a sphere-plate geometry system based on the following equations

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(Bergendahl and Grasso, 1999; Vanoss, 1995):

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ΦTotal = ΦLW + ΦEL + ΦAB ∆G LW = −

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−1

(2)

  1 + exp(− κh ) ∆G EL = πrεε 0 2ζ b ζ s ln + ζ b2 + ζ s2 ln[1 + exp(− 2κh )]  1 − exp(− κh )  

(

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h − h   ∆ G AB = 2π r λ AB ∆ G hAB0 exp  0  λ AB 

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(1)

(3)

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wavelength of the interaction (usually taken as 100 nm), ε0 is the dielectric

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permittivity of the vacuum (8.854 × 10−12 C V−1 m−1), ε is the dielectric constant of

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water (78.5), ζb and ζs is the zeta potential of bacteria and sand, respectively, λAB is the

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decay length of water (1 nm), and h0 is the distance of the closest approach (0.158 nm)

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(Bergendahl and Grasso, 1999). The quantity A132 is the Hamaker constant for

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substances “1” and “2” in the presence of medium “3” and can be determined from

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the Hamaker constant of each material. The detailed calculation of A132 based on

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surface free energy information is given in the SI. The calculation of κ and ∆GAB is

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also provided in the Supplementary Materials.

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3.

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3.1. Influence of BPA on Transport and Deposition of Cells

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Results and Discussion

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To understand the effect of BPA on the transport and deposition of bacteria in

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porous media, the transport behaviors of Gram-negative E.coli in packed quartz sand

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both with and without 100 µg/L BPA were examined in NaCl solution at two ionic

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strengths (10 and 25 mM). In the absence of BPA, the breakthrough curves at higher

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ionic strength were lower than those acquired at lower ionic strength (Figure 1, left,

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open symbols), indicating that the transport of E.coli was sensitive to ionic strength.

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The observation was qualitatively consistent with the less negative cell zeta potential

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observed at higher ionic strength (Table S2) and agreed with the DLVO theory. The

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decreased bacteria transport with the increase of ionic strength has also been widely

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noteworthy observation was that the breakthrough curve of E.coli when BPA was

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present in suspensions (Figure 1a, solid symbols) was higher than that in the absence

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of BPA (Figure 1a, open symbols). This was true under both ionic strength conditions

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(10 and 25 mM NaCl). Specifically, in 10 and 25 mM NaCl solutions, 81.98% and

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52.80% of E.coli broke through the column when BPA was absent in cell suspensions,

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respectively; whereas, 96.65% and 78.31% of E.coli passed through the porous media

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in the presence of BPA in 10 and 25 mM NaCl solutions, respectively. This

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observation demonstrated that the presence of BPA increased E.coli transport in

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packed quartz sand under both ionic strength conditions in NaCl solutions.

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FIGURE 1.

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To investigate whether the presence of BPA would also affect the transport of

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E.coli in divalent ion solutions, E.coli transport experiments in the quartz sand both

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with and without BPA in suspensions were conducted at two ionic strengths (1.2 and 5

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mM) in CaCl2 solutions (Figure 1c). Similar to the observations in NaCl solutions, the

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breakthrough curves of bacteria when BPA was present in suspensions (Figure 1c,

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solid symbols) were higher than those without BPA (Figure 1c, open symbols) under

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both examined ionic strength conditions in CaCl2 solutions. Clearly, the presence of

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BPA in cell suspensions also increased the transport of E.coli in divalent ion (CaCl2)

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solutions.

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To testify whether the presence of BPA would also affect the transport behaviors

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of Gram-positive bacteria, transport experiments of B. subtilis, typical Gram-positive 12

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suspensions at two ionic strengths (10 and 25 mM) in NaCl solutions. Similar to the

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observation for E.coli (Figure 1a), the breakthrough curves of B. subtilis with BPA in

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cell suspensions were also higher than those without BPA (Figure 2a). This held true

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for both examined ionic strength conditions. The results showed that the presence of

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BPA in cell suspensions also increased the transport of Gram-positive B. subtilis in

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porous media. FIGURE 2.

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Previous studies found that the copresence of colloids (clay and nano-particles)

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in cell suspensions would change the deposition behaviors of bacteria in porous media

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(Yang et al., 2012b; 2013). To examine whether the presence of BPA in suspensions

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would affect the deposition of bacteria in quartz sand, the retained profiles of both

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Gram-negative E.coli and Gram-positive B. subtilis with and without BPA in cell

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suspensions under all examined solution conditions were acquired (Figure 1, right).

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As expected from the mass balance consideration (Table S1), the magnitudes of the

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retained profiles varied oppositely to the breakthrough plateaus (Figures 1 and 2,

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right). The amount of bacteria retained in the quartz sand at lower ionic strength was

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less than that at higher ionic strength in both NaCl and CaCl2 solutions, which was

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consistent with the trend of zeta potential versus ionic strength and agreed with DLVO

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theory. Under all investigated solution conditions in both NaCl and CaCl2 solutions,

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the amount of retained cells when BPA was present in the suspension (Figures 1 and 2,

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right, solid symbols) was lower than that without BPA (Figure 1, right, open symbols).

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bacteria in porous media under all examined solution conditions. Close comparison

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the shapes of the retained profiles obtained with BPA versus those without BPA

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indicated that for both Gram-negative E.coli and Gram-positive B. subtilis, the overall

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shape of the retained profile with BPA in suspensions was similar to that without BPA

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under all examined solution conditions. This observation showed that under all

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examined conditions, although the copresence of BPA decreased the cell deposition in

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quartz sand, yet it did not change the shape of cell retained profiles.

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3.2. Mechanisms Driving the Altered Transport of Cells by BPA

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3.2.1. Alteration in the Surface Properties of Bacteria

Many previous studies have shown that coexisting colloids such as humic acid

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(Chowdhury et al., 2012a; Jiang et al., 2012; Johnson and Logan, 1996; Yang et al.,

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2016) and clay particles (Cai et al., 2014; Yang et al., 2012b) can change the surface

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properties of colloids and thus influence their fate and transport in quartz sand. For

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example, Johnson and Logan (Johnson and Logan, 1996) found that the addition of

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humic acid to cell suspensions would change cell zeta potentials, which affected the

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transport behaviors of bacteria in porous media. In the present study, the copresence

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of BPA in the cell suspension might also change the surface properties of the bacteria,

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resulting in the increased transport and decreased retention of bacteria in the quartz

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sand. To test this hypothesis, the zeta potentials of bacteria with and without the

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co-presence of BPA in cell suspensions were examined under all experimental ionic

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ACCEPTED MANUSCRIPT strength conditions in both NaCl and CaCl2 solutions. The results are provided in

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Table S2. Under all examined solution conditions, the zeta potential of bacteria in the

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presence of BPA was found to be similar to those in the absence of BPA (Table S2).

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This was true for both cell types. This observation demonstrated that the presence of

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BPA did not have a significant effect on the properties of cell surfaces. Clearly, the

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increased cell transport induced by BPA was not likely caused by changes in cell zeta

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potentials.

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The transport of colloids in porous media would be affected by colloid sizes.

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Specifically, increasing colloid size has been found to decrease colloid transport (Cai

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et al., 2014), whereas decreasing the size of colloids can greatly increase their

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transport in porous media (Chowdhury et al., 2012c). To investigate whether the size

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of bacteria was altered by the presence of BPA, the cell sizes both with and without

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BPA in solutions were determined using an inverted microscope (Ti-E, Nikon, Japan).

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The sizes of at least 60 cells were measured for each sample and the results showed

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that for all cell types, the bacterial sizes in the presence of BPA were equivalent to

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those in the absence of BPA (data not shown). To further confirm the effect of BPA on

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cell size, dynamic light scattering (Zetasizer Nano, ZS90) was also used to measure

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the size of bacteria both in the absence and presence of BPA in NaCl and CaCl2

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solutions. The results are shown in Table S2. Similar to the microscope observations,

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DLS measurement showed that the size of bacteria in the presence of BPA was

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equivalent to that in the absence of BPA. This observation further demonstrated that

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the addition of BPA in bacterial suspensions did not alter the cell sizes. Herein, the

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increased cell transport obtained when BPA was present in suspensions was not driven

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by changes in bacterial surface charge or cell size. Although the surface charge and the cell size was not changed by the presence of

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BPA, interaction between BPA and extracellular polymeric substances (EPS),

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biopolymers accumulating on or around microbial cell surface with the major

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components to be polysaccharide and protein (Long et al., 2009), as well as polymer

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(i.e. protein) on cell membrane might still be present. Previous studies (Wu et al.,

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2016; Yang et al., 2012a) have also found that organic matters such as humic acid and

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PFOA would adsorb onto cell surfaces, which yet did not alter the surface charge and

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cell size. The amounts of BPA adsorbed onto bacteria in 25 mM NaCl and 5 mM

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CaCl2 solutions were determined (Figure S2). Under both examined solution

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conditions, portion of BPA adsorbed onto cell surfaces. Specifically, in 25 mM NaCl

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solutions, 5% and 9% of BPA adsorbed onto untreated (with EPS) and CER-treated

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cells (without EPS), respectively, while, in 5 mM CaCl2 solutions, the BPA adsorption

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rate onto untreated and treated cells was 8% and 12%, respectively. Endo et al. (Endo

319

et al., 2007) also reported that small portion (3.8%) of BPA adsorbed onto lactococci.

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Previous studies (Wu et al., 2016; Yang et al., 2012a) have shown that the

321

adsorption of organic matter (i.e. humic acid and PFOA) did not contribute to the

322

increased cell transport in porous media. To determine whether the adsorption of BPA

323

onto cell surfaces has contribution to the increased cell transport with the copresence

324

of BPA, transport experiments for both untreated and treated cells were conducted

325

under representative conditions (25 mM NaCl and 5 mM CaCl2) with bacteria 16

ACCEPTED MANUSCRIPT suspension premixed with 100 µg/L BPA, yet from which the suspended (un-adsorbed)

327

BPA was removed via filtration with 0.22 µm nylon membranes under vacuum.

328

Regardless the presence or absence of EPS, the breakthrough curves of bacteria

329

pre-mixed with BPA yet with the removal of suspended BPA were found to be

330

equivalent to those in the absence of BPA in cell suspensions (cells without BPA

331

pre-mixed) (Figure 3, solid squares versus open squares). The observation indicated

332

that although BPA adsorbed onto cell surfaces, yet it did not change the transport

333

behaviors of bacteria in quartz sand. Clearly, the increased cell transport obtained with

334

BPA copresent in suspensions was not likely caused by adsorption of BPA onto cell

335

surfaces.

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Moreover, comparison the transport behaviors of EPS-removed bacteria (treated

337

cells) in the presence of BPA versus those of absence of BPA showed that similar to

338

the untreated cells (EPS present cells), the breakthrough curves for EPS-removed cells

339

in the presence of BPA (Figure 3, right, solid triangles) were also higher than those

340

without BPA in suspensions (Figure 3, right, solid squares). This was true in both 25

341

mM NaCl and 5 mM CaCl2 solutions. Accordingly, the retained profiles of treated

342

bacteria in the presence of BPA were lower than those in the absence of BPA (Figure

343

S3). The observation clearly showed that regardless the presence or absence of EPS,

344

the presence of BPA in solutions enhanced the transport and deceased the retention of

345

bacteria in porous media. As stated above, for both untreated and treated cells, the

346

adsorption of BPA onto cell surfaces did not change the transport behaviors of

347

bacteria in quartz sand. Obviously, other mechanism instead of interaction with

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ACCEPTED MANUSCRIPT 348

(adsorption onto) cell surfaces contributed to the increased cell transport obtained

349

when BPA was copresent in suspensions. FIGURE 3.

350

352 353

3.2.2. Alteration in the Zeta Potentials of Quartz Sand

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Previous studies have found that the presence of organic matter components such

355

as perfluoroalkyl acids (Wu et al., 2016; Zhang et al., 2014) and humic acid (Yang et

356

al., 2012a) changed the zeta potential of quartz sand. However, in the present study,

357

equivalent zeta potentials were observed for quartz sand both in the presence and

358

absence of BPA under all examined solution conditions (Table S2), indicating that the

359

presence of BPA in cell suspensions had no significant effect on the zeta potential of

360

quartz sand. Obviously, the increased transport and decreased deposition of bacteria

361

induced by BPA was not caused by alteration of the zeta potentials of quartz sand.

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3.2.3. Interaction Energy between Bacteria and Quartz Sand

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As stated above, the zeta potentials of both bacteria and quartz sand in the

365

presence of BPA were comparable to those in the absence of BPA. Moreover,

366

equivalent sizes were obtained for bacteria both in the presence and absence of BPA

367

in suspensions. If the presence of BPA did not affect the contact angle of the bacteria,

368

the Hamaker constant of cell–water–sand would not be changed. Thus, the interaction

369

profile between bacteria and quartz sand with BPA would be similar to that without 18

ACCEPTED MANUSCRIPT BPA. However, the contact angle of bacteria when BPA was present in the cell

371

suspension was different to that without BPA. Previous study (Wu et al., 2016) also

372

reported that the presence of PFOA in the suspension changed the contact angle of

373

bacteria. The resulting interaction energy profiles including LW, EL, and AB

374

interactions for bacteria–sand in the presence and absence of BPA in suspensions

375

under the examined solution conditions are provided in Figure 4. In both NaCl and

376

CaCl2 solutions, the bacteria–sand interaction energy in both the presence and

377

absence of BPA at high ionic strength was smaller than that at low ionic strength. This

378

theoretically supports the observation that greater deposition of bacteria was acquired

379

at high ionic strength. It was noteworthy that under all examined conditions, the

380

interaction energy between bacteria and quartz sand with BPA in suspension was

381

lower than that without BPA. According to the calculated energy profile, the cell

382

deposition in quartz sand would be increased and the transport of cells should be

383

decreased. However, the bacteria transport trends observed in the present study

384

(Figures 1 and 2) were opposite to those predicted by theory. For instance, 19.56%

385

and 4.78% of the bacteria were found to deposit on quartz sand in the presence and

386

absence of BPA in 10 mM NaCl solution, respectively. The contradiction between the

387

observations and the theory prediction indicates that other mechanisms drove the

388

increased bacteria transport in the presence of BPA.

389

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FIGURE 4.

390 391

3.2.4. Competition of Deposition Sites by BPA 19

ACCEPTED MANUSCRIPT It should be also noted that even in the presence of an energy barrier

393

(unfavorable conditions), the deposition of bacteria still occurred. Surface roughness

394

and/or chemical heterogeneity on the sand surface have been widely reported to

395

contribute to the colloid deposition under unfavorable conditions (Bradford and

396

Torkzaban, 2015; Han et al., 2014). For instance, nanoscale roughness can

397

significantly reduce the energy barrier, and the energy barrier can be eliminated

398

entirely under certain conditions, resulting in the deposition of colloid (Bradford and

399

Torkzaban, 2013; 2015). Additionally, chemical heterogeneity (e.g., due to metal

400

oxides) on the collector surface may also allow colloid deposition in the presence of

401

an energy barrier (Dong et al., 2014; Kim et al., 2008b). The chemical heterogeneity

402

of quartz sand might be changed by the adsorption of BPA onto sand surface, which

403

thus would affect cell transport behaviors.

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To investigate whether the chemical heterogeneity would be changed with the

405

addition of BPA, BPA transport tests (Figure S4) was conducted in 25 mM NaCl and 5

406

mM CaCl2 solutions. Figure S4 showed that even the zeta potentials of quartz sand

407

was not changed, adsorption of BPA onto the surface of quartz sand definitely

408

occurred. Particularly, around 59% and 80% of BPA were found to be adsorbed onto

409

quartz sand surface in 25 mM NaCl and 5 mM CaCl2 solutions, respectively (Figure

410

S4). The adsorption of BPA onto sand surfaces would lead to the variation of quartz

411

sand chemical heterogeneity. To further determine whether the BPA adsorbed on the

412

surface of the quartz sand surface (that changed the chemical heterogeneity of sand

413

surface) would affect the transport behavior of bacteria, additional transport

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20

ACCEPTED MANUSCRIPT experiments that involved pre-covering the deposition sites on the quartz sand with

415

BPA (pretreating the columns with three pore volumes of 100 µg/L BPA solution at

416

experimental ionic strength) were conducted. Since BPA has the same effect on the

417

different cell strains under all examined conditions, pretreatment experiments were

418

performed only with E.coli as the representative bacteria. In comparison with

419

transport experiments conducted without BPA pretreatment (Figure 5, left, solid

420

triangles), higher cell breakthrough curves were observed for columns pretreated with

421

BPA yet without BPA in cell suspensions in both 10 and 25 mM NaCl solutions

422

(Figure 5, left, open squares). Accordingly, lower retained profiles were observed for

423

these columns (Figure 5, right, open squares).

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FIGURE 5.

424

Moreover, pretreatment experiments conducted at two ionic strengths (1.2 and 5

426

mM) in CaCl2 solutions yielded the same results as those in NaCl solutions.

427

Specifically, under both examined ionic strength conditions in CaCl2 solutions, the

428

E.coli breakthrough curves were higher, and the corresponding retained profiles were

429

lower, for columns with BPA pretreatment yet without BPA present in suspensions

430

(Figure 6, open squares) relative to those without BPA pretreatment (Figure 6, solid

431

squares). These observations showed that BPA competed with bacteria for the

432

deposition sites on quartz sand surfaces, resulting in fewer sites for bacteria deposition.

433

Clearly, sites competition by BPA contributed to the enhanced transport and decreased

434

deposition when BPA was present in cell suspensions.

435

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FIGURE 6. 21

ACCEPTED MANUSCRIPT More importantly, under all examined ionic strengths in NaCl and CaCl2

437

solutions, the breakthrough curves and retained profiles for columns pretreated with

438

BPA yet without BPA present in suspensions (Figures 5 and 6, open squares) were

439

similar to those for columns without pretreatment yet with BPA in cell suspensions

440

(Figures 5 and 6, solid triangles). Moreover, the breakthrough curves and retained

441

profiles with BPA pretreatment but without BPA in suspensions were also equivalent

442

to those pre-equilibrated with BPA and with BPA in bacteria suspensions (Figures 5

443

and 6, solid squares). These observations show that BPA pretreatment had a similar

444

effect on cell transport behavior as the presence of BPA in cell suspensions. Therefore,

445

under all examined conditions regardless of ionic strength and ion valence,

446

competition for sites on quartz sand surfaces by BPA was the sole contributor to the

447

increased transport and decreased deposition of bacteria in quartz sand.

448 449

4.

Conclusion

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The findings from this study give an insight into the effects of BPA on the

451

transport of bacteria in porous media. The core results showed that regardless of

452

bacteria type, ionic strength, ion types, and the presence or absence of EPS, BPA

453

copresent in suspensions would increase the transport of bacteria and decreased the

454

deposition of bacteria in quartz sand under all experimental conditions. The presence

455

of BPA increases bacterial transport by competing for deposition sites on the quartz

456

sand surfaces. This process will increase the environmental risks associated with

457

bacteria transport, especially pathogens are released into aquatic environment where

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ACCEPTED MANUSCRIPT 458

BPA was present. The experimental results also have potential implications for estimation the fate

460

and transport of bacteria in natural environments containing other similar organic

461

matters. Despite of their different intrinsic properties, based on the present study, the

462

presence of organic matters would have these potential effects: (i) via interaction with

463

cells, the surface properties of bacteria (zeta potentials, sizes, or hydrophobicity)

464

might be altered; (ii) via adsorption onto sand surfaces, the surface properties

465

(physical and chemical heterogeneity) of porous media would be changed,

466

consequently providing additional sites or blocking sites for cell deposition; and (iii)

467

via providing other interaction forces (such as steric repulsion, hydrophobicity,

468

hydrogen-bond interaction or polymeric interaction), the total interaction forces

469

between cell and sand would be affected. Through the above mentioned effects (one

470

or more), the fate and transport of bacteria (even other colloids) would be influenced

471

by organic matter present in real environment.

474

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Acknowledgments

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This work was supported by the National Nature Science Foundation of China

475

under Grants No. 41422106 and No. 21177002, and the program for New Century

476

Excellent Talents in University under Grant No. NCET-13-0010. We acknowledge the

477

editor and the reviewers for their very helpful comments.

478 479

Appendix A. Supplementary data 23

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Supplementary data are provided in the Supplementary Materials.

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24

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Wu, D., Tong, M. and Kim, H., 2016. Influence of perfluorooctanoic acid on the

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transport and deposition behaviors of bacteria in quartz sand. Environ. Sci. Technol.

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hazardous waste landfill leachates. Chemosphere 42, 415-418.

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Yang, H., Ge, Z., Wu, D., Tong, M. and Ni, J., 2016. Cotransport of bacteria with

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hematite in porous media: effects of ion valence and humic acid. Water Res. 88,

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586-594.

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Yang, H.Y., Kim, H. and Tong, M.P., 2012a. Influence of humic acid on the transport

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behavior of bacteria in quartz sand. Colloid Surface B 91, 122-129.

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Yang, H.Y., Tong, M.P. and Kim, H., 2012b. Influence of Bentonite Particles on

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Representative Gram Negative and Gram Positive Bacterial Deposition in Porous

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Media. Environmental Science & Technology 46, 11627-11634.

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Yang, H.Y., Tong, M.P. and Kim, H., 2013. Effect of carbon nanotubes on the

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transport and retention of bacteria in saturated porous Media. Environ. Sci. Technol.

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47, 11537-11544.

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Zhang, M., Shi, Y., Lu, Y., Johnson, A.C., Sarvajayakesavalu, S., Liu, Z., Su, C.,

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Zhang, Y., Juergens, M.D. and Jin, X., 2017. The relative risk and its distribution of

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endocrine disrupting chemicals, pharmaceuticals and personal care products to

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freshwater organisms in the Bohai Rim, China. Sci Total Environ 590-591, 633-642.

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Zhang, R.M., Yan, W. and Jing, C.Y., 2014. Mechanistic study of PFOS adsorption on

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Zhao, W., Liu, X., Huang, Q., Walker, S.L. and Cai, P., 2012. Interactions of

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pathogens Escherichia coli and Streptococcus suis with clay minerals. Appl. Clay Sci.

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Zhao, W., Walker, S.L., Huang, Q. and Cai, P., 2014. Adhesion of bacterial pathogens

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to soil colloidal particles: influences of cell type, natural organic matter, and solution

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chemistry. Water Res. 53, 35-46.

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ACCEPTED MANUSCRIPT 10 mM w/o BPA 25 mM w/o BPA

1.2

(a) NaCl

10 mM w/ BPA 25 mM w/ BPA

1.2 mM w/o BPA 5 mM w/o BPA

7.5

E. coli

1.2 mM w/ BPA 5 mM w/ BPA

(b) NaCl

E. coli

1.0 7.0

0.4 0.2 0.0 0 1.2 1.0

2

4

(c) CaCl2

6

E. coli Log # of Cell

0.4 0.2 0.0 0 687

2

4 6 Pore Volume

7.0

M AN U

C/Co

0.6

6.0

5.5 0.00 0.02 0.04 0.06 0.08 0.10 7.5 (d) CaCl2 E. coli

8

0.8

6.5

SC

0.6

RI PT

Log # of Cell

C/Co

0.8

8

6.5

6.0 0.00 0.02 0.04 0.06 0.08 0.10 Distance (m)

FIGURE 1. Breakthrough curves (left) and retained profiles (right) for E.coli in the

689

absence (open symbols) and presence (solid symbols) of BPA in cell suspensions in

690

both NaCl (10 and 25 mM, squares and circles, respectively) and CaCl2 (1.2 and 5

691

mM, upward triangles and downward triangles, respectively) solutions at pH 6.3.

692

Error bars represent standard deviations of replicate experiments (n ≥ 2).

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ACCEPTED MANUSCRIPT 10 mM NaCl w/o BPA

25 mM NaCl w/o BPA

10 mM NaCl w/ BPA

25 mM NaCl w/ BPA

1.2

(a)

B. subtilis

1.0

RI PT

C/Co

0.8 0.6 0.4

0.0 0

694

7.0

6.5

8

B. subtilis

M AN U

(b)

4 6 Pore Volume

TE D

Log # of Cell

7.5

2

SC

0.2

6.0 0.00 0.02 0.04 0.06 0.08 0.10 Distance (m)

FIGURE 2. Breakthrough curves (left) and retained profiles (right) for B. subtilis in

696

the absence (open symbols) and presence (solid symbols) of BPA in cell suspensions

697

in 10 and 25 mM NaCl solutions at pH 6.3. Error bars represent standard deviations of

698

replicate experiments (n ≥ 2).

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ACCEPTED MANUSCRIPT

(a) 25 mM NaCl

0.6 0.4

2

4

(c) 5 mM CaCl2

Untreated E.coli

0.8

C/Co

0.4

0.6 0.4

2

4

(d) 5 mM CaCl2

6

8

Treated E.coli

0.2

0.2

700

0.0 0 1.0

8

0.6

0.0 0

0.4

M AN U

C/Co

0.8

6

Treated E.coli

0.6

0.2

0.2 0.0 0 1.0

(b) 25 mM NaCl

0.8

C/Co

C/Co

0.8

1.0

Untreated E.coli

w/ BPA

SC

1.0

w/o suspended BPA

RI PT

w/o BPA

2

4 6 Pore Volume

8

0.0 0

2

4 6 Pore Volume

8

FIGURE 3. Breakthrough curves for E. coli (left for untreated with EPS and right for

702

treated without EPS) without BPA (solid squares), pre-mixed with BPA yet without

703

suspended BPA (open squares), and with (solid triangles) BPA in suspensions in 25

704

mM NaCl and 5 mM CaCl2 solutions in quartz sand. The data for the case without

705

BPA and with BPA in suspensions (left, solid symbols) were replotted from Figure

706

1.Error bars represent standard deviations of replicate experiments (n ≥ 2).

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ACCEPTED MANUSCRIPT w/o BPA

w/ BPA (b) 25 mM NaCl

4

4

3x10 0.2 40.0 5x10 (c) 1.2 mM CaCl

0.4

0.6 0.0

4

4x10

4

0.4

0.6

SC

709

FIGURE 4. Interaction energy between bacteria and quartz sand in the absence

710

(dashed line) and presence (solid line) of BPA in cell suspensions.

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0.2 0.4 0.6 0.0 0.2 0.4 0.6 Separation Distance (nm) Separation Distance (nm)

711

0.0

0.2

(d) 5 mM CaCl2

2

3x10

RI PT

4x10

M AN U

Interaction Energy (kT)

Interaction Energy (kT)

4

5x10 (a) 10 mM NaCl

35

ACCEPTED MANUSCRIPT w/o BPA Pre w/o BPA

w/ BPA Pre w/ BPA

1.2

7.5 (a) 10 mM NaCl

(b) 10 mM NaCl

E. coli

E. coli

1.0 7.0 0.6 0.4 0.2 2

4

6

(c) 25 mM NaCl

6.0

5.5 0.00 0.02 0.04 0.06 0.08 0.10 7.5

8 E. coli

(d) 25 mM NaCl

1.0 7.0

Log # of Cell

0.6 0.4 0.2 0.0 0

712

2

4 6 Pore Volume

6.5

M AN U

C/Co

0.8

E. coli

SC

0.0 0 1.2

6.5

RI PT

Log # of Cell

C/Co

0.8

8

6.0

5.5 0.00 0.02 0.04 0.06 0.08 0.10 Distance (m)

FIGURE 5. Breakthrough curves (left) and retained profiles (right) for E. coli in the

714

absence (open symbols) and presence (solid symbols) of BPA in cell suspensions both

715

with (squares) and without (triangles) pretreatment of the quartz sand with three pore

716

volumes of 100 µg/L BPA solution in 10 and 25 mM NaCl solutions. The data for the

717

case without BPA pretreatment of the quartz sand (open symbols) were replotted from

718

Figure 1. Error bars represent standard deviations of replicate experiments (n ≥ 2).

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ACCEPTED MANUSCRIPT w/o BPA Pre w/o BPA

7.5

1.2

(b) 1.2 mM CaCl2

E. coli Log # of Cell

C/Co

0.8 0.6 0.4

7.0

6.5

0.2 0.0 0 1.2 1.0

2

4

(c) 5 mM CaCl2

6

E. coli Log # of Cell

0.4 0.2 2

4 6 Pore Volume

7.0

6.5

M AN U

C/Co

0.6

0.0 0

6.0 0.00 0.02 0.04 0.06 0.08 0.10 7.5 (d) 5 mM CaCl2 E. coli

8

0.8

E. coli

RI PT

(a) 1.2 mM CaCl2

SC

1.0

w/ BPA Pre w/ BPA

8

6.0 0.00 0.02 0.04 0.06 0.08 0.10 Distance (m)

FIGURE 6. Breakthrough curves (left) and retained profiles (right) for E. coli in the

722

absence (open symbols) and presence (solid symbols) of BPA in cell suspensions both

723

with (squares) and without (triangles) pretreatment of the quartz sand with three pore

724

volumes of 100 µg/L BPA solution in 1.2 and 5 mM CaCl2 solutions. The data for the

725

case without BPA pretreatment of the quartz sand (open symbols) were replotted from

726

Figure 1. Error bars represent standard deviations of replicate experiments (n ≥ 2).

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ACCEPTED MANUSCRIPT Highlights Transport of bacteria in porous media was affected by Bisphenol A (BPA).




BPA increased the transport of both Gram-negative and Gram-positive cells.




BPA increased cell transport regardless of ionic strength, ion valence, and EPS.




Repulsive interaction between bacteria and quartz sand was decreased by BPA.




Competition deposition sites by BPA drove to the increased cell transport.

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