1

Plant root exudates decrease mobility of smectite colloids in porous media in contrast to

humic acid

Yuan Tian1, Cheng-Hua Liu

1,2, Alvin J.M Smucker

1, Hui Li

1, Wei Zhang

1,2*

1 Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI

48824

2 Environmental Science and Policy Program, Michigan State University, East Lansing, MI

48824

* Corresponding Author, phone: (517) 353-0471, fax: (517) 355-0270, email:

weizhang@msu.edu

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Plant root exudates decrease mobility of smectite colloids in porous media in contrast to 1

humic acid 2

3

ABSTRACT 4

Plant root exudates are primarily composed of carbohydrates (CHs), amino acids (AAs) 5

and organic acids (OAs). Little is known about how plant root exudates influence stability and 6

mobility of clay colloids in soil profile. In this study, transport behaviors of K+-saturated 7

smectite colloids dispersed in artificial maize root exudate (ARE) solution, humic acid (HA) 8

solution, and deionized water through water-saturated sand columns were investigated with 9

solution ionic strength of 0.1 and 10 mM KCl and pH of 5, 7 and 9, respectively. Results showed 10

that smectite colloids were more aggregated and less transported in ARE solution, followed by in 11

water and HA solution. This trend became less apparent with increasing pH, but more 12

pronounced with increasing ionic strength, suggesting that enhanced stability and mobility of 13

HA-dispersed smectite colloids likely resulted from increased electrostatic and/or steric 14

repulsions. The results of CH-, AA-, or OA-dispersed smectite colloids revealed that the AA 15

fraction was primarily responsible for the enhanced colloid retention because positively charged 16

amine groups in AAs (especially lysine) might neutralize the negative surface charge of colloids 17

and promote inter-surface bridging. The residual colloids after flushing with deionized water 18

(thus eliminating secondary energy minimum) decreased in the order of the ARE-, water-, and 19

HA-dispersed colloids, suggesting greater retention by primary energy minimum and pore 20

straining for the ARE-dispersed smectite colloids. Overall, in contrast to humic acid, plant root 21

exudates decreased the stability and mobility of smectite colloids, thus facilitating the retention 22

of clay colloids in root zones during water percolation events. 23

24

Keywords: aggregation, transport, smectite clay, plant root exudates, humic acid, environmental 25

fate, mobility 26

27

Abbreviations: CHs, carbohydrates; AAs, amino acids; OAs, organic acids; AREs, artificial root 28

exudates; REs, root exudates; HA, humic acid; NOM, natural organic matter; TOC, total organic 29

carbon; EPM, electrophoretic mobility; PVs, pore volumes; BTC, breakthrough curve.30

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INTRODUCTION 31

Movement of clay colloids in soil profile controls many environmental processes, 32

including facilitated contaminant transport, soil formation, etc. (Bradford and Torkzaban, 2008, 33

McCarthy and Zachara, 1989, Ryan and Elimelech, 1996, Schaetzl and Anderson, 2005). Clay 34

colloids, especially 2:1 clay smectites, typically exhibit a strong affinity to a range of 35

contaminants such as radionuclides, heavy metals, pesticides and pharmaceuticals (Korichi and 36

Bensmaili, 2009, Li et al., 2004b, Sipos et al., 2008, Wang et al., 2009). Clay movement often 37

facilitates the transport of contaminants that otherwise remain immobile within soil matrix, 38

subsequently contributing to groundwater contamination (Kersting et al., 1999, McCarthy and 39

Zachara, 1989, Ryan and Elimelech, 1996). From a pedogenetic perspective, downward transport 40

(i.e., eluviation) and accumulation (i.e., illuviation) of clays in sandy soils could create stratified 41

soil layers. For instance, thin layers (or lamellae) of clay (< 0.5 cm) termed as Bt horizons are 42

formed in sandy soils (Rawling 3rd, 2000, Schaetzl and Anderson, 2005), which alter water and 43

solute flow and plant productivity. Therefore, it is very important to fully understand the 44

transport of clay colloids in the subsurface and relevant controlling environmental factors. 45

Extensive studies have been conducted to elucidate deposition and release behaviors of 46

colloids in the subsurface (Bradford et al., 2013, Bradford and Torkzaban, 2008, Ryan and 47

Elimelech, 1996). Direct attachments on grain surfaces via primary or secondary energy minima 48

and trapping in small pore space (e.g., wedging and pore straining) are recognized as the main 49

mechanisms responsible for colloid retention in saturated porous media (Bradford et al., 2004, 50

Bradford et al., 2009, Kim et al., 2010, Tian et al., 2012). Hydrodynamic and chemical 51

parameters including flow regime, solution pH, ionic strength, and natural organic matter (NOM) 52

are important factors controlling colloid transport. Among the complex NOM fractions, humic 53

substances such as humic and fulvic acids are often perceived as large complex assemblages of 54

macromolecules containing numerous functional groups, which tend to induce electrostatic and 55

steric repulsions and thus enhance colloid stability and mobility (Franchi and O'Melia, 2003, 56

Morales et al., 2011, Zhang et al., 2013). However, little is known about the effect of non-humic 57

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NOM fractions on colloid transport. Non-humic NOM fraction typically consists of organic 58

compounds secreted by plant roots, e.g., root exudates (REs) (Nardi et al., 2000) as well as many 59

macromolecules such as lipids, proteins, and polysaccharides. While the exact composition of 60

REs varies among plant species (Gunawardena et al., 2001, Powell and Klironomos, 2007), 61

carbohydrates (CHs) are the most abundant compounds, followed by amino acids (AAs) and 62

other organic acids (OAs) (Jones et al., 2009). Despite REs are mostly biodegradable labile 63

carbon, continual production of REs by healthy plant roots in soil rhizosphere results in 64

accumulation of REs in soils (Bolan et al., 1994, Strobel, 2001). However, little information is 65

currently available regarding the effects of REs on colloid stability and mobility. Amino acids 66

may induce colloid aggregation via surface charge reduction and/or inter-surface bridging, or 67

promote colloid stability by increasing electrostatic and/or steric repulsions (Molina et al., 2011, 68

Zakaria et al., 2013), whereas organic acids such as citric, malonic, and oxalic acids could 69

enhance colloid mobilization by increasing negative surface charges (Lowry et al., 2004, Slowey 70

et al., 2005). 71

Given the paucity of research regarding the effects of REs on colloid transport, this study 72

aimed to fill the knowledge gap by examining differences in the transport of smectite colloids 73

dispersed by REs or HA in saturated sand columns. To do so, transport and retention behaviors 74

of smectite colloids in sand columns were investigated at ionic strength of 0.1 and 10 mM KCl 75

and solution pH of 5, 7 and 9, respectively. Colloid transport and retention mechanisms were 76

elucidated by altering electrostatic and steric forces between colloids and sand surfaces as 77

influenced by HA, REs, or solution pH and ionic strength. 78

MATERIALS AND METHODS 79

Artificial Root Exudates and Humic Acid 80

Artificial root exudates (AREs) of maize were composed of seven carbohydrates (CHs), 81

twelve amino acids (AAs) and four organic acids (OAs) at predetermined ratios, which were 82

adapted from previous reports (Buyanovsky and Wagner, 1997, Guckert et al., 1991, Paul and 83

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Clark, 1996) (Table S1, Supplemental Information). Total organic carbon (TOC) concentration 84

of ARE solution was determined as 12.0 mg C/L using a TOC analyzer (Shamidzu, Kyoto, 85

Japan). Solutions containing individual ARE component such as CHs, AAs or OAs were also 86

prepared and determined to have TOC of 8.0, 0.7 and 3.6 mg C/L, respectively. 87

HA (Elliott Soil HA Standard, 1S102H) was obtained from International Humic 88

Substances Society (St. Paul, MN, USA). To prepare the stock HA solution, 50 mg HA was 89

dissolved in 1 L of deionized (DI) water at pH 7. The HA solution was stirred overnight and then 90

filtered through 0.45 µm membrane. The filtered HA solution was diluted to 12 mg C/L 91

comparable to the TOC concentration of the ARE solution. 92

Colloid Suspensions 93

A reference smectite (SWy-2) clay was obtained from the Clay Minerals Society 94

(Columbia, MO). The smectite clay was saturated with K+ by dispersing 10 g of smectite 95

samples in 1 L of 0.5 M KCl solution as described by Li et al. (2003). Briefly, the smectite 96

suspensions were shaken for 24 h, and then fresh KCl solution was used to displace the original 97

solutions after centrifugation. This process was repeated four times to ensure complete K+ 98

saturation. Afterwards the K+-saturated smectite was thoroughly washed with approximately 1 L 99

of DI water to remove excess salt indicated by a negative test of AgNO3 solution. Finally, the 100

K+-saturated smectite suspension was freeze-dried to obtain dry powers and stored for later use. 101

To prepare colloid suspensions, K+-saturated smectite (100 mg) was suspended in 1 L of 102

ARE solution (12 mg C/L), HA solution (12 mg C/L), DI water, and solutions containing 103

individual ARE component (i.e., CHs, AAs or OAs) at ionic strength of 0.1 and 10 mM (KCl), 104

respectively. The higher level of 10 mM was selected to represent average ionic strength in soil 105

solution (Harter and Naidu, 2001), and the lower level of 0.1 mM to reflect that of soil solution 106

in low-salinity soils or diluted during rainwater percolation events. Under each ionic strength, the 107

pH of smectite suspension was adjusted to 5, 7 and 9 using 0.1 M KOH or HCl solution, 108

respectively. The resultant suspension was then ultrasonicated for 30 min (Misonix S3000). 109

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Intensity-weighed hydrodynamic diameter (Dh), zeta potential and electrophoretic mobility 110

(EPM) of smectite were determined using a Zetasizer Nano-ZS (Malvern Instrument Co., 111

Westborough, MA). Aggregation kinetics of smectite colloids dispersed in ARE solution, water, 112

and HA solution at pH 7 under 0.1 and 10 mM was determined by measuring Dh over the first 30 113

min. Fresh smectite suspensions were used for the following transport experiments, and the 114

colloid-free ARE solutions, water, and HA solutions were used as background solutions. 115

Column Experiments 116

Packed-column experiments were used to investigate the deposition and transport of 117

smectite colloids in water-saturated porous media. Quartz sand (Unimin Co., Ottawa, MN) used 118

in this study was sieved to obtain the size fraction of 0.4–0.5 mm. The sand was washed 119

sequentially by tap water and DI water, oven-dried, and stored for later use. The sand was wet-120

packed into an acrylic column with 2.5 cm in diameter and 12 cm in height. Stainless steel mesh 121

of 50-µm pores (Spectra/Mesh, Spectrum Laboratories, Inc.) were placed at both ends of the 122

column so as to better distribute the flow. A peristaltic pump (Masterflex L/S, Cole Parmer 123

Instrument, Vernon Hills, IL) was connected to the inlet at the top of the column to regulate the 124

downward flow at a flow rate of 2.0 mL/min throughout the experiments. After the column was 125

flushed with colloid-free background solution for three pore volumes (PVs), smectite suspension 126

in the identical background solution was applied to the column for 2 PVs, followed by the final 127

flush with background solution for another 2 PVs. In the tracer experiment, the colloid input 128

suspension was replaced with KBr solution (50 mg/L). The colloid input suspension was 129

continuously stirred on a stirring plate so as to maintain the suspension homogeneity throughout 130

the 4-hour experimental period. Effluent samples were collected from the bottom of the column 131

using a fraction collector (ISCO Retriever 500, Lincoln, NE). The colloid concentration was 132

measured by the absorbance at wavelength of 550 nm using Cary 50 UV-Vis Spectrophotometer 133

(Varian Inc., Palo Alto, CA), and bromide concentration by ICS-2000i ion chromatography 134

(Dionex, Sunnyvale, CA). The baseline absorbance of background effluent was subtracted from 135

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the absorbance of smectite effluent samples. Breakthrough curves (BTCs) were then plotted as 136

normalized effluent concentrations versus PVs. 137

The above procedure constituted Phase 1 of the column experiments, i.e., the deposition 138

stage, in which the smectite colloids were retained in the column. For the smectite colloid 139

suspensions under 10 mM ionic strength, the column experiments were extended to Phase 2 (i.e., 140

the release stage) in which the background solution was switched to DI water in order to release 141

the smectite colloids retained at the secondary energy minimum as commonly implemented in 142

other studies (Hahn et al., 2004, Sang et al., 2013, Shen et al., 2007). It is generally agreed that 143

the secondary minimum is eliminated when switching to DI water, and consequently the colloids 144

retained at the secondary minimum are re-entrained back to bulk water and thus transported out 145

of the column. We selected the experiments under 10 mM ionic strength for the Phase 2 due to 146

appreciable smectite colloid deposition during Phase 1. Colloid mass recoveries from the 147

effluents in the Phase 1 (M1) and Phase 2 (M2) were calculated from the BTCs by dividing 148

colloid mass recovered from the effluents by the total applied colloid mass. The amount of 149

colloids retained in the Phase 1 (Md1) could be calculated as 1−M1. The amount of colloids 150

remaining in the column after the Phase 2 (Md2) was determined as 1−M1−M2, which was 151

considered to be retained by primary energy minimum and/or pore straining rather than the 152

secondary minimum (Sang et al., 2013). The fraction of released colloids in the Phase 2 over the 153

total retained colloid in the Phase 1 (Mr) was calculated as M2/Md1. 154

Mathematical Model 155

An advection-dispersion equation coupled with first-order kinetic deposition was used to 156

describe the BTCs of smectite colloids or bromide tracer in the porous media with zero 157

deposition term for the tracer (Grolimund et al., 1998). The governing equation can be written as: 158

kCz

Cv

z

CD

t

C−

∂

∂−

∂

∂=

∂

∂

2

2

(1) 159

where C is the aqueous smectite concentration, t is the lapsed time, D is the hydrodynamic 160

dispersion coefficient, v is the pore water velocity, z is the travel distance in the direction of flow, 161

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and k is the first-order deposition rate coefficient. This model was applied to the experimental 162

BTCs using CXTFIT Code 2.0 (Tang et al., 2010) with a zero initial concentration, a pulse-input 163

boundary condition and a zero-concentration-gradient boundary condition at the outlet. The 164

Levenberg-Marquardt algorithm was used to estimate transport parameters. Hydrodynamic 165

properties of the columns was characterized by the bromide tracer experiment, and the value of 166

D was estimated from fitting the bromide BTC. Assuming the same D value for bromide and 167

smectite colloids, the best-fit values of k were then estimated (Simunek et al., 2008). 168

The overall experiments were designed to elucidate the contrasting effects of AREs and 169

HA on the stability and mobility of smectite colloids by manipulating surface interaction forces 170

with varying solution parameters, i.e., dispersant type (i.e., ARE solution, HA solution, or DI 171

water), solution pH, and ionic strength. Water-dispersed smectite suspensions were used as 172

organic-free control treatment. We first investigated the aggregation kinetics of ARE-, HA-, and 173

water-dispersed smectite suspensions at pH 7 and ionic strength of 0.1 mM and 10 mM, followed 174

by the column transport experiments at ionic strength of 0.1 and 10 mM and solution pH of 5, 7, 175

and 9, respectively. In addition, the transport of smectite colloids dispersed in either CH, AA or 176

OA component of AREs was investigated at 0.1 mM ionic strength and solution pH 5, 7, and 9 177

so as to identify the ARE component primarily responsible for the effect of AREs on colloid 178

transport. Finally, colloid retention mechanisms were explored by examining colloid retention 179

and release behaviors before and after elution with DI water. At the following, experimental 180

results were presented and discussed according to this overall experimental design. 181

RESULTS AND DISCUSSION 182

Aggregation Kinetics 183

As shown in Figure 1, compared with the water-dispersed (600 nm) and ARE-dispersed 184

smectite (609 nm), the initial Dh of HA-dispersed smectite (485 nm) was lower under 10 mM 185

ionic strength and pH 7. It could be due to stronger stabilization effect of HA on smectite 186

colloids during the ultrasonication process, resulted from increased electrostatic and steric 187

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repulsions induced by HA coatings on colloid surface (Zhang et al., 2013). As shown in Table 1, 188

surface charge of smectite colloids dispersed in HA solution was more negative than the ones 189

dispersed in water and ARE solutions at all pHs, which clearly demonstrated enhanced 190

electrostatic repulsion for HA-dispersed smectite colloids. While we did not measure steric 191

repulsion per se, steric repulsion offered by HA coatings can be important, given the ample 192

evidence in the literature (Franchi and O'Melia, 2003, Morales et al., 2011, Wang et al., 2013, 193

Zhang et al., 2013). 194

The aggregation kinetics during the first 30 min (Figure 1) indicated that under lower 195

ionic strength (0.1 mM KCl) the aggregation of smectite colloids was slow and no obvious 196

difference was found among three dispersion methods. Under higher ionic strength (10 mM KCl), 197

the aggregation of HA-dispersed smectite was slightly greater than that under lower ionic 198

strength, whereas the aggregation of water-dispersed and ARE-dispersed smectite became much 199

more pronounced. Clearly, ionic strength had more impact on the aggregation of water- and 200

ARE-dispersed smectite than that of HA-dispersed smectite. As discussed previously, this could 201

be due to increased electrostatic and/or steric repulsions provided by HA. ARE-dispersed 202

smectite had the largest aggregate size at the end of aggregation experiment, indicating that 203

repulsion between smectite colloids was much more limited in the ARE solutions. 204

Deposition of Smectite in Sand Columns 205

The tracer BTC was well fitted with the advection-dispersion equation (Figure S1, 206

Supplemental Information), suggesting that the saturated sand column was free of wall-effect 207

and short-circuit and preferential flows. Transport of smectite colloids in saturated sand columns 208

showed typical colloid breakthrough characteristics (Figure 2), as evidenced by symmetrical 209

BTCs with effluent concentration plateau and minimal retardation (Bradford et al., 2009, 210

Bradford and Torkzaban, 2008). The BTCs of smectite colloids were successfully described by 211

the advection-dispersion equation with first-order kinetic deposition (R2 > 0.97, Table 2), and the 212

model fitting parameters are shown in Table 2. 213

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First, we examined the mobility of smectite colloids under three pHs at low ionic strength 214

of 0.1 mM (Figure 2A-C and Table 2). The deposition rate coefficients (k) for all the smectite 215

suspensions studied were low at 0.1 mM ionic strength (Table 2), indicating relatively low 216

retention in the sand column. At pH 5, more ARE-dispersed colloids were retained than water- 217

and HA-dispersed colloids (Figure 2A and Table 2), but the difference diminished with 218

increasing pH (Figure 2B-C). At pH 9, colloid retention was negligible with effluent recovery of 219

nearly 100% (Table 2). This trend clearly indicates the role of electrostatic interactions in colloid 220

deposition by altering surface charge of colloids or sand grains. Measured zeta potential of ARE-221

dispersed smectite was changed from −46.0 ± 1.9 mV to −36.3 ± 1.4 mV when solution pH was 222

lowered from 9 to 5 (Table 1). Similarly, the negative surface charge of sand grains also 223

decreased in magnitude with lowering solution pH, as measured in our previous study (Zhang et 224

al., 2012). Therefore, the increased retention of ARE-dispersed smectite at pH 5 was probably 225

due to decreased electrostatic repulsion. Nonetheless, the difference between ARE-, water-, and 226

HA-dispersed smectite at pH 5 cannot be explained solely by average electrostatic interaction, 227

because their zeta potentials differed only by 3.6 mV (Table 1). Given that AREs are a mixture 228

of CH, AA and OA compounds, the contributions from these ARE components need to be 229

understood in order to better explore other mechanisms, which will be further elucidated later. 230

The plausible mechanisms may include increased surface heterogeneities or inter-surface 231

bridging, due to interactions of AREs with smectite and sand grains (probably involving some 232

AAs), which typically enhance colloid deposition by lowering total surface interaction energy or 233

cross-linking colloids and sand surfaces (Bouchard et al., 2012, Crespilho et al., 2009, Ryan and 234

Elimelech, 1996, Tufenkji and Elimelech, 2005, Zakaria et al., 2013). This could obviously 235

explain the different retention between ARE- and water-dispersed smectite colloids. This 236

inhibitory effect of AREs on colloid mobility is thus illustrated in Figure 3. Conversely, the 237

presence of HA would not only increase the negative surface charge (Table 1), but also introduce 238

steric repulsion, thus contributing to increased total repulsive interaction energy and enhanced 239

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colloid mobility (Figure 3). Nonetheless, it appears that total surface interaction energy between 240

water-dispersed smectite and sand grains was sufficiently repulsive with the effluent recovery 241

approaching 100%. Thus, the addition of HA could not further decrease the retention of smectite. 242

In order to identify the component of AREs that was responsible for the enhanced colloid 243

retention observed in Figure 2A, the BTCs of colloids dispersed in solutions of individual ARE 244

component are shown in Figure 2D-F. More colloids in AA solution were retained, followed by 245

colloids in OA and CH solutions (Figure 2D-F). Therefore, it is likely that the AA component in 246

AREs was responsible for the enhanced retention of ARE-dispersed colloids compared with 247

water- and HA-dispersed colloids. It is known that within the test pH range CHs are neutral 248

species and OAs carry net negative charges, whereas most AAs are zwitterionic with net positive 249

charges at pH 5, and neutral or negative charge at pH 7 and 9 (Table S2-S4). Among twelve AAs 250

in the AREs, six AAs (i.e., alanine, isoleucine, leucine, methionine, phenylalanine, tyrosine) 251

have hydrophobic side-chains, and one particular AA (i.e., lysine) always carry net positive 252

charge at all pHs (Table S3). As adsorption of AAs by clays primarily results from electrostatic 253

interaction through positive charged amine group with the negatively charged clay surface 254

(Henrichs and Sugai, 1993, Wang and Lee, 1993), it is likely that this association of AAs 255

(particularly lysine) may neutralize the negative charges on the surfaces of smectite and sand, 256

which not only decreases electrostatic repulsion, but also creates local surface heterogeneities 257

due to hydrophobic side-chains of many AAs. Binding of AAs with the solid surfaces may also 258

promote bridging through two amine groups for some AAs (e.g., lysine) by electrostatic 259

interaction or hydrogen bonding (Crespilho et al., 2009, Zakaria et al., 2013). These effects 260

collectively contributed to greater deposition of smectite colloids in the presence of AAs. 261

Nonetheless, no difference among the zeta potentials of AA-, OA-, and water-dispersed smectite 262

colloids at pH 5 remained to be explained. But this seems to support the abovementioned 263

mechanisms of surface heterogeneities or inter-surface bridging, because otherwise the 264

difference in the transport of AA- and water-dispersed smectite would not be observed. Similarly, 265

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the mechanisms underlying the more negative zeta potentials of CH-dispersed smectite are 266

unclear. Neutral CHs may be intercalated into the interlayers of smectite colloids (Greenland, 267

1956a, Greenland, 1956b, Lynch et al., 1956), as the relatively less hydrated smectite interlayers 268

(compared to bulk solution) facilitates the intercalations of neutral organic compounds from 269

aqueous solution (Li et al., 2004a, Liu et al., 2009). But it is unknown how intercalation of CHs 270

influences the zeta potential of smectite colloids. Alternatively, CHs may coordinate directly 271

with exchangeable cations or form hydrogen bonding with hydration water of the cations 272

(McBride, 1994), thus shielding the positive charge of cations and leading to more negative zeta 273

potential. Finally, the enhancing effect of AA component appeared to be masked for the ARE-274

dispersed smectite colloids at higher pH (Figure 2 and Table 2). This was likely because the 275

enhancing effect was negated by the opposite effect from the overwhelming concentration of 276

negative charged OA species at high pH (Table S4) (Zakaria et al., 2013). 277

At higher ionic strength level (i.e., 10 mM), the difference among the transport of ARE-, 278

water-, and HA-dispersed colloids was significantly enhanced (Figure 2G-I), compared to the 279

results measured at lower ionic strength (Figure 2A-C). Similarly, the effect of solution pH on 280

colloid transport was also signified at higher ionic strength. This was resulted from 281

simultaneously enhanced aggregation and deposition under high ionic strength, because of 282

reduced electrostatic repulsion. Interestingly, there was no difference in the transport of water-283

dispersed smectite at three pHs (Table 2), indicating that the observed pH effects on the transport 284

of ARE- and HA-dispersed smectite (Figure 3) were largely due to surface charge and 285

conformation changes of organic-coated smectite colloids induced by changing solution pH. In 286

addition to electrostatic interaction, smectite colloids is known to adsorb more HA than CHs and 287

AAs (Feng et al., 2005), thus leading to greater steric repulsion. Consequently, the retention of 288

smectite was lowest in the presence of HA. 289

Release of Smectite from Sand Columns 290

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The release of retained smectite colloids from the sand column under pH 5, 7 and 9 are 291

shown in Table 3 and Figure 4. Compared with smectite colloids dispersed in water and HA 292

solution, the ARE-dispersed colloids had lower release percentage (Mr) under all three pHs, e.g., 293

Mr was 20% for ARE-dispersed smectite compared with 61% for water-dispersed smectite and 294

56% for HA-dispersed smectite at pH 5. Consequently, the amount of colloids remained in the 295

column after the Phase 2 (Md2) were the greatest for the ARE-dispersed colloids, followed by the 296

water-dispersed and HA-dispersed colloids. As the secondary energy minimal were eliminated 297

during the Phase 2, the greater retention of the ARE-dispersed smectite colloids could be due to 298

primary energy minimum or pore straining (Sang et al., 2013). Since the quartz sand surface 299

contains surface chemical heterogeneous sites such as coatings of metal oxides with variable 300

surface charge under changing solution pH (Ryan and Elimelech, 1996, Zhang et al., 2012), it is 301

expected that the retention at the primary minimum would decrease with increasing solution pH 302

(Zhou et al., 2011), consistent with our observations for all tested smectite colloid suspensions 303

(Table 3). Nonetheless, it is not certain whether the positively charged sites are completely 304

masked at pH 9 because typical isoelectric points of aluminum or iron oxides may range up to 305

pH 10 (Zhang et al., 2012). Thus, the retained colloids at pH 9 might be partially retained at the 306

primary minimum, but mainly retained by pore straining. Therefore, pore straining could retain 307

up to 16% of the ARE-dispersed colloids, 12% of water-dispersed colloids, and 5% of HA-308

dispersed colloids at pH 9. However, pore straining may play a more significant role at lower pH, 309

as more colloids weakly associated with the solid-water interface may be carried by water flow 310

to pore straining sites hydrochemically favorable for retention such as grain-grain contacts, and 311

sand surface pits, valleys, and crevices (Bradford and Torkzaban, 2008, Bradford et al., 2007, 312

Shen et al., 2011). 313

Additionally, these findings indicated the stronger affinity of ARE-dispersed smectite 314

colloids to the porous media than the water- and HA-dispersed ones. Compared with HA, 315

sorption of AREs on the smectite could potentially counteract the original negative charges on 316

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the surfaces of smectite. Introducing the HA onto the smectite could enhance the negative charge 317

on the surfaces or induce steric repulsion (Figure 3). As a result of increased negative surface 318

charge and sorbed NOM layers, HA-dispersed smectite showed the enhanced repulsion and 319

weaker affinity to the surface of porous media than ARE-dispersed smectite. 320

CONCLUSION 321

Aggregation and transport behaviors of dispersed smectite colloids using ARE solution, 322

water, and HA solution were investigated at 0.1 and 10 mM KCl ionic strength and pH 5, 7 and 323

9. Stronger stabilization effects of HA in dispersion of smectite was found, compared with that 324

of AREs and water, due to electrosteric repulsions offered by HA coatings. The ARE-dispersed 325

smectite colloids were more retained than water- and HA-dispersed colloids, due to the 326

contribution of amino acids in ARE solution. At higher ionic strength level, the difference among 327

the transport of ARE-, water-, and HA-dispersed colloids was significantly enhanced, due to the 328

reduced electrostatic repulsion and greater adsorption of HA. Our findings suggest that, during 329

rainfall events, in contrary to the role of humic substances the REs may help retain colloidal 330

particles (e.g., natural clay colloids) in the root zone. In sandy soils, root exudates produced from 331

established healthy plant roots could retard the downward eluviation of clays, and accumulate the 332

soil clays in the plant root zone, thus ameliorating low water and nutrient retention capacity of 333

the sandy soils. In the context of contaminant transport, root exudates in the plant root zone 334

could reduce deep leaching of clay-associated contaminants, thus potentially protecting 335

groundwater and augmenting phytoremediation at contaminated sites. Given that this study was 336

performed with one type of clay (i.e., smectite) and one TOC concentration under laboratory 337

conditions, future study should focus the effects of root exudate concentrations and clay types, 338

and corroborate the laboratory findings with well-designed field research. 339

ACKNOWLEDGMENTS 340

This research was funded by USDA-NIFA Hatch Program (MICL02248) and USDA-341

NRCS Conservation Innovation Grant (69-3A75-13-93). The views and opinions of the authors 342

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15

expressed herein do not necessarily state or reflect those of the authors’ organizations or the 343

funding agencies. Mention of trade names or commercial products does not constitute 344

endorsement or recommendation for use. 345

Supplemental information is available in the online version of this article, including 346

bromide tracer breakthrough curve, composition of AREs, charge calculations of carbohydrates, 347

amino acids and organic acids. 348

349

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510

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512

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Figure Captions 513

Figure 1. Aggregation kinetics of smectite colloids respectively dispersed in artificial root 514

exudate (ARE) solution (12 mg C/L), water, and humic acid (HA) solution (12 mg C/L) at pH 7 515

and ionic strength of 0.1 or 10 mM KCl. 516

Figure 2. Breakthrough curves (BTCs) of smectite colloids respectively dispersed in water or 517

artificial root exudate (ARE), humic acid (HA), carbohydrate (CH), amino acid (AA), and 518

organic acid (OA) solutions at pH 5, 7 and 9 and ionic strength of 0.1 or 10 mM KCl. Symbols 519

are experimental data and lines are model results. 520

Figure 3. Schematic of smectite colloids dispersed by humic acid (HA) and artificial root 521

exudates (AREs) consisting of carbohydrates (CHs), amino acids (AAs) and organic acids 522

(OAs). 523

Figure 4. Release of smectite colloids respectively dispersed in artificial root exudate (ARE) 524

solution, water, and humic acid (HA) solution in saturated sand column at 10 mM KCl ionic 525

strength and solution pH of (A) 5, (B) 7 and (C) 9. 526

527

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Tables 528

Table 1. Zeta potential and electrophoretic mobility (EPM) of smectite under various conditions. 529

Dispersant

Ionic

Strength

(mM)

Zeta potential (mV) EPM (×10-8

m2/(Vs))

pH = 5 pH = 7 pH = 9 pH = 5 pH = 7 pH = 9

AREs 0.1 -36.3 ± 1.4 -38.7 ± 1.5 -46.0 ± 1.9 -2.84 ± 0.11 -3.04 ± 0.12 -3.61 ± 0.15

Water 0.1 -37.6 ± 0.8 -41.0 ± 2.1 -48.6 ± 0.8 -2.95 ± 0.07 -3.21 ± 0.16 -3.81 ± 0.06

HA 0.1 -39.9 ± 1.2 -40.1 ± 1.6 -48.8 ± 1.4 -3.13 ± 0.09 -3.14 ± 0.12 -3.83 ± 0.11

AREs 10 -18.1 ± 0.5 -21.0 ± 0.5 -23.5 ± 0.7 -1.42 ± 0.04 -1.65 ± 0.04 -1.84 ± 0.05

Water 10 -22.6 ± 0.9 -23.7 ± 0.6 -23.1 ± 0.4 -1.78 ± 0.07 -1.86 ± 0.05 -1.81 ± 0.04

HA 10 -30.7 ± 0.6 -33.0 ± 0.6 -32.5 ± 1.4 -2.41 ± 0.05 -2.59 ± 0.05 -2.55 ± 0.11

CH 0.1 -43.6 ± 2.9 -44.0 ± 2.7 -45.6 ± 2.8 -3.42 ± 0.23 -3.45 ± 0.21 -3.57 ± 0.22

AA 0.1 -36.8 ± 0.8 -37.3 ± 1.7 -39.5 ± 2.2 -2.89 ± 0.06 -2.93 ± 0.13 -3.10 ± 0.17

OA 0.1 -35.5 ± 1.5 -45.6 ± 2.1 -44.6 ± 2.6 -2.79 ± 0.12 -3.57 ± 0.17 -3.50 ± 0.20

530

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Table 2. Summary of effluent mass recoveries and model results for transport of smectite 531

colloids under various conditions. 532

Dispersant

Ionic

Strength

(mM)

Effluent mass recoveries

(M1)

Deposition rate

coefficient (k, min-1

) R

2

pH=5 pH=7 pH=9 pH=5 pH=7 pH=9 pH=5 pH=7 pH=9

AREs 0.1 0.89 0.95 0.99 0.012 0.006 0.000 1.00 0.99 1.00

Water 0.1 1.00 1.00 1.01 0.002 0.003 0.000 1.00 0.99 1.00

HA 0.1 0.99 1.00 1.01 0.001 0.000 0.000 0.99 1.00 1.00

AREs 10 0.30 0.50 0.61 0.123 0.070 0.051 0.99 0.99 0.99

Water 10 0.56 0.56 0.56 0.059 0.059 0.059 0.98 0.99 0.98

HA 10 0.68 0.73 0.74 0.039 0.032 0.030 1.00 0.99 1.00

CH 0.1 0.96 0.98 0.97 0.003 0.001 0.002 0.99 0.99 0.98

AA 0.1 0.84 0.87 0.91 0.016 0.012 0.008 0.99 0.99 1.00

OA 0.1 0.86 0.97 0.99 0.014 0.002 0.000 0.99 1.00 1.00

533

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Table 3. Colloid retention and release during the Phase 1 (the deposition stage) and Phase 2 (the 534

release stage) for smectite respectively dispersed in artificial root exudate (AREs) solution (12 535

mg C/L), water, and humic acid (HA) solution (12 mg C/L) in saturated porous media under 10 536

mM KCl ionic strength and solution pH of 5, 7, and 9. 537

pH Dispersant

Phase 1 Phase 2 Colloid retained

after Phase 2

(Md2, fraction of

total applied)

Colloid

retained (Md1,

fraction of

total applied)

Colloid recovered

from effluents

(M1, fraction of

total applied)

Colloid recovered

from effluents

(M2, fraction of

total applied)

Colloid released

(Mr, fraction of

total retained)

5 AREs 0.70 0.30 0.14 0.20 0.56

5 Water 0.44 0.56 0.27 0.61 0.17

5 HA 0.32 0.68 0.18 0.56 0.14

7 AREs 0.50 0.50 0.21 0.42 0.29

7 Water 0.44 0.56 0.29 0.66 0.15

7 HA 0.27 0.73 0.19 0.70 0.08

9 AREs 0.39 0.61 0.23 0.59 0.16

9 Water 0.44 0.56 0.32 0.73 0.12

9 HA 0.26 0.74 0.21 0.81 0.05

538

539

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Figure 1. Aggregation kinetics of smectite colloids respectively dispersed in artificial root exudate (ARE) solution (12 mg C/L), water and humic acid (HA) solution (12 mg C/L) at pH 7 and ionic strength of 0.1 or

10 mM KCl. 179x142mm (300 x 300 DPI)

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Figure 2. Breakthrough curves (BTCs) of smectite colloids respectively dispersed in water or artificial root exudate (ARE), humic acid (HA), carbohydrate (CH), amino acid (AA), and organic acid (OA) solutions at pH

5, 7 and 9 and ionic strength of 0.1 or 10 mM KCl. Symbols are experimental data and lines are model

results. 202x160mm (300 x 300 DPI)

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Figure 3. Schematic of smectite colloids dispersed by humic acid (HA) and artificial root exudates (AREs) consisting of carbohydrates (CHs), amino acids (AAs) and organic acids (OAs).

100x74mm (300 x 300 DPI)

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Figure 4. Release of smectite colloids respectively dispersed in artificial root exudate (ARE) solution, water, and humic acid (HA) solution in saturated sand column at 10 mM KCl ionic strength and solution pH of (A) 5,

(B) 7 and (C) 9. 106x29mm (300 x 300 DPI)

Page 28 of 33Soil Sci. Soc. Am. J.Accepted paper, posted 01/13/2015. doi:10.2136/sssaj2014.10.0412

Supplemental Information 1

Plant root exudates decrease mobility of smectite colloids in porous media in 2

contrast to humic acid 3

4

Yuan Tian1, Cheng-Hua Liu1,2, Alvin J.M Smucker1, Hui Li1, Wei Zhang1,2* 5

6 1 Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI 7

48824 8 2 Environmental Science and Policy Program, Michigan State University, East Lansing, MI 48824 9

10

11

* Corresponding Author, phone: (517) 355-0271 ext. 1244, fax: (517) 355-0270, email: 12

weizhang@msu.edu 13

14

5 pages, 1 figure, and 4 tables. 15

16

1

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Figure S1. Breakthrough curve (BTC) of bromide (Br) in saturated sand column. Symbols are 18

experimental data and lines are model results. 19

20

0 1 2 3 4 50.0

0.2

0.4

0.6

0.8

1.0

Data Model

C/C

o

Pore Volume

2

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Table S1. Components and concentrations of artificial root exudates (AREs) †. 21 Carbo-

hydrates

Molecular

formula

Concentration Amino

acids

Molecular

formula

Concentration Organic

acids

Molecular

formula

Concentration

mg/L µM mg/L µM mg/L µM

Arabinose C5H10O5 1.4 9.3 Alanine C3H7NO2 0.1 1.1 Acetic acid C2H4O2 2.1 35.0

Galactose C6H12O6 4.0 22.2 Asparagine C4H8N2O3 0.4 3.0 Butyric acid C4H8O2 2.1 23.8

Glucose C6H12O6 3.6 20.0 Glutamine C5H10N2O3 0.4 2.7 Malonic acid C3H4O4 2.1 20.2

Mannose C6H12O6 2.9 16.1 Glycine C2H5NO2 0.2 2.7 Succinic acid C4H6O4 2.1 17.9

Ribose C5H10O5 2.0 13.3 Isoleucine C6H13NO2 0.1 0.8

Sucrose C12H22O11 4.1 12.0 Leucine C6H13NO2 0.1 0.8

Xylose C5H10O5 1.6 10.7 Lysine C6H14N2O2 0.1 0.7

Methionine C5H11NO2S 0.4 2.7

Phenylalanine C9H11NO2 0.1 0.6

Proline C5H9NO2 0.9 7.8

Tyrosine C9H11NO3 0.4 2.2

Valine C5H11NO2 0.3 2.6

Total: 19.5 103.6 Total: 3.4 27.6 Total: 8.4 96.8

† Adapted from previous reports (Buyanovsky and Wagner, 1997, Guckert et al., 1991, Paul and 22 Clark, 1996) 23 24 25 26 Table S2. Charges of carbohydrates (CHs) under pH 5, 7 and 9. 27

Carbo- hydrates

pKa † PZC ‡ pH = 5 pH = 7 pH = 9 §

+ o - + o - + o - Arabinose 12.46 12.46 0 100 0 0 100 0 0 100 0 Galactose 12.35 12.35 0 100 0 0 100 0 0 100 0 Glucose 12.46 12.46 0 100 0 0 100 0 0 100 0 Mannose 12.08 12.08 0 100 0 0 100 0 0 100 0 Ribose 12.11 12.11 0 100 0 0 100 0 0 100 0 Sucrose 12.62 12.62 0 100 0 0 100 0 0 100 0 Xylose 12.15 12.15 0 100 0 0 100 0 0 100 0

† pKa values are obtained from (Speight and Lange, 2005). 28 ‡ PZC: point of zero charge 29 § +: positive; O: neutral; -: negative 30

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Table S3. Charges of amino acids (AAs) under pH 5, 7 and 9. 32

Amino acids pKa †

PZC ‡

pH = 5 pH = 7 pH = 9 §

pKa1 pKa2 pKa3 + o - + o - + o - Alanine 2.34 9.69 6.00 0.2 99.8 0.0 0.0 99.8 0.2 0.0 83.0 17.0 Asparagine 2.02 8.80 5.41 0.1 99.9 0.0 0.0 98.4 1.6 0.0 38.7 61.3 Glutamine 2.17 9.13 5.65 0.1 99.9 0.0 0.0 99.3 0.7 0.0 57.4 42.6 Glycine 2.34 9.60 5.97 0.2 99.8 0.0 0.0 99.7 0.3 0.0 79.9 20.1 Isoleucine 2.36 9.60 6.02 0.2 99.8 0.0 0.0 99.7 0.3 0.0 79.9 20.1 Leucine 2.36 9.60 5.98 0.2 99.8 0.0 0.0 99.7 0.3 0.0 79.9 20.1 Lysine 2.18 8.95 10.53 9.74 99.8 0.2 0.0 98.9 1.1 0 52.9 47.1 0.0 Methionine 2.28 9.21 5.74 0.2 99.8 0.0 0.0 99.4 0.6 0.0 61.9 38.1 Phenylalanine 1.83 9.13 5.48 0.1 99.9 0.0 0.0 99.3 0.7 0.0 57.4 42.6 Proline 1.99 10.6 6.3 0.1 99.9 0.0 0.0 100.0 0.0 0.0 97.5 2.5 Tyrosine 2.2 9.11 5.66 0.2 99.8 0.0 0.0 99.2 0.8 0.0 56.3 43.7 Valine 2.32 9.62 5.96 0.2 99.8 0.0 0.0 99.8 0.2 0.0 80.7 19.3

† pKa values are obtained from (Speight and Lange, 2005). 33 ‡ PZC: point of zero charge 34 § +: positive; O: neutral; -: negative 35 36 37 38

Table S4. Charges of organic acids (OAs) under pH 5, 7 and 9. 39

Organic acids

pKa † PZC

‡

pH = 5 pH = 7 pH = 9 §

pKa1 pKa2 o - - - o - - - o - - - Acetic acid 4.75 4.75 36.0 64.0 0.6 99.4 0.0 100.0 Butyric acid 4.82 4.82 39.8 60.2 0.7 99.3 0.0 100.0 Malonic acid 2.83 5.69 2.83 0.6 82.6 16.9 0.0 4.7 95.3 0.0 0.0 100.0 Succinic acid 4.16 5.61 4.16 10.4 71.9 17.7 0.0 3.9 96.1 0.0 0.0 100.0

† pKa values are obtained from (Speight and Lange, 2005). 40 ‡ PZC: point of zero charge 41 § O: neutral; -: negative for pKa1; - -: negative for pKa2 42

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REFERENCES 44

Buyanovsky, G.A., and G.H. Wagner. 1997. Crop residue input to soil organic matter on Sanborn 45

Field. In: E.A. Paul, K.H. Paustian, E.T. Elliott and C.V. Cole, Soil Organic Matter in 46

Temperate Agroecoystems: Long-Term Experiments in North America. CRPC Press, Inc., 47

Boca Raton, FL. p. 73-84. 48

Guckert, A., M. Chavanon, M. Mench, J.L. Morel, and G. Villemin. 1991. Root exudation in beta 49

vulgaris: A comparison with Zea mays. In: B.L. McMichael and H. Persson, Developments 50

in Agricultural and Managed Forest Ecology. Elsevier. p. 449-455. 51

Paul, E.A., and F.E. Clark. 1996. Soil Microbiology and Biochemistry. Academic Press, San 52

Diego, CA. 53

Speight, J.G., and N.A. Lange. 2005. Lange's Handbook of Chemistry. McGraw-Hill, New York. 54

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