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Journal of Environmental Quality 32:816-823 (2003)
© 2003 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America

TECHNICAL REPORTS
Ground Water Quality

Virus Retention and Transport as Influenced by Different Forms of Soil Organic Matter

Jie Zhuang and Yan Jin*

Department of Plant and Soil Sciences, Univ. of Delaware, Newark, DE 19717-1303

* Corresponding author (yjin{at}udel.edu)

Received for publication April 25, 2002.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Organic materials are widespread in natural soil and aquatic environments. Their effect on virus transport is very important in assessing the risk for contamination of ground water by viruses. This study aimed to determine how different forms (mineral-associated and dissolved) of natural organic matter influence the retention and transport of two bacteriophages (MS-2 and {phi}X174) in two porous media (a sand and a soil). We found that mineral-associated organic matter significantly promoted the transport of one virus (MS-2) but not the other ({phi}X174) in a phosphate-buffered saline solution. Similarly, MS-2 was retained less in sand columns with increasing concentrations of dissolved humic acid, while little effect was observed for {phi}X174 under the same conditions. The two viruses have different surface properties and thus exhibited different reactivity to the metal oxides present on sand particles and were affected differently by organic matter. Because the organic matter used in the study was negatively charged and hydrophilic, blocking of virus sorption sites and increasing of virus–medium electrostatic repulsion arising from modification of the sand and virus surface by organic matter are probably responsible for the facilitated transport. For dissolved humic acid, its competition for sorption sites with viruses was an additional mechanism involved. This study suggests that the effect of organic matter varied depending on the organic material properties and the type of viruses involved. As a general trend, the effect of organic matter was dominated by electrostatic rather than hydrophobic interactions.

Abbreviations: BP, breakthrough percentage • GA, Georgia soil • HA, humic acid • OM, organic matter • PBS, phosphate-buffered saline • PV, pore volume • WWS, water-washed sand


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
THE MICROBIAL QUALITY of ground water has particular public health importance because numerous urban centers around the world rely on ground water as their major source of drinking water. Previous research has demonstrated that enteric viruses of fecal origin survive in and are transported by ground water (Gerba, 1985). Viruses have been found even in fully treated drinking waters (Rose et al., 1986). Every year, about 70% of the waterborne disease outbreaks in the United States can be attributed to contaminated ground water (Craun, 1991; Herwaldt et al., 1992). Wastewater effluents, sewage wastes, leaking septic tanks, private waste-disposal systems, and municipal sanitary landfills are common sources of bacterial and viral pathogens in contaminated ground water (Yates et al., 1985). Therefore, understanding the fate and transport of viruses in soil and ground water is critical for designing protective zones around water supply wells and developing regulations such as the Ground Water Rule (Macler and Merkle, 2000).

Many studies have been conducted both in the laboratory and field to investigate sorption, inactivation, and transport of various viruses in different porous media (Bales et al., 1995; DeBorde et al., 1999; Jin et al., 1997; Pieper et al., 1997; Schijven et al., 1999; Zhuang and Jin, 2003). It has been demonstrated that temperature, solution chemistry, clay composition, metal oxides, degree of saturation of the solid media, and virus strains are primary factors influencing virus survival and transport in the subsurface environment (Jin and Flury, 2002).

The presence of organic materials is another important factor influencing virus fate and transport in porous media (Gerba et al., 1975). Organic materials are present in almost all subsurface media, although their quantities vary. In most natural soils, the organic matter (OM) content is lower than 50 g kg-1 and the average dissolved organic carbon (OC) concentration in ground water is approximately 1 mg L-1 (Leenheer et al., 1974; Thurman, 1985). Viruses are sometimes released into the subsurface through media such as septic tank liquids that contain high concentrations of organic C. In these natural media, organic materials, more than 90% of which consists of humic acid and fulvic acid (Shimizu et al., 1998), exist in the aqueous phase (Thurman, 1985). They can influence transport of contaminants directly (McCarthy and Zachara, 1989) as well as indirectly by being adsorbed as a film on the surfaces of solid grains, which alters the surface charge and aggregation behavior of reactive Fe and Al oxides and layer silicate minerals (Kretzschmar et al., 1997; Zhuang and Yu, 2002). These reactions can greatly affect virus–particle interactions at the solid–liquid interface and therefore virus mobility.

In a review by Schijven and Hassanizadeh (2000), the researchers pointed out that effects of OM are probably responsible for the considerable uncertainties associated with predicting virus removal and transport in porous media. Contradictory results on the OM effect on virus behavior have been reported in the literature. On the one hand, studies have shown that presence of OM can reduce virus attachment (Gerba, 1984) and thus facilitate virus transport by providing additional negative charges, covering positively charged sites, or competing with viruses for attachment sites (Bixby and O'Brien, 1979; Fuhs et al., 1985; Gerba et al., 1975; Moore et al., 1981; Pieper et al., 1997; Powelson et al., 1991). On the other hand, researchers have also observed that OM inhibits virus transport by promoting hydrophobic interactions between viruses and grain surfaces (Bales et al., 1993; Kinoshita et al., 1993). Clearly, ambiguity exists in the literature, which hinders our ability to make definite conclusions about the effect of organic materials on virus behavior.

A major obstacle to understanding the effect of OM on virus behavior in porous media is the lack of experiments that investigate the phenomenon in a systematic manner using OM having a variety of forms and properties with different viruses. The primary objective of this study was to examine the effects of both mineral-associated and dissolved organic materials on virus retention during transport through saturated sand columns. By conducting column experiments, we first studied the effect of mineral-associated OM using both OM-coated sand and a soil containing natural OM. Then the effect of dissolved organic matter was investigated with input virus solutions containing various concentrations of humic acid.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Preparation of Porous Materials
The porous media selected in this study included Accusand (Unimin Corporation, Le Sueur, MN) and a Georgia soil (Thermic Typic Haplohumod), which was collected from Brunswick, GA and provided by Dr. Lena Ma of the University of Florida. The sand and soil were treated in five different manners to obtain the following materials that have different properties: water-washed sand (WWS), organic matter–coated sand (OM-coated WWS), metal oxides–removed sand (oxides-removed WWS), Georgia soil (GA), and Georgia soil with natural organic matter removed (OM-removed GA). Table 1 lists some of the physical and chemical properties of these materials.


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  		Table 1. Some physical and chemical properties of experimental materials.

 
The WWS was prepared by washing the grain size-mixed Accusand in tap water until the rinse water was free of suspended impurities, rinsing with deionized water, and oven-drying at 105°C. The OM-coated WWS was prepared by coating an organic material on the WWS. The organic material (Code BS103P, from the International Humic Substances Society) contained 45.7% carbon, 3.13% nitrogen, 4.74% hydrogen, and 15% ash. The coating method is briefly described as follows. First, in a plastic beaker, 20 g of the organic material was dissolved in 200 mL KOH (0.1 M) and stirred for 30 min. Next, 200 g of oxides-removed WWS was added to the OM suspension and stirred vigorously for 10 min. The suspension was then allowed to stand for approximately 8 h during which it was stirred for 10 min once every hour. Subsequently, 6 M HCl was titrated into the suspension under well-mixed conditions until the suspension pH reached 2.0. The suspension was kept at a constant temperature of 70°C for 24 h and stirred periodically. Finally, the coated sand was washed using deionized water until there was no impurity in the supernatant. To obtain the OM-removed GA, we treated the Georgia soil three times with NaOCl according to the procedure of Lavkulich and Wiens (1970) to remove OM that was originally present in the soil. The reacted soil was washed with deionized water until the supernatant was clear. Oxides-removed WWS was prepared following a modified method of Mehra and Jackson (1960), which was described in Zhuang and Jin (2003).

Viruses and Viral Assay
Two bacteriophages, MS-2 and {phi}X174, were used in this study as models for human enteric viruses. Bacteriophage MS-2 is a male-specific, unenveloped, single-stranded RNA phage (van Regenmortel et al., 2000) with a diameter of 24 to 26 nm and a low isoelectric point (pI) of 3.9 (Zerda, 1982, as cited in Gerba, 1984). The MS-2 virus infects and replicates in Escherichia coli (American Type Culture Collection [ATCC] 15597) bacterial strains with sex pili. Bacteriophage {phi}X174 is a somatic, single-stranded DNA phage with a diameter of 25 to 27 nm (Hall et al., 1959) and a pI of 6.6 (Aach, 1963, as cited in Ackermann and DuBow, 1987). It was grown on its host E. coli ATCC 13706. Each virus was plated on trypticase soy agar and detected by plaque formation in bacterial-laden semisolid agar media (Adams, 1959). All assays were performed in duplicate. The plates were incubated at 37°C for 12 and 7 h for MS-2 and {phi}X174, respectively. More detailed assay procedures can be found in Jin et al. (2000).

Virus Transport Experiments
Eight virus breakthrough experiments were performed under saturated flow conditions. Among them, four column experiments were conducted to investigate effects of mineral-associated OM on virus transport using WWS, OM-coated WWS, GA soil, and OM-removed GA. Three experiments focused on examining virus transport as affected by dissolved OM at various concentrations (1, 5, and 50 mg L-1). The dissolved OM was a natural humic acid (HA) purchased from the International Humic Substances Society (Code 1S102H), which contained 58.1% carbon, 3.7% hydrogen, 34.1% oxygen, 4.1% nitrogen, 0.44% sulfur, 0.24% phosphate, and 0.88% ash. The HA is composed of both hydrophobic (206 nmol mg-1) and hydrophilic (571 nmol mg-1) amino acids. The eighth experiment was conducted to study viral response to the removal of metal oxides from WWS. Conditions of the column experiments are presented in Table 2.


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  		Table 2. The experimental parameters of virus transport.

 
The column system used in the study was the same as that in Jin et al. (2000). The system consisted of a 10-cm-long, 5.1-cm-diameter column and a top and a bottom plate, all made of acrylate, and was sealed with an O-ring on each end (the O-ring had no contact with the interior of the column). A stainless steel screen was placed on the bottom plate for mechanical support. Teflon tubing was used throughout the system except for a portion of tygon tubing needed in the pump. Tests indicated no virus sorption onto or inactivation by column materials and tubing (Jin et al., 2000). When packing the columns, a deaerated phosphate-buffered saline (PBS) solution (0.02 M Na2HPO4, 0.10 M NaCl, and 0.003 M KCl, pH 7.5) was introduced into the column first, followed by slowly pouring the sample (sand or soil) in 1-cm increments while stirred with an autoclaved rod to ensure packing uniformity and to avoid air entrapment in the column. We selected PBS as the buffer in this study because viruses survive longer in phosphate-containing solutions (Zhuang and Jin, 2003) and also because it would allow us to compare results from this study with those from other experiments in which PBS was used.

All experiments were conducted in a large refrigerator at approximately 4°C to minimize possible virus inactivation by high temperatures. Before each experiment, the packed column was flushed with at least 10 pore volumes (PVs) of the autoclaved and deaerated PBS solution to standardize the chemical conditions of the experimental system and to establish a steady state flow status. Then, input solution was introduced into the column as a step input using a peristaltic pump. We prepared the input solutions by dissolving bromide tracer (KBr in 50 mg L-1) and suspending the bacteriophages MS-2 and {phi}X174 into the PBS solution. The inlet concentrations of both bacteriophages were approximately 5 x 108 plaque-forming units (pfu) L-1. Column effluent samples were collected in 15-mL polypropylene centrifuge tubes with a fraction collector. Bromide tracer was analyzed using ion chromatography (Dionex Corporation, Sunnyvale, CA).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Bromide Transport
Bromide breakthrough curves from all experiments are plotted in Fig. 1 . The dispersion coefficients (D) (Table 2) were determined by fitting the standard convection–dispersion equation for a conservative solute to the bromide breakthrough curves (van Genuchten and Alves, 1982). The estimated D values for the GA and OM-removed GA soils were larger than we expected, which was probably caused by the insufficient number of samples analyzed for the sharply rising portion of the breakthrough curves. Nonetheless, the bromide curve reproduced very well, indicating that the column system was stable and the hydrodynamic conditions were similar in all experiments.



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  		Fig. 1. Bromide breakthrough from eight saturated columns. GA, Georgia soil; OM, organic matter; WWS, water-washed sand. The terms WWS + 1HA, WWS + 5HA, and WWS + 50HA refer to virus transports through WWS in phosphate-buffered saline (PBS) solution containing 1, 5, and 50 mg L-1 humic acid, respectively.

 
Effects of Organic Matter Coating on Virus Transport
Organic matter coating represents a scenario where OM was deposited on sand surfaces to form a uniform and complete film. Breakthrough curves of MS-2 and {phi}X174 as affected by the OM coating are presented in Fig. 2 . As illustrated in Fig. 2a, MS-2 concentrations in the effluent were much less reduced in the OM-coated sand than in the uncoated sand. The C/C0 values increased very slowly to only 0.08 after 22 PVs passed through the WWS, whereas it reached unity at 2.6 PVs in the OM-coated WWS. To quantitatively compare the extent of virus transport in each experiment, we calculated a breakthrough percentage (BP), which is defined as the ratio of the total number of virus particles transported through the column to the total number of input virus particles for the same experimental duration (7 PVs). As shown in Table 3, the BP value for MS-2 was significantly higher for the OM-coated WWS column (71%) than for the WWS column (0.8%). The very low transport of MS-2 through the WWS-packed column without OM coincided with the observations by Chu et al. (2000)(2001), where they attributed the strong viral removal to sorption and inactivation of MS-2 by the metals and metal oxides present in the WWS. Direct experimental evidence is provided in Fig. 3a , where transport of MS-2 increased significantly after metal oxides were removed from the sand.



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  		Fig. 2. Breakthrough curves of (a) MS-2 and (b) {phi}X174 from columns packed with water-washed sand (WWS) and organic matter (OM)–coated WWS.

 

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  		Table 3. Breakthrough percentage (BP) of viruses during the transport.

 


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  		Fig. 3. Breakthrough curves of (a) MS-2 and (b) {phi}X174 from columns packed with water-washed sand (WWS) and oxides-removed WWS.

 
In comparison, the transport patterns of {phi}X174 through the two media did not differ from each other as significantly as MS-2 (Fig. 2b). Complete breakthrough was obtained in both experiments, indicating a low retention of {phi}X174 on both WWS and OM-coated WWS surfaces. This is also indicated by the BP values, which were 77% for the OM-coated sand column and 70% for the uncoated sand column (Table 3). A careful comparison of the breakthrough curves suggests that presence of OM slightly reduced the delay of {phi}X174 transport through the sand. The plateau concentration was reached at 1.6 PVs in the presence of OM coating and at 2.9 PVs in the absence of OM. Unlike MS-2, {phi}X174 was not reactive to the metal oxides presented on WWS (Fig. 3b and Table 3). Because breakthrough of {phi}X174 was already quite rapid and complete from the WWS column, it was difficult to evaluate the OM effect in this particular medium.

The above results, especially for MS-2, agree well with those of Powelson et al. (1991) and Pieper et al. (1997). Powelson et al. (1991) observed that natural OM found in sewage sludge decreased the removal of MS-2 in unsaturated loamy sand. Pieper et al. (1997) concluded that higher OM content in a contaminated zone played a dominant role in enhancing PRD1 transport. However, the results from this study did not conform to those of Bales et al. (1993), who found that OM (C18–chlorosilane) artificially coated on silica beads increased attachment of MS-2 to the silica beads by providing hydrophobic sorption sites for viruses. Kinoshita et al. (1993) also reported that higher organic C contents retarded MS-2 transport due to hydrophobic interaction.

The apparently inconsistent results reported in the literature and obtained in this study seem to suggest that different mechanisms are involved in the interactions between viruses and organic materials, depending on their nature and sources. Natural OMs are notoriously heterogeneous because they contain different amounts and types of functional groups and therefore vary in their hydrophilic and hydrophobic properties. Organic matter sorbed on soil particles can provide additional negative charges that repulse viruses or cover positively charged sites, which may decrease the electrostatic interactions between viruses and soil particles. On the other hand, sorbed OM may also provide hydrophobic sorption sites for the more hydrophobic viruses where their sorption is otherwise very low (Bales et al., 1993). Therefore, the relative importance of the electrostatic interaction and the hydrophobic interaction may vary depending on the specific forms and/or properties of the OM on solid surfaces and the surface properties of the viruses.

Based on the above discussion, the transport behavior of MS-2 observed in this study may not necessarily be contradictory to the findings of Bales et al. (1993), since they used a pure hydrophobic organic material (C18–chlorosilane) while the OM used in this study was a peat humic acid containing 15% ash, indicating a relatively high hydrophilicity. The complete MS-2 breakthrough from the OM-containing columns, as shown in Fig. 2a, suggests that electrostatic interactions (repulsion) between MS-2 and OM, rather than hydrophobic interactions (attraction), dominated in the overall effect by OM. As suggested by Penrod et al. (1996) and Redman et al. (1997), the attachment rate of MS-2 might also be determined by steric repulsion (an electrostatic interaction) of hydrophilic loops that protrude from the surface of MS-2. Therefore, in the columns containing mineral-associated OM, blocking of the surface sites favorable for MS-2 sorption and development of an electrostatic barrier by sorbed OM might be another reason for the inhibited virus attachment and consequently increased viral transport. Pieper et al. (1997) and Ryan et al. (1999) obtained similar results with PRD1.

The differences observed between MS-2 and {phi}X174 in their reactions with WWS and OM coating are probably due to the difference in their isoelectric points. At the experimental pH of 7.5, MS-2, which has an isoelectric point (pI) of 3.9, would be more negatively charged than {phi}X174, which has a pI of 6.6. This further supports our conclusion that electrostatic interactions played a dominant role in our experiments.

Effects of Removing Organic Matter from Soil on Virus Transport
In natural environments, organic material may chemically combine with or partially cover inorganic minerals with heterogeneous features. Therefore, removing OM from a soil represents a scenario different from OM coating for studying the effect of mineral-associated OM on virus behavior. Figure 4 shows the breakthrough curves from two experiments conducted using GA soil and OM-removed GA soil. The results indicate that removal of naturally associated OM from the soil particles decreased MS-2 concentrations in the early transport stage and delayed the time it took to reach a plateau C/C0 by approximately 1.7 PVs (Fig. 4a). This implies that removing the mineral-associated OM resulted in exposure of more surface sites favorable for MS-2 sorption. The BP value was 69% for GA soil and 63% for OM-removed GA (Table 3), suggesting that the OM originally present in the GA soil did not react strongly with MS-2 through hydrophobic interactions.



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  		Fig. 4. Breakthrough curves of (a) MS-2 and (b) {phi}X174 from columns packed with Georgia soil (GA) and organic matter (OM)–removed GA soil.

 
Similar breakthrough behavior was observed for {phi}X174 in GA and OM-removed GA soils (Fig. 4b). The BP values in the duration of 7 PVs were 85% for both columns, indicating a low retention of {phi}X174 by the GA soil and a minimal effect of OM.

Effects of Dissolved Humic Acid on Virus Transport
To examine the effect of dissolved HA on virus retention and transport, we conducted three column experiments by adding HA to virus input solutions at three concentrations (1, 5, and 50 mg L-1). The breakthrough curves of MS-2 and {phi}X174 from these experiments are shown in Fig. 5 . The presence of HA significantly promoted the transport of MS-2 in all cases and the effect increased with increasing HA concentrations (Fig. 5a). The BP value for MS-2 was increased from 0.8% at 0 HA concentration to 1.1% at 1 mg L-1 HA, 39% at 5 mg L-1 HA, and 67% at 50 mg L-1 HA (Table 3). It is also interesting to notice that the shape of the breakthrough curve at 1 mg L-1 was significantly different from the curves at the other HA input levels, suggesting that the mechanism involved might be concentration dependent.



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  		Fig. 5. Breakthrough curves of (a) MS-2 and (b) {phi}X174 from water-washed sand (WWS)–packed columns in phosphate-buffered saline (PBS) solution containing different concentrations of dissolved humic acid (HA).

 
Similar to the results observed earlier on the effect of mineral-associated OM, addition of HA to the input solution produced minimal effect on promoting the transport of {phi}X174 through WWS (Fig. 5b). Complete breakthrough of {phi}X174 arrived at almost the same time for all columns with varying HA concentrations. The BP values for {phi}X174 did not differ much from each other and were 70, 94, and 90% at HA concentrations of 0, 5, and 50 mg L-1, respectively. Because strong virus–sand interaction was not observed in the transport of {phi}X174 through the WWS without HA, the effect of dissolved HA could not be effectively evaluated. However, it was clear that the dissolved HA did not hinder the transport of {phi}X174 through WWS.

The concentrations of HA in the effluent samples were also measured. Figure 6a shows the HA breakthrough curves for the different HA input levels. The transport of HA seemed concentration dependent, showing less retardation as concentration increased (Fig. 6a). This behavior is indicative of nonlinear sorption (see figure insert in Fig. 6b), which is commonly described by the Freundlich or Langmuir relationship over a large range of concentrations (Vermeer et al., 1998). Jury and Flühler (1992) interpreted the Freundlich adsorption process as one in which compounds are more strongly retarded at lower concentrations. The nonlinear sorption of the HA (Fig. 6b) suggests a strong HA–surface interaction at the early transport stage and a weak interaction (increased repulsion) in the later stage where relatively constant HA concentrations in the effluent were measured.



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  		Fig. 6. Breakthrough curves of dissolved humic acid (HA) from (a) water-washed sand (WWS)–packed columns and (b) dynamics of amount of HA sorption. The insert was plotted based on the sorption data of HA at approximately 19.5 pore volumes (PVs) in the three column experiments.

 
Competition between HA and viruses for sorption sites was probably the controlling mechanism during the early stage of virus transport. Because both HA and virus particles are negatively charged polyelectrolytes and contain many similar function groups, they may favor the same sorption sites on solid surfaces (Gerba, 1985). Both electrostatic interactions and specific sorption are involved in the binding of OM to mineral particles (Gu et al., 1994; Tipping, 1981; Vermeer et al., 1998). Specific sorption usually results in formation of an inner-sphere complex, which has high binding energy. On the contrary, bacteriophages (MS-2 and {phi}X174) are primarily associated with solid surfaces as an outer-sphere complex, which has weak binding (Zhuang and Jin, 2003). Therefore, HA sorption was more favorable, which resulted in reduced virus retention and increased transport.

Once a critical amount of the dissolved HA was sorbed on the sand, it played the same role as the mineral-associated OM. Therefore, electrostatic repulsion dominated the virus–surface interactions at the later stages of transport. Sorbed HA increased the negative charges on the solid surfaces and provided an electrostatic barrier that minimized the subsequent virus attachment. The jump increase in MS-2 outflow concentrations at approximately 13 PVs in the experiment with 1 mg L-1 HA (shown in Fig. 5a) was probably caused by such an effect.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Results from this study indicate that the effect of OM on virus retention is very complex, depending on both the nature of the OM and the type of viruses involved. Although OM in natural soils all consists of humic substances, they are usually different from each other in form, composition, and properties. Different sources, mineralization conditions, and formation age contribute to the variations found in natural soil OM. In comparing past work with this study, the apparent inconsistency reported about the OM effect on virus behavior in porous media may not be that difficult to understand. The collective results seem to suggest that if the dominant mechanism controlling OM–virus interaction was electrostatic, virus transport would be promoted. Likewise, if the dominant mechanism was hydrophobic, virus transport would be retarded. We believe that the extensive heterogeneity of natural OM is responsible for the various effects of OM on virus fate and transport. To fully understand the role that OM plays in affecting virus behavior in the subsurface environment, future studies should focus on the characterization of both virus and OM and the identification of the controlling mechanisms in any particular system.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 


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