Elsevier

Water Research

Volume 44, Issue 4, February 2010, Pages 1182-1192
Water Research

Transport of selected bacterial pathogens in agricultural soil and quartz sand

https://doi.org/10.1016/j.watres.2008.11.038Get rights and content

Abstract

The protection of groundwater supplies from microbial contamination necessitates a solid understanding of the key factors controlling the migration and retention of pathogenic organisms through the subsurface environment. The transport behavior of five waterborne pathogens was examined using laboratory-scale columns packed with clean quartz at two solution ionic strengths (10 mM and 30 mM). Escherichia coli O157:H7 and Yersinia enterocolitica were selected as representative Gram-negative pathogens, Enterococcus faecalis was selected as a representative Gram-positive organism, and two cyanobacteria (Microcystis aeruginosa and Anabaena flos-aquae) were also studied. The five organisms exhibit differing attachment efficiencies to the quartz sand. The surface (zeta) potential of the microorganisms was characterized over a broad range of pH values (2–8) at two ionic strengths (10 mM and 30 mM). These measurements are used to evaluate the observed attachment behavior within the context of the DLVO theory of colloidal stability. To better understand the possible link between bacterial transport in model quartz sand systems and natural soil matrices, additional experiments were conducted with two of the selected organisms using columns packed with loamy sand obtained from an agricultural field. This investigation highlights the need for further characterization of waterborne pathogen surface properties and transport behavior over a broader range of environmentally relevant conditions.

Introduction

Walkerton, Ontario and Milwaukee, Wisconsin remain recent reminders of the potential devastation caused by microbial contamination of public drinking water supplies (Smith and Perdek, 2004). According to the World Health Organization, waterborne disease remains the leading cause of death worldwide, with millions of deaths annually attributed to lack of access to clean sources of potable water. Increasing agricultural activity and expanding urbanization contribute to the deterioration of surface water and groundwater quality (Smith and Perdek, 2004).

Worldwide, at least 1.5 billion people depend on groundwater as their sole source of drinking water (World Resources Institute, 2000). Hence, strategies for the prevention and remediation of groundwater contamination are of key importance. The development of groundwater protection policies necessitates knowledge of the fundamental processes controlling the transport and fate of biological and non-biological contaminants in different natural subsurface environments. A good understanding of these mechanisms is also of importance for the correct implementation of riverbank filtration – a process used for the treatment of surface waters aimed at potable use (Tufenkji et al., 2002). A growing research effort has thus been aimed at developing an improved understanding of the migration and retention of microbial pathogens in model or natural granular environments (Castro and Tufenkji, 2007, Dai and Hozalski, 2002, Harter et al., 2000, Hijnen et al., 2005, Tufenkji, 2007).

Many studies examining the interaction of microorganisms with soil, sand, gravel or other model granular materials have been conducted using laboratory-scale columns under well-controlled environmental conditions (Bolster et al., 2006, Brown and Jaffe, 2001, Brown et al., 2002, Camesano and Logan, 1998, Castro and Tufenkji, 2007, Dai and Hozalski, 2002, Harter et al., 2000, Harvey and Harms, 2001, Hijnen et al., 2005, Kim et al., 2008, Li and Logan, 1999). Laboratory experiments have been conducted to examine the influence of pore water solution chemistry (e.g., salt concentration, pH, ion valence), velocity, matrix moisture content, temperature, and geochemistry (i.e., grain surface properties) on microbial transport and retention in granular porous matrices (Harvey and Harms, 2001). Quartz sand, either clean or coated, and glass beads have all been implemented as model granular materials in such studies. Some researchers have also investigated the transport of microorganisms through columns packed with excavated soils or undisturbed soil cores, yielding additional information regarding the influence of soil chemistry and matrix structure on microbial transport and retention (Banks et al., 2003, Guimaraes et al., 1997, Hekman et al., 1995, Huysman and Verstraete, 1993, Li and Logan, 1999). However, few experimental investigations have aimed to compare the transport behavior of microorganisms in model granular materials (e.g., clean quartz sand or glass beads) with natural sands or soils (Brush et al., 1999, Li and Logan, 1999). Although a large number of studies of microbial transport have been published over the past two decades, our ability to predict the migration potential of bacteria, viruses or protozoa in natural subsurface environments remains limited.

One drawback associated with the current body of literature is the limited number of studies examining the transport and fate of waterborne pathogenic microbes in model or natural granular systems (Brush et al., 1999, Castro and Tufenkji, 2007, Harter et al., 2000, Hijnen et al., 2005). A recent study demonstrated significant transport differences between Shiga-toxin producing Escherichia coli (E. coli) O157:H7 and nontoxigenic surrogates of the same species (Castro and Tufenkji, 2007). Such reports underscore the need for more investigations evaluating the behavior of pathogenic strains of waterborne microbial contaminants. Another limitation of the current literature is the lack of studies examining the transport behavior of Gram-positive organisms. A great deal of research has been conducted to evaluate the transport and fate of Gram-negative bacteria, including E. coli, Pseudomonas aeruginosa, and Burkholderia, however, much fewer studies have been conducted with environmentally relevant enteric Gram-positive pathogens such as Enterococcus faecalis (E. faecalis) (Harvey and Harms, 2001).

Recent experimental investigations of microbial transport in granular porous systems have sometimes been accompanied by characterization of the physicochemical properties of the microbes of interest (Bolster et al., 2006, Foppen and Schijven, 2005, Redman et al., 1997, Walker et al., 2004). Measurements of microbe size, shape, surface charge (i.e., zeta potential) and cell surface hydrophobicity have all demonstrated varying levels of relevance in interpretation of microbial transport data (Abu-Lail and Camesano, 2003, Bolster et al., 2006, Castro and Tufenkji, 2007, Dong et al., 2002, Foppen and Schijven, 2005, Redman et al., 1997, Tong et al., 2005, Tufenkji, 2006, Walker et al., 2004). Such measurements are also of interest in understanding the aggregation potential of organisms in aqueous environments (Eboigbodin et al., 2005, Marshall, 1984). Although data relating the surface and physical properties of microbes is of interest in environmental fate studies, such information for waterborne microbial pathogens remains limited (Castro and Tufenkji, 2007, Dai and Hozalski, 2003, Gallardo-Moreno et al., 2003, Hsu and Huang, 2002, Lytle et al., 2002, Lytle et al., 1999, Rivas et al., 2005).

In this study, we investigate the transport potential and physicochemical properties of a broad range of bacterial pathogens. E. coli O157:H7 and Yersinia enterocolitica (Y. enterocolitica) were selected as representative Gram-negative pathogens whereas E. faecalis was selected as a representative Gram-positive fecal indicator. Because of the growing importance of cyanobacteria as surface water contaminants and their relevance as potential contaminants during surface water infiltration (e.g., Groundwater-Under-Direct-Influence (GWUDI) scenarios), the organisms Microcystis aeruginosa (M. aeruginosa) and Anabaena flos-aquae (A. flos-aquae) were also examined. Well-controlled laboratory experiments were conducted to evaluate the migration potential of the five organisms in columns packed with clean quartz sand. Two of the organisms (E. coli and E. faecalis) were also studied in columns packed with agricultural soil for comparison with the model granular material. The surface (i.e., zeta) potential of the organisms was characterized over a broad range of solution conditions and the cell size was measured for the condition of the transport experiments. Finally, the experimental results are analyzed within the context of the classic Derjaguin–Landau–Verwey–Overbeek (DLVO) theory of colloidal stability (Derjaguin and Landau, 1941, Verwey and Overbeek, 1948).

Section snippets

Bacteria selection and preparation

The pathogenic or toxigenic organisms used in this study include the two Gram-negative bacteria, E. coli O157:H7 ATCC 700927 and Yersinia enterocolitica (Y. enterocolitica) ATCC 23715, the Gram-positive strain E. faecalis ATCC 29212, and the two cyanobacteria, M. aeruginosa UTCC 299 and Anabaena flos-aquae UTCC 607 (obtained from the University of Toronto Culture Collection of Algae and Cyanobacteria). Pure cultures of E. coli and E. faecalis were maintained at −80 °C in Luria-Bertani (LB)

Electrokinetic properties of bacteria

The ζ-potential of different Gram-negative and Gram-positive bacteria was determined over a broad range of pH values (2–8) and at two different solution ionic strengths (IS). Fig. 1a compares the ζ-potentials of the five selected microbes when suspended in 10 mM KCl. All of the microbes examined are negatively charged over most of the pH range and exhibit an increase in the magnitude of charge with increasing pH. This behavior can be explained by the increased deprotonation of cell surface

Conclusions

The filtration behavior of five selected bacterial pathogens was examined in laboratory-scale columns packed with clean quartz sand at two IS and a pH near 6. Comparison of the results from this study with those previously reported indicates an interesting link between the experimental α value and the dimensionless parameter, NDLVO. The noted importance of electrostatic interactions in colloid stability (i.e., colloid attachment to surfaces and colloid aggregation) emphasizes the value of

Acknowledgments

This research was supported by the Fonds québécois de la recherche sur la nature et les technologies (FQRNT Team Grant), the Canadian Water Network (CWN) and the Canada Foundation for Innovation (CFI). The authors acknowledge G. Faubert (McGill) and C. Madramootoo (McGill) for helpful discussions and access to the field site, S. Gruenheid (McGill) for providing ATCC 700927, M. Assanta (AAFC) for providing ATCC 23715, and R. Piscolla for completing the soil sizing analysis.

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