EFFECTS OF SOIL MATRIC SUCTION ON RETENTION AND PERCOLATION OF BACILLUS SUBTILIS IN INTACT SOIL CORES GUANGMING JIANG1,∗ , MIKE J. NOONAN2 and TAREKA J. RATECLIFFE2 1
College of Environmental & Resource Sciences, Southwest University of Science and Technology, Mianyang 621002, P. R. China, and Now at School of Engineering and Information Technology, Deakin University, Pigdons Rd, Geelong, Victoria 3217, Australia; 2 Agriculture and Life Sciences Division, P. O. Box 84, Lincoln University, Canterbury, New Zealand (∗ author for correspondence, e-mail:
[email protected],
[email protected])
(Received 20 October 2005; accepted 26 March 2006)
Abstract. Bacillus subtilis endospores (resistant to rifampicin) irrigated on the surface of intact soil cores (20 cm diameter × 8 cm length) which were equilibrated under selected suctions, i.e. 0, 0.5, 2, 5, 10 kPa, were then percolated by saturated water flow. The bacterial retention and percolation percentage were significantly correlated with the suctions. The higher retention with higher suction was explained by micropore storage, attachment to static air-water interface (AWI), and irreversible adsorption to soil particles. The bacterial percolation was mainly controlled by initial replacement of pore water storage, and following reversible detachment process. Another sensitivity experiment with four replicates using lincomycin-resistant B. subtilis at 0 and 0.5 kPa suctions revealed that small increase (0 to 0.5 kPa) in soil matric suction incurred a substantial higher level of bacterial retention. Based on our experimental results, soil matric suction was proposed as a comprehensive parameter to monitor bacterial transport and fate for animal waste disposal (irrigation) and subsurface bioremediation. Keywords: Bacillus subtilis, soil matric suction, micropore water storage, soil water replacement, air-water interface, reversible adsorption
1. Introduction Bacterial transport and retention in soils have been given attention because of their importance in groundwater contamination, subsurface bioremediation, and facilitated transport of pollutants (Abu-Ashour et al., 1994a; Kim and Corapcioglu, 2002; Pierzynski, 2000). Land treatment of wastewater, and land disposal of sewage sludge have produced microbial transport through vadose zone and subsequent contamination of aquifers (Unc and Goss, 2003). In agriculture areas, animal wastes containing faecal bacteria are produced all year and storage before application to land can produce its own problems with heavy precipitation (Unc and Goss, 2004). The quantitative characterization of bacterial transport and retention in heterogeneous soils is essential for many environmental and agronomic practices. Factors controlling the bacterial transport in soils include properties of soil, bacteria and soil water. Important soil characteristics include porosity and pore size distribution, clay content, organic content, metal oxides on particulates, and Water, Air, and Soil Pollution (2006) 177: 211–226 DOI: 10.1007/s11270-006-9150-x
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structure (Abu-Ashour et al., 1994b; Fontes et al., 1991; Mills et al., 1994; van Elsas et al., 1991; Wiencek et al., 1991). The solution ionic strength, pH, and saturation were reported to influence the fate and transport of bacteria (Li and Logan, 1999; Wan et al., 1994; Yee et al., 2000). Cell properties such as size, surface hydrophobicity, surface charges, motility, encapsulation, and flagellation are also important determinants of bacterial transport in soils (Gannon et al., 1991; Lindqvist et al., 1994; Weiss et al., 1995). Soil matric suction (equal to the negative value of soil water potential) reflects interactions of soil water content, flow velocity, and pore space properties. For a specified soil, higher soil suction indicates that the soil has lower water content, i.e. more unsaturated. The relationship between soil suction and water content is named soil moisture characteristics (Hillel, 1998). Many empirical pedo-transfer functions (PTFs) were reported to describe the estimation of water content from soil suctions, e.g. the well-known van Genuchten function (van Genuchten, 1980). Soils under suction (unsaturated) have lower hydraulic conductivity, which means flow velocity is lower compared with saturated soils at the same hydraulic gradient. In brief, effects of soil water suctions comprise influences from water content, flow velocity and pore diameter. Effects of water content and flow velocity were reported in several literature (Camesano and Logan, 1998; Hendry et al., 1999; Parke et al., 1986; Powelson and Mills, 2001). Though the influences of pore sizes were frequently discussed by previous research (e.g. pore size exclusion, macropore flow), no similar research focused on effects of soil water suctions (Beven and Germann, 1982; McGechan, 2002; Sirivithayapakorn and Keller, 2003). The objectives of this study were to determine, when bacterial suspension was applied onto soils under suction, whether and to what degree will the soil matric suction affect the number of bacteria recovered in the drainage water. Tension tables were employed to control the suctions of small lysimeters with undisturbed soil cores. Weights of soil cores, volume and bacterial concentration in leachate were continuously monitored to demonstrate the relationship between suction and bacterial retention/percolation.
2. Materials and Methods 2.1. PREPARATION
OF SOIL CORES
Experiments were carried out using Templeton silt loam soil (Smith et al., 1997). Intact soil cores were taken using a modification of the methods described by Cameron et al. (1992). A 30 mm (high) ×5 mm (wall thickness) cutting ring made from PVC pipe with a sharpened edge was fitted and glued at the bottom of a 200 mm diameter × 300 mm long PVC pipe that acted as a casing. The cutting ring produced a 5 mm gap between the soil core and the casing. Soil cores of slightly larger diameter than the casings were excavated 30 mm at a time. The casings were
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carefully lowered over the excavated soil core, inserting the core into the casing and pushing excess soil aside by the cutting ring. The grass on the surface was trimmed to a height of approximately 5 mm. The soil core was taken out of the casing and inverted onto a 10 mm thick plate of the same diameter and 2 × 40 mm length plastic ring put over the soil and the plate. Three rubber ‘O’ rings were placed near the original surface of the soil to contain the molten wax (see Figure 1). Liquified Vaseline (Shell Co., Wellington, New Zealand) was poured in to fill the gap between the side of the soil core and the two 40 mm long plastic casing. The base of the soil core was cut flush with the plastic casing. To prevent the wax from being smeared onto the soil surface, it was cut from the centre of the soil core. The soil core and plastic ring were inverted and molten wax was applied to fill the annular gap up to the soil surface. 2.2. BACTERIAL
SAMPLING AND ASSAY
B. subtilis endospores mainly inhabit in natural environments such as soil and water (Slepecky and Hemphill, 1992). They are persistent and so biological factors such as regrowth and die-off would be omitted. B. subtilis can be distinguished from other soil bacteria on tryptone glucose agar because of its bright orange colonies. The two selected antibiotic (rifampicin- and lincomycin-) resistant strains were prepared according to Houston et al. (1989). The strain resistant to rifampicin was used for experiments with suctions ranging from 0 to 10 kPa; while lincomycinresistant spores (dormant cells) were used for comparison of bacterial percolation between 0 kPa and 0.5 kPa suction. B. subtilis endospores water samples were enumerated by plate counting method. Before inoculating to agar plates, 150 mL subsamples were taken from the bulk leachate after vigorous shaking. The 150 mL samples were heat treated for 30 min in an 80◦ C water bath (20 min to heat up to 80 ◦ C and 10 min at 80 ◦ C to kill vegetative cells). The culturing medium used was rifampicin or lincomycin supplemented tryptone-glucose-agar (TGA) medium (1% tryptone, 0.5% glucose, 1.5% agar, 5 μg/mL rifampicin or 0.5 mg/mL lincomycin). Colony forming units were counted after incubation of 100 μL sample in TGA plates at 30 ◦ C overnight. 2.3. TENSION
TABLE AND PERCOLATING EXPERIMENTAL SETUP
First, used lining media (coarse sands and silica flour) in tension tables were emptied and cleaned. The siphon was then established to about 20 mm above the bottom of the tray. Coarse sands were spreaded evenly in the tray to a depth of 10 mm. About 3 L slurry of silica flour was poured carefully and slowly onto the tray in case of burrowing holes in the sand. Then, 0.5 kPa suction was applied to check the functionality of the tension tables. Prepared soil cores were placed on polyester gauze, and shifted to tension tables. Siphon devices of the tension table helped maintain constant suctions in soil cores.
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Figure 1. Schematics of soil core preparation. The first sealing tube holds the molten Vaseline. The second one holds casing up and provides 7∼10 mm extra soil when inverted the core to fill in the gap from bottom. The third sealing tube helps prevent loss of Vaseline.
The soil cores were allowed to equilibrate with specified suctions for a specified period (up to seven days). When equilibrium reached, the bacterial suspension was sprayed on the soil surface by hand sprayer. The subsequent saturated water percolation was applied to soil cores using Mariotte setup (see Figure 2). 2.4. BACTERIAL
PERCOLATION EXPERIMENTS
Variables for the experiments are listed in Table I. For the first group of experiment (experiment No. 1 to 10), pairs of soil cores was first equilibrated to 0, 0.5, 2, and 5 kPa suctions. In the second stage, cores were brought to equilibrium in thirteen
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TABLE I Experimental variables Expt. no.
Bacteria†
Cell concentration (cfu/mL)
Total number
Suctions (kPa)‡
1∼8 9∼10 11∼18 19∼20
RIF – LIN –
5.37 × 106 ∼1.22 × 107 0 7.42 × 106 ∼1.19 × 107 0
5.706 × 108 0 5.912 × 108 0
0.5, 2, 5, 10 0 0, 0.5 0
†
RIF and LIN are B. subtilis resistant to rifampicin and lincomycin, respectively. Two replicates for each suction (experiments 1∼8), and four replicates for each suction (experiments 11∼18).
‡
days on tension tables with suctions of 0.5, 2, 5, and 10 kPa. The weight changes of cores were recorded and used as references for volume of bacterial suspension to be applied. Tension tables were covered with plastic sheet to prevent water evaporation. Rifampicin resistant B. subtilis endospore suspensions (20.6 mL, 2.77 × 107 cfu/mL) were diluted to the volume of water loss (46.6 ∼ 106.2 mL, 5.37 × 106 ∼1.22 × 107 cfu/mL) during equilibration from first stage to the second stage. The prepared suspension was sprayed onto the soil surface. Applied bacterial suspension will lower the suctions to that at the first equilibrating stage. However, soil cores were still unsaturated or nearly saturated. When cores equilibrated to new suctions, they were placed on a stainless steel wire mesh held part way down a funnel to collect drainage water. Irrigation of bacteria-free water commenced 18 h after bacterial application. One litre water was applied as flood irrigation and an approximately 10 mm water head was maintained by mariotte.
Figure 2. Schematics of tension table and bacterial percolation setup.
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Based on the results from the first group of experiments, matric suction as low as 0.5 kPa was effective in changing the soil retention ability for inoculated bacteria. This was also demonstrated in a bigger soil lysimeter (Jiang et al., 2005). Thus, only 0 kPa (saturated soil cores) and 0.5 kPa were selected in further experiments (experiment No. 11 ∼ 20). Five soil cores were reduced to 0.5 kPa suction and other five cores were saturated by sitting the cores in a water bath. A suspension (4 ml, 1.478 × 108 cfu/mL) of lincomycin resistant B. subtilis was diluted to the appropriate volume (49.5 ∼ 79.7 ml, 7.418 × 106 ∼1.194 × 107 cfu/mL) for four of 0.5 kPa cores. Bacterial suspension of the average volume (59.6 ml) was added to the four of the saturated columns. One suction core and one saturated core acted as controls with water replacing the bacterial suspension. Drainage water was collected as this appeared immediately on application to the saturated column.
3. Results 3.1. DRAINAGE Drainage during three sequential bacterial percolations with five selected suctions (Expt. 1 ∼ 10) is shown in Figure 3. Drainage during the first leaching event has a bigger variation than the following leaching events, because soil cores with higher suction needed more water to bring them to saturated condition. The average cumulate drainage for different suctions was 112.39 mm (Standard deviation = 5.09), varying from 106.15 ± 1.64 (10 kPa) to 119 ± 0.19 mm H2 O (0 kPa). The drainage for each leaching events and suctions had no significant difference, thus it would not produce deflective influence on the number of percolated bacteria. All soil cores had the same dimensions and soils, thus benefited the similar water drainage characteristics. This helped to compare the difference of bacterial retention and percolation caused by suctions, rather than different drainage volume. 3.2. CELLS
RECOVERED PERCENTAGE
After approximately 100 mm of drainage, the percentage of applied bacteria that were recovered in the drainage water was less than 5% for all cores (Expt. 1 ∼ 10). The silt loam soils under suctions showed very high bacterial retention ability regardless of magnitude of suctions. And, the cores with the highest suctions showed the lowest recovery percentages, 1.5 and 1.4 for 10 kPa, 1.5 and 2.2 for 5 kPa, 2.2 and 3.3 for 2 kPa, and 2.0 and 4.3 for 0.5 kPa suction. The control cores (0 kPa) without bacterial inoculation had no recovery of bacteria. This indicated that no indigenous B. subtilis endospores in the soil or they are in very low numbers out of the detection limit. The average recovered percentage of applied cells in leachate decreased with increased suctions, from 3.19 ± 1.56 (0.5 kPa) to 1.46 ± 0.07 (10 kPa).
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Figure 3. Drainage under the selected suctions (10, 5, 2, 0.5, and 0 kPa) for three sequential leaching events. Error bars indicates the standard deviation of two replicates for each suction and leaching event.
It is also noticeable that recovery percentage of higher suctions has lower variation. The soil cores might differ from each other in soil properties (e.g. porosity) although prepared according to the same methods and other factors were the same for replicates. The ANOVA results showed that recovery percentage had no significant difference among selected suctions (P = 0.34). However, the bacterial percolation showed very apparent tendency with suctions, the correlation coefficient (r = 0.6754) between the percentage of bacterial recovery and the increase of soil suction was significant (P = 0.03). Lack of statistical significance for cell recovery between suctions was due to the soil heterogeneity and extremely great variance under lower suctions.
3.3. R EVERSIBLE
BACTERIAL DETACHMENT
The bacterial recovery percentage with drainage and results of linear regression were shown in Figure 5 and Table II. A part of the applied bacteria was postulated being attached to soil particles and static air-water interface (AWI), while
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Figure 4. Recovered percentage of B. subtilis endospores in leachate for five suctions. Error bars indicate standard deviation of two replicates with the same suction.
some bacteria were still suspended in soil pore water. The bacterial attachment was highly irreversible, indicating by very small linear slopes in Figure 5. And thus, after three leaching events, over 96% of applied bacteria were retained in soil cores. The control cores had a slope of zero, which demonstrated background levels of B. subtilis was negligible or not percolated by the leaching. Linear regression results showed that the bacterial percolation rate is reversibly related to suctions. The slopes of regression lines decreased with increasing suctions, from 0.0264 at 0.5 kPa to 0.0097 at 10 kPa. Therefore, bacteria applied to soil cores under higher suction were more difficult to be percolated by leaching water. The linear relationship between percolated bacteria and drainage conformed to data reported by other researchers (Bales et al., 1991; Yee et al., 2000). Though heterogeneity of soil properties caused the poor correlation at 0.5 kPa (indicating by high standard deviations and low correlation coefficient), it is obvious that the detachment rate decreases with increasing suctions. All regression results did not pass through the origin, which possibly because the initial bacterial percolation was not caused by detachment of captured cell. At the beginning of leaching, a part of suspended bacteria in soil water, especially in macropores, were flushed through the soil cores before detachment happened. For suctions 2, 5, and 10 kPa,
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TABLE II Coefficients for linear regression of bacterial percolationa Suctions (kPa)
b0
b1
r2
0 0.5 2 5 10
0 −0.0249 ± 1.3048 0.9811 ± 0.5611 0.6026 ± 0.1404 0.4776 ± 0.0016
0 0.0264 ± 0.0226 0.0162 ± 0.0022 0.0121 ± 0.003 0.0097 ± 0.0004
NA 0.9007 0.9883 0.9701 0.9574
a
The parameters were estimated in SigmaPlot 8.0 (SPSS Inc.) by least squares method based on y = b0 + b1 x. Where, y is cells recovered percentage (No /Ni %) in leachate and x is drainage (mm). r 2 is correlation coefficient. NA indicates not available.
Figure 5. Bacterial recovery percentage in leachate vs. drainage and linear regression results for different suctions.
the initial bacterial percolation, as indicated by b0 values in Table II, decreased with higher suctions. This indicated that soil pores under higher suction held the applied bacterial suspension more tightly. The exceptional result at 0.5 kPa was ascribed to soil core heterogeneity between the replicates.
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Figure 6. Bacterial percolation percent of unsaturated (with 0.5 kPa suction) and saturated soil cores. Error bars are standard deviation of four replicates for the two suctions.
3.4. UNSATURATED (0.5
KPA SUCTION ) VS . SATURATED SOIL CORES
The lack of statistically significance for selected suctions in the first group of experiments was attributed to the high soil heterogeneity. One possible solution for this problem was increasing the number of replicates. In the second group of experiments, four replicates rather than two were used. When 0.5 kPa suction was compared with the saturated cores (0 kPa), the saturated cores showed recovered percentages between 1.9 and 17.8 while the 0.5 kPa suction ranged between 3.8 and 12.4. In this experiment the bacterial concentration of the first leaching event (c. 33 mm H2 O) was not as different as subsequent leaching as it was in many other experiments. This was probably due to that most of percolated bacteria during the first leaching event were from those captured by mobile air-water interface or suspended in soil water. Controls again showed no bacteria in leachate. The average values for 0.5 kPa and saturated cores were 7.01 ± 3.88 and 11.11 ± 6.69, respectively. However, t-test of the recovered percentage for two suctions did not show significant difference (P = 0.3391). The great variances of four replicates between the two suctions compromised the difference (see Figure 6). Soil heterogeneity of pore sizes and pore connectivity were supposed to be responsible for the variation of bacterial percolation. The poor conformity of the
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results to the first group of experiments suggested that small intact cores were not appropriate for good reproducibility, although provided satisfactory comparable results.
4. Discussion Before doing field tests of bacterial transport, the behavior of these organisms in well-controlled experimental conditions must be explored first. The use of small column with intact soil cores was representative of natural soil properties, and easy to manipulate and reproduce. Nevertheless, edge flow effects induced by column wall are more likely to happen in smaller core systems. Previous research showed that the specifically treated soil column as stated in the methods was invulnerable to this problem. Therefore, small intact soil cores in this paper were feasible in studying bacterial retention and percolation with various suctions. The soil extracted in the experiments was topsoil (c. 30 cm from soil surface) and did not represent the structural, physical and chemical properties of subsoil or gravel aquifer, which were also important for bacterial transport. The lack of reproducibility of bacterial retention and percolation in our experiments indicated that small soil cores also inherited the heterogeneous characteristics of soils. One possible solution is to employ as many replicates as possible for quantitative studies. The bacterial movement through soils was mainly facilitated by soil water flow, especially macropore flow induced by water potential gradient. Bacterial transport was called a passive transport because water serves as the carrier for bacterial cells (McGechan and Lewis, 2002). Former research showed that bacterial transport was enhanced by higher water content (Jewett et al., 1999; Powelson and Mills, 2001). A suction of 0.5 kPa was reported to heavily reduce bacterial recovery in leaching water through an intact soil column (0.5 m diameter by 0.7 m depth) with continuous water flow (Jiang et al., 2005). Treatment of soil cores with different suctions actually controlled the water content, which was inversely related to suction. Besides, the retention of inoculated bacteria to soils was by means of adsorption. This mechanism could be described by DLVO theory and modeled qualitatively by colloid filtration theory (Harvey and Garabedian, 1991; Hermansson, 1999). Bacterial attachment was a complicated process, which resulted from the net force of van deer Waals forces, double electrostatic layer and steric forces (McDowell-Boyer et al., 1986). However, this attachment process was reported to get equilibrated very promptly (e.g. in 20 minutes, see Huysman and Verstraete, 1993). In this experiment, the soil cores inoculated with bacterial suspension were allowed to equilibrate for 18 h. Thus, it was reasonable to postulate that bacterial attachment was equilibrated before the water leaching events. Soil, as a porous medium, contains a large number of interconnected pores with different shapes and sizes, in which water will be emptied by suction under unsaturated conditions. Unsaturated soil will have its bigger pores emptied of water
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first. The relationship between soil suctions and pore diameter can be described by capillary rise equation (Hillel, 1998), which is adapted to calculate the largest waterfilled pore diameter. The largest water-filled pore diameter for the experimental suctions of 0.5, 2, 5, 10 kPa was 600, 150, 60, 30 μm, respectively. The pores with diameter greater than these critical values will be emptied by suction, while smaller pores will be water-filled. The bacteria applied to soil cores with various suctions thus entered different sized pores. Under higher suctions, bacteria were trapped in smaller pores. The pore water flow rate (water flux) is directly proportional to the fourth power of pore size, which can be described by Poiseuille’s law (Hillel, 1998). Therefore, bacteria captured in smaller pores are much more difficult to be percolated by convection effects of subsequent saturated leaching water, which was mainly flow through bigger pores. Because of the difficulty in replacing water in small pores, the storage of initial applied bacterial suspension in pores with extremely slow flow velocity was a possible explanation of the high bacterial retention observed in soil cores with high suctions. Smaller soil pores also provides more opportunities for sorption to occur between cells and soil particulates (McGechan and Lewis, 2002). The bacterial attachment to particles partly determines their retention because of the low flow rate in small pores. The detachment process was facilitated by hydrodynamic shearing force. Since smaller pores have mild hydrodynamic dispersion, flow velocity was not effective for detachment of most bacteria in those pores. In brief, high bacterial attachment and low detachment rate under higher suctions also contributes to the high bacterial retention in soil cores. Unsaturated soil can be considered as a tri-phase porous medium, of which the static air-water interface was reported to be especially effective for bacterial attachment (Schaefer et al., 2000; Schafer et al., 1998; Thompson et al., 1998). When unsaturated soil became saturated and produced leachate, a part of the static air-water interface would be mobilized and produced high number of bacteria in effluent (Wan et al., 1994). On the other hand, the static air-water interface might also be dispersed gradually without significant mobilization during the leaching events. Under higher suctions, the air-water interface was distributed in smaller pores, where water velocity were low and static AWI was more difficult to be mobilized. Therefore, the bacterial attachment to static air-water interface and subsequent dispersion mechanism partly explained the higher retention of bacteria in soil cores. For bacteria recovered in leachate, although the numbers were directly proportional to the volume of drainage, as shown in Figure 5, the bacterial percolation was not induced by a single mechanism. As stated above, the initial applied bacteria were partly attached to soil particles and partly stored in soil water at buoyant state. Most bacterial suspension was stored in small pores under suctions, which would not produce prominent water flow. Only a small percent of the stored bacteria would be replaced by bacteria-free water when soil cores started leaching.
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This replacement mechanism was denoted by the intercept and b0 value of regression lines in Figure 5 and Table II. According to the suctions and their corresponding pore sizes, higher suctions would have lower degree of replacement, i.e. small b0 . This explanation was consistent for suctions of 2, 5, 10 kPa, but not 0.5 kPa, which had a relative high variance of recovery percentage caused by soil heterogeneity. Bacterial attachment was reported to be composed of irreversible and reversible sorption to particles (Fontes et al., 1991; Harvey and Garabedian, 1991). Also, the attachment/detachment was sometimes modeled as a first-order kinetic process, by which the number of bacteria attached or detached was proportional to the concentration in soil water or on soil particles. Compared to the large number of bacteria applied, only a small percent was percolated. If the equilibrated attachment was also taken into account, it was arguable to regard the bacterial concentration on soil particles as constant for the detachment process. The linear relationship of percolated bacterial number with drainage was agreeable to the above interpretation. Also, the detachment was favorable under high water velocity by means of stronger shearing force, which was demonstrated by greater slopes and b1 values of regression lines in Figure 5 and Table II. To summarize the above discussion, it was evident that bacterial retention was much higher than bacterial percolation under all experimental conditions. Micropore storage, static AWI attachment, and irreversible adsorption to particles overwhelmed replacement of soil water storage and reversible detachment. For intermittent application of bacteria-contained waste (i.e. dairy shed effluent, biologicallytreated wastewater) to unsaturated soils followed by water irrigation or precipitation which occurred in field conditions frequently, the above-mentioned mechanisms were in control of bacterial retention and percolation. The findings help to prevent bacterial contamination of shallow groundwater by controlling soil matric suction and application rate. Applying waste to soil with high suctions without making soil saturated would therefore increase retained proportion of applied microbes even suffered by subsequent saturated leaching. Based on the relationship between soil matric suction and water content, pore size, and pore water velocity, we proposed soil matric suction as an important parameter to be monitored for land application of animal wastes, bioremediation process, and manipulation of soil for controlling inoculated bio-agents. Further experimental study and mathematical modeling on bacterial transport and retention through soil columns under suctions with continuous flow will provide more insights into the effects of soil matric suction.
5. Acknowledgments We thank the New Zealand Foundation of Research, Science and Technology (FoRST) for funding the research programme. We also thank Andrea Coup, Neil
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Smith for their expert technical assistance, and Richard Sedcole for statistical advice. Appreciation is given to B. N. Dancer at University of Wales, Institute of Science and Technology for supplying bacteria used in the research. Guangming Jiang is grateful for his postgraduate scholarship funded from NZAID (New Zealand Agency for International Development).
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