Microbial Availability of Different Forms of Phenanthrene in Soils

Feb 13, 2009 - Ter Laak , T. L.; Barendregt , A.; Hermens , J. L. M. Freely dissolved pore water concentrations and sorption coefficients of PAHs in s...
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Environ. Sci. Technol. 2009, 43, 1852–1857

Microbial Availability of Different Forms of Phenanthrene in Soils Y U Y A N G , †,‡ W E S L E Y H U N T E R , ‡ S H U T A O , † A N D J A Y G A N * ,‡ Laboratory for Earth Surface Processes, College of Urban and Environmental Sciences, Peking University, Beijing, China, and Department of Environmental Sciences, University of California, Riverside, California

Received October 21, 2008. Revised manuscript received January 13, 2009. Accepted January 15, 2009.

Microbial degradation is the most important removal process for hydrophobic organic compounds (HOCs) in soil or sediment, and chemical availability is often a governing factor. However, the availability of HOCs in the sorbed forms is still a topic of debate. In this study, we applied rigorous kinetics analysis to the relationship between the freely dissolved concentration (Cfree) of phenanthrene (PHE) measured by polydimethylsiloxane (PDMS) fibers and its degradation by a PAH degrading bacterium PYR-1 under a range of soil conditions. In solutions of soils with varying organic carbon (OC) contents, Cfree of PHE decreased from 28.63 ( 2.15 to 0.79 ( 0.04 µg L-1 when the soil OC content changed from 0.23 to 7.1%. Correlation analysis between Cfree and PHE mineralization rates revealed that the bacterium quickly exhausted the PHE pool available for equilibrium distribution, including Cfree and the reversibly sorbed fraction, after which the sequestered pool was utilized. In addition, unlike changes in Cfree, degradation rates of total PHE only varied by a factor of 1.6-2.1 over the same soil OC range. Regression analysis using a multivariate relationship showed that soil OC content and porosity properties such as soil surface area had a compounded effect on the microbial availability of PHE in these soils. The kinetics analysis using Cfree, as proposed in this study, may be applied to other HOCs to gain a better understanding of microbial availability under various conditions.

Introduction Microbial degradation is the most important attenuation process for hydrophobic organic compounds (HOCs) in soil. Availability of HOCs to soil microorganisms is a topic that has received a great deal of attention, but our present understanding of the governing processes is still inconclusive (1, 2). While many studies show that soil organic matter is the most important variable for controlling the microbial availability of HOCs in soil (3, 4), a point of debate is the availability of the sorbed form of HOCs in microbial degradation (5-8). There exists ample evidence that suggests both views, i.e., microorganisms are capable of accessing only the freely dissolved form (5, 9), and microbes are also able to degrade the sorbed contaminant (6-8, 10-14). In addition, when sorbed HOCs are indirectly degraded through desorption into pore water, availability of sorbed HOCs to * Corresponding author e-mail: [email protected]. † Peking University. ‡ University of California, Riverside. 1852

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microorganism likely depends on the speed of desorption that may vary over soil types, HOC types, and contact time (15-20). It is accepted that in a soil or sediment, the freely dissolved concentration (Cfree) of a chemical is associated with the desorbable fraction of the sorbed contaminant (21, 22). Therefore, careful characterization of changes in Cfree during microbial degradation should shed light on the availability of sorbed HOCs. While Cfree is traditionally difficult to quantify, recent studies have established solid-phase microextraction (SPME) as a reliable method for detecting Cfree for a range of HOCs in soil and sediment (23, 24). Several variations of SPME, including disposable fibers, have been used to gain a better understanding of bioavailability of HOCs in causing baseline and acute toxicities to invertebrates (2, 25, 26). However, to our knowledge, so far SPME has not been used to evaluate microbial availability of HOCs. In this study, we used disposable polydimethylsiloxane (PDMS) fibers to detect Cfree of phenanthrene (PHE) in concurrence to measurement of its degradation by a PAH degrading bacterium in a range of soils. The correlation between Cfree and PHE degradation was analyzed against soil organic carbon (OC) content and time to ascertain microbial utilization of the different forms of PHE. The data were further used to delineate soil properties influencing the availability of PHE to the bacterium.

Experimental Section Soils. The tested soils were sampled from various locations in the surrounding areas of Beijing, China. The soils, with OC contents ranging from 0.23 to 7.1%, were crushed and sieved through a 2-mm mesh. Contents of soil OC, humic acid (HA), and fulvic acid (FA) were characterized in a previous study (27). The soil porosity was determined by using an ASAP 2010 Brunauer-Emmett-Teller (BET)-N2 Analyzer (Micromeritics, Norcross, GA). The surface area was calculated by the multipoint BET method (28). The total pore volume was determined as the amount of nitrogen sorbed at P/P0 ) 0.95 (29, 30). The micropore volume was calculated from the Dubinin-Raduskhevich equation, and the mesopore volume was calculated as the difference between the total and micropore volumes (28, 29). Selected properties for these soils are shown in Table 1. Chemicals. 14C-Phenanthrene (g95% purity, 40-60 mCi per mmol) and humic acid were obtained from Sigma-Aldrich (St. Louis, MO). The PYR-1 bacteria strain was donated by Dr. Cerniglia of the U.S. Food and Drug Administration in Jefferson, AR. The Spectrum/Spectra Por Dispodialyzer dialysis tube (1000 Dalton cutoff) was obtained from Fisher (Pittsburgh, PA). The PDMS fibers (430 µm glass core with 35 µm PDMS coating, Polymicro Technologies, Phoenix, AZ) were used for measuring Cfree. Fibers were cleaned by Soxhlet extraction with ethyl acetate for 72 h before use. Method Development. The partition coefficient (Kf) of PHE between PDMS and water was experimentally determined to allow calculation of Cfree from the concentration in PDMS fiber (CPDMS). A separate experiment was carried out to test the effect of dissolved organic matter (DOM) on Cfree measurement by SPME using dialysis membranes. Accumulation of PHE was determined for PDMS fibers in water and a DOM source (Aldrich HA) that were isolated by a dialysis membrane. The accumulation kinetics was analyzed to discern the matrix effect by DOM. Experimental details are given in the Supporting Information. Measurement of Freely Dissolved Concentrations. The Cfree of PHE was measured using the above SPME method in 10.1021/es802966z CCC: $40.75

 2009 American Chemical Society

Published on Web 02/13/2009

TABLE 1. Selected Properties of the Five Soils Used in the Present Study soil

A

B

C

D

E

OC (%) FAb (%) HAc (%) surface aread (m2 g-1) micropore volumee (cm3 g-1) mesopore volumef (cm3 g-1)

0.23 0.17 0.06 25.83 1.15 × 10-2 2.07 × 10-2

1.1 0.32 0.18 11.95 5.53 × 10-3 8.45 × 10-3

2.1 0.65 0.45 4.91 2.20 × 10-3 5.72 × 10-3

4.5 1.2 0.76 4.79 2.15 × 10-3 2.69 × 10-3

7.1 1.8 1.5 1.81 8.32 × 10-4 3.47 × 10-3

a

a Total organic carbon. b Fulvic acid. c Humic acid. d Surface area calculated using the multipoint Brunauer-EmmettTeller (BET) method. e Micropore volume calculated using the Dubinin-Raduskhevich equation. f Mesopore volume calculated from the difference between the total pore volume and micropore volume.

the solutions of the five soils that were aged for different lengths of time. A 20-g air-dried soil subsample was spiked with 1000 ng g-1 of 14C-PHE in 125-mL glass jars, and the spiked samples were rolled at 200 rpm for 21 d at room temperature. The equilibrated samples were further kept in the dark and at room temperature for aging. After 21, 50, 100, and 150 d of incubation, aliquots of soils were removed and used for measuring Cfree of PHE in the soil solution. An aliquot of the soil (1.0 g for the soil with 0.23% TOC and 0.5 g for all other soils) was transferred to a 6-mL glass vial, together with one piece of 0.5-cm PDMS fiber and 2 mL of 200 mg L-1 NaN3 solution. The samples were rolled at 200 rpm at room temperature for 3 d, which was found previously to be long enough for achieving equilibrium for PHE (24). Accumulation of 14C-PHE into PDMS (CPDMS) was measured on a Beckman LS 5000TD liquid scintillation counter (LSC) (Fullerton, CA), from which Cfree was calculated using the above obtained Kf. Simultaneously, 14C-PHE remaining in the soils was measured by combusting a small aliquot of soil at 900 °C using an OX-500 Biological Oxidizer (R. J. Harvey, Hillsdale, NJ). The 14CO2 produced from the combustion was trapped in 15 mL of Carbon-14 Cocktail (R. J. Harvey) and measured by LSC. The measurement showed that PHE did not undergo detectable degradation up to 150 d under the experimental conditions. Phenanthrene Degradation Experiment. Mycobacterium vanbaalenii PYR-1, which was originally isolated from an oil contaminated sediment, is well-known for its ability to mineralize PAHs by mono- and dioxygenase reactions (31, 32). The PYR-1 strain was cultured in 100 mL of a minimal salt medium (MSM) with around 1.0 g L-1 of pyrene as the carbon source. The strain was cultured in 250-mL Erlenmeyer flasks on a horizontal shaker at 28 °C and 120 rpm for 30 d, when the microbial DNA reached 28.7 ( 10.6 ng mL-1. The DNA was collected by the Fast DNA Spin Kit for soils (Bio 101 System, La Jolla, CA) and measured on Nanodrop ND-100 (Wilmington, DE). To evaluate the degradability of 14C-PHE, after 21, 50, 100, 150 d of incubation, 0.2 g of the soil sample was transferred to a 40-mL amber “respirometer” with 2.0 mL of PYR-1 strain solution diluted 10 times using MSM. The setup of the respirometers was similar to a previously reported method (33, 34). Briefly, a 40-mL amber glass vial was attached with a 2.0-mL GC vial (filled with 1.0 mL of 1 M NaOH solution) under the septum so that the evolved 14CO2 was trapped in the base solution. At 1, 3, 5, 24, 48, 96, 120, 144, 168, and 216 h, the NaOH solution was exchanged using syringes, and the sample solution was mixed with 5 mL of Carbon-14 cocktail for measurement of 14C activity, from which the mineralization rate of 14C-PHE was calculated. Three replicates were used for each measurement. Quality Assessment and Control. Several quality control measures were used in this study. Blank soil samples were spiked with a known amount of 14C-PHE and immediately combusted to test the 14C recovery of the combustion method. The mean recovery was 80.1%. During the degradability

experiment, positive controls were included to test the degradation capacity of the PYR-1 strain. Briefly, 2.0 mL of the PYR-1 strain solution was directly spiked with 1000 µg L-1 of 14C-PHE, and the evolved 14CO2 in the positive control was found to be 5.9 to 166 times that produced by the soil samples, suggesting viability of the PYR-1 strain. In addition, the mass balance for the degradation experiment was determined by accounting for 14C associated with the residue soil after centrifugation and the average recovery was found to be 85.2%. Statistical Analysis. All the model fits of data were conducted using SigmaPlot 10.0 (San Jose, CA). The correlation test was carried out using SPSS 10.0 (Chicago, IL).

Results and Discussion Freely Dissolved Concentrations of Phenanthrene in Soils. In soil-free solutions, CPDMS was found to be highly linear (R2 ) 0.996) in relation to the aqueous phase concentration Cw at equilibrium (Figure S1, Supporting Infromation). The calculated log Kf was 3.66 ( 0.23, which was in good agreement with the value (3.83 ( 0.01) in Ter Laak et al. (24). Dialysis membranes were used to test the effect of DOM on PHE uptake kinetics by PDMS fibers. The accumulated amount of PHE on the PDMS fiber inside the dialysis tube (with DOM) was significantly smaller than that outside the membrane during the first few hours (Figure S2, Supporting Infromation). For instance, the amount of PHE on the 1-cm PDMS fiber at 1 h was 36.8 ( 8.4 ng inside the tube and 63.1 ( 4.1 ng outside the tube. The corresponding values at 3 h were 71.5 ( 21.4 ng and 92.3 ( 11.2 ng. However, an apparent equilibrium was reached at 5 h (Figure S2), after which PHE concentrations on both fibers were identical. There have been several studies showing that typical levels of DOM (4-27 mg L-1) had no effect on Cfree measurement (35-37). Results from the present study suggested that equilibrium was quickly reached for PHE accumulation on PDMS fibers, and at equilibrium, DOM had no effect on PHE uptake kinetics by PDMS fibers, thus justifying the use of PDMS fibers for measuring Cfree of PHE in soil solutions. Disposable PDMS fibers were used to measure Cfree of PHE in the solutions of five soils with varying OC contents and also after the soils were aged for different lengths of time. Aging under the used conditions appeared to have little effect on the measured Cfree for the same soil. This was in contrast to previous studies confirming the effects of aging, and one possible reason was the relatively short contact time (up to 150 d) used in the present study, as compared with 300 d to 14 months in previous research (16, 17). However, Cfree of PHE displayed a significant decreasing trend with increasing soil OC content. After averaging across the different aging times, Cfree decreased by a factor of 36 while soil OC content increased by a factor of 30. The derived log KOC for PHE, ranging from 4.29 to 4.36, was similar for the different soils used in this study and was further comparable to the KOC range (log KOC ) 4.05 to 5.81) in Ter Laak et al. (24). VOL. 43, NO. 6, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 2. Degradation fractions of phenanthrene in soils at 216 h after inoculation of the PYR-1 strain. Bars represent standard deviations (n ) 3).

TABLE 2. Correlation between the Degradation Rate (% · h-1) of Phenanthrene by the PYR-1 Strain and the Freely Dissolved Concentration Cfree in Five Soils with Different Organic Carbon Contents intervals 0-1 h 1-3 h 3-5 h 120-144 h 144-168 h 168-216 h

FIGURE 1. Phenanthrene (PHE) degradation kinetics up to 216 d by the PYR-1 strain in two soils aged 21, 50, 100, and 150 d. (A) Soil with 2.1% organic carbon content. (B) Soil with 7.1% organic carbon content. CK: positive control with PHE spiked in soil-free medium; PR: predicted kinetics based on the coupled fast equilibrium and first-order degradation model. Bars represent standard deviations (n ) 3). Microbial Availability of Phenanthrene in Sorbed Forms. The degradation kinetics of PHE was measured as mineralization to CO2 in the five soils up to 216 h after inoculation of the PAH degrading bacterium PYR-1, as shown in Figure 1 for soils with 2.1% and 7.1% OC contents. Again, aging appeared to have an insignificant effect on the overall patterns of PHE mineralization in the same soil. After averaging across the different aging treatments, 52.0 ( 11.5 to 113.1 ( 2.2% of the spiked PHE was mineralized by the PYR-1 strain after 216 h. From the soil-free controls, the first-order degradation rate constant k for the freely dissolved PHE was calculated to be 0.027 ( 0.0038 h-1. To test whether the PYR-1 strain degraded only Cfree, a coupled fast equilibrium and firstorder degradation model was applied to the data (6, 12, 38): F ) e-Bfkt Bf )

1 1 + Kdm ⁄ V

(1) (2)

where F is the residue fraction of PHE in soil at time t, Bf is the bioavailability factor, V is the volume of the aqueous phase (2.0 mL in this study), m is the mass of the soil (0.2 g in this study), and Kd is the partition coefficient for PHE between soil and water phases, which was known from Cfree in soil solutions. Fit of data to eq 1 showed that estimated F values, under the assumption that only Cfree was available to the PYR-1 strain, were significantly greater than the measured residue fractions (Figure 2). For instance, the calculated residue fractions at 216 h for soils with 1.1% and 7.5% OC were 73.8 ( 9.5% and 95.5 ( 1.7%, respectively, while the measured residues were only 38.5 ( 3.4% and 44.6 ( 3.4%, respectively. For the soil with 0.23% OC, the calculated residue was 27.4 ( 10.3%, which was also much greater than the measured value (1.61 ( 0.63%). These discrepancies suggested that the assumption that only Cfree, which was sustained by desorption, was available to the bacteria resulted 1854

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ra P R2 a

0.733 0.908 0.483 0.001 0.001 0.031 0.537 0.825 0.233

0.577 0.008 0.333

0.345 0.136 0.119

0.028 0.908 0.001

Pearson correlation coefficient.

in substantial underestimations of PHE degradation by PYR1, or that the bacterium degraded PHE in the sorbed form. Guerin and Boyd (12) determined the differential bioavailability of naphthalene sorbed on soils to bacteria and observed organism specificity of the availability. Phenanthrene is less water soluble and less biodegradable than naphthalene. The present study provided evidence that sorbed PHE was directly available to Mycobacterium PYR-1, which may have important implications in in situ bioremediation of hydrophobic contaminants such as PHE. The degradation rate (% h-1) of PHE was calculated by dividing the mineralized fraction during a given time interval over the time increment, and the correlation between degradation rate and Cfree was then evaluated as a function of elapsed time t (Table 2). Pearson correlation analysis was further applied to quantitatively analyze the relationship between degradation rate and Cfree. The correlation was significant for time points up to 144 h (Pearson correlation coefficient r ) 0.483-0.908, significance level P ) 0.001-0.031), with the interval of 1-3 h showing the best relationship (r ) 0.908, P ) 0.001). However, Pearson correlation coefficient r decreased with t. For instance, correlation for the intervals of 144-168 h (P ) 0.136) and 168-216 h (P ) 0.908) was not statistically significant. Therefore, while PHE degradation was significantly related to Cfree of PHE in the soils initially, Cfree was not a dominating factor for the microbial availability of PHE after 144 h. As Cfree was at equilibrium with the desorbable fraction of PHE, the diminishing dependence of PHE degradation on Cfree over t suggested that the PYR-1 strain also utilized the fraction of sorbed PHE that was in the nondesorbable or sequestered form at a later stage, an observation consistent with earlier research (39, 40). The regressive dependence of PHE degradation on Cfree further implied that the PYR-1 strain first accessed the freely dissolved and reversibly sorbed fractions, and then the sequestered pool. Previous studies using Tenax-aided depletive desorption revealed that sorbed HOCs in soil or sediment were desorbed at different rates (41-43). Feng et al. (6) demonstrated the direct availability of sorbed biphenyl to bacteria, by using a

FIGURE 3. Correlations between the observed and predicted degradation fractions at different intervals. (A) 1 h, (B) 3 h, (C) 24 h, and (D) 144 h after bacteria inoculation. Predictions were based on the multivariate linear model including organic carbon content (OC) and humic coverage index (HCI). The dotted lines represented the 1:1 ratio between the measured and predicted values. Vertical and horizontal bars represent standard deviations of the predicted and observed values, respectively (n ) 3). model coupling desorption and mineralization. Uyttebroek et al. (8) reported that the mineralization rates of PHE on synthetic sorbents were higher than the initial abiotic desorption rate. Studies also showed that some microorganisms were able to metabolize the sequestered PAHs by directly attaching to particles or enhancing contaminant desorption (44, 45), a phenomenon considered as the microorganisms’ adaption to the low availability of PAHs (7, 46). It has also been shown that bacteria can form biofilms in response to the low availability of target compounds (7). Therefore, by following the relationship between Cfree and degradability, we further confirmed that sorbed PHE, including a fraction in the sequestered form, could be directly accessed by the bacteria. Effects of Soil Properties on Phenanthrene Degradation. Compared with the response of Cfree to soil OC content variations, the response of PHE degradation was much smaller. Unlike the 36-fold decrease in Cfree, the degraded fraction of PHE after 216 h only decreased by a factor of 1.6 to 2.1 over the same OC content range (Figure 2). Therefore, soil OC was apparently not the only property affecting the microbial availability of PHE in these soils. Several previous studies showed that soil porosity also affected sequestration and microbial availability of HOCs (10, 46-49). Analysis of the five soils used in this study showed that along with the 30-fold increase in soil OC content, soil surface area decreased from 25.83 to 1.81 m2 g-1, while the micropore volume decreased from 0.0115 to 0.000832 cm3 g-1, suggesting a negative relationship between soil porosity and OC content. This observation was consistent with Bogan et al. (48), who also found that the surface area and pore volume of six soils were inversely related with the soil OC content. The reduced porosity likely inhibited the sequestration of PHE in soils with higher OC contents, resulting in a relatively larger fraction of PHE in the more readily available form in those soils. To account for the effect of soil OC on soil porosity, Bogan et al. (48) introduced the humic coverage

index HCI, which was the ratio of the amount of humic acid (HA) and fulvic acid (FA) to surface area (SA). In the present study, in order to taking into account also the role of soil OC content, we modified the equation as below: D ) aOC + b

( HASA+ FA ) + c

(3)

where D is the degraded fraction of PHE in a given time interval, the ratio of (HA + FA) to SA is taken as HCI, and a, b, and c are regression constants. Data fit showed that there was generally a good correlation between degraded fractions of PHE from the different time intervals with soil OC and HCI (P ) 0.001-0.054, Figure 3). It is noteworthy that constant a was always negative, suggesting a negative effect of soil OC content on PHE availability. In comparison, constant b was always positive, suggesting that increasing surface area decreased the microbial availability of PHE. The overall analysis showed that the microbial availability of PHE was influenced by both soil OC and soil porosity properties, which contributed to a less than proportional response of PHE degradability to soil OC variations. Results from this study showed that the reversibly sorbed fraction and even some sequestered fraction of PHE were utilized by a microbial degrader in soils. The PAH degrader was found to first degrade the PHE pool available for equilibrium partition in the soils, and after the exhaustion of this readily available pool, to further degrade some of the sequestered PHE unavailable for partitioning, resulting in a deviation from a quantitative relationship between degradability and Cfree over time. Regression analysis also showed that both soil OC content and soil porosity affected the overall microbial availability of PHE in soils. This study highlights a new approach to characterize microbial availability of HOCs through kinetics analysis between degradation and Cfree. A similar approach may be applied to other HOCs to gain a better understanding of their microbial availability in soils VOL. 43, NO. 6, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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or sediments in a range of scenarios, such as during natural attenuation, bioremediation, and evaluation of aging effects.

Acknowledgments This study was supported by the China Scholarship Council to Yu Yang. We thank Dr. Cerniglia for providing the bacteria used in this study. We also thank Dr. Crowley for valuable comments on the research.

Supporting Information Available Experimental details on Kf determination and evaluation of matrix effect in measurement of freely dissolved concentrations using polydimethylsiloxane (PDMS) fibers; additional paragraphs and figures. These materials are available free of charge via the Internet at http://pubs.acs.org.

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