Effects of Plant and Soil Amendment on Remediation Performance and Methane Mitigation in Petroleum-Contaminated Soil
Department of Environmental Science and Engineering, Ewha Womans University, Seoul 03760, Republic of KoreaCorrespondence to:
J. Microbiol. Biotechnol. 2021; 31(1): 104-114
Published January 28, 2021
Copyright © The Korean Society for Microbiology and Biotechnology.
Petroleum hydrocarbons (PHs) are the most widely used fossil fuels worldwide and refined PH products (
Soils become extremely hydrophobic when polluted with PHs, thereby causing water deficiencies and an insufficient supply of major nutrients such as nitrogen and phosphorus, which are essential for plant and soil microorganism growth . This leads to a reduction in the diversity and activity of soil biota including plants, animals, and microorganisms, and consequently affects the overall soil ecosystem . Additionally, soil PH pollution impairs not only the specific contaminated area but also the aesthetic and economic value of the soil by causing odor problems associated with volatile PHs . Thus, considering the levels of incidence and potential damage, PH soil contamination is a major environmental problem that needs to be rapidly dealt with through appropriate remediation techniques.
Rhizoremediation, a representative biological remediation technique for treating petroleum-contaminated soils, removes organic pollutants by increasing the metabolic activity of rhizosphere microorganisms through plant synergisms . Various soil amendments are usually added during rhizoremediation to improve remediation efficiency by enhancing soil physicochemical characteristics such as fertility, water content, and nutrients [3, 5]. Particularly, the addition of soil amendments alters the amount of soil carbon and nitrogen utilized by soil microorganisms. For example, the application of organic fertilizers including manure was reported to increase soil methane emissions by supplying nutrients and organic acids .
Plants may also become involved in rhizosphere microorganism community composition and recent studies have reported that soil methane emissions were modified by changes in the microbiota composition involved in soil organic matter metabolic processes, which in turn had been altered by plant root exudation . However, the effects of plants on soil methane emissions have been found to vary depending on plant type and environmental conditions.
Also, PH-contaminated soil is seen increasingly as a considerable anthropogenic source of atmospheric methane. A recent in situ study of methane emissions in oil fields showed that methane emissions from contaminated soil were much higher (60-1,800 μg/m-2/h-1) than those from uncontaminated soil (29-33 μg/m-2/h-1) and suggested that PH biodegradation is mainly attributed to anaerobic microbial hydrocarbon degradation through methanogenesis . Methane is a major greenhouse gas estimated to have a global warming potential (GWP) of 28–36 over 100 years . When soils become contaminated with high oil concentrations, oxygen in the soil could be rapidly consumed, thereby resulting in anaerobic conditions . This phenomenon can stimulate the syntrophy between PH-degrading fermentation bacteria and methanogenic bacteria, which increases soil methane emissions . However, greenhouse gas emissions from soil are yet to be considered a major factor in rhizoremediation techniques and the effect of plants and soil amendments on the methane emission characteristics of rhizosphere microbial communities in petroleum-contaminated soil remains unclear.
In this study, the effects of major rhizoremediation factors (plants and soil amendments) on the remediation performance and potential methane emission characteristics in diesel-contaminated soil were investigated through an indoor pot experiment. Three types of soil systems, including a control condition (no planting), maize planting, and tall fescue planting, were set up. Maize and tall fescue were each selected as representative species of two plant groups: agronomic crops and grasses, respectively, which have distinct features for successful rhizoremediation, such as high biomass or extensive rhizosphere surface. Compost was applied as a soil amendment to investigate its usefulness associated with the degradation activity increase of indigenous microorganisms and methane emission reduction in the diesel-contaminated soil. The effects of exogenous microorganisms were studied compared to chemical nutrient (control).
During a 95-day period, rhizosphere soils were collected and soil residual total petroleum hydrocarbon (TPH) concentrations and potential methane emissions were analyzed. To follow up overall soil microorganism activity during remediation, dehydrogenase activity was analyzed as this enzyme is closely related to the microbial organic matter degradation process . The rhizosphere bacterial community dynamics and key functional genes were investigated through Illumina MiSeq sequencing and quantitative polymerase chain reaction (qPCR), respectively. The abundances of
The results of this study can be used to develop rhizoremediation strategies for methane emission mitigation during the remediation of diesel-contaminated soil.
Materials and Methods
Soil, Plants, and Soil Amendments Preparation
Potting soil mixture was purchased from a commercial provider (Simpol, Korea) and organic matter content, total nitrogen (T-N), ammonium nitrogen (NH4+-N) and total phosphorus (T-P) were measured as 41.38%, 0.450%, 2.58 mg/kg, and 1278.07 mg/kg, respectively. The soil mixture was contaminated with diesel to obtain a final concentration of 30,000 mg diesel/kg-soil. The diesel-contaminated soil was aged at 20°C without light for 5 days and manually mixed once a day during the aging process. A chemical nutrient and compost were then prepared as soil amendments. To prepare the chemical nutrient, 2.7 g of NH2CONH2, 3.4 g of (NH4)2HPO4, and 0.9 g of K2SO4 were added to 1 L of distilled water (2 g/l nitrogen; 0.8 g/l phosphate; and 0.4 g/l potassium). The compost, which was a mixture of pig manure with sawdust (6:4; v/v), was matured for 6 months (Korea). The organic matter content of the compost (T-N, NH4+-N, and T-P) was measured at 67.74%, 2.630%, 371.60 mg/kg, and 22834.52 mg/kg, respectively.
The initial pH of the soil mixture was 5.2 and the final pH after the experiment period was increased to the range of 5.8~6.6, depending on the type of plants and soil amendments.
Pot Experiment Preparation
A 3×3 factorial design pot experiment was conducted to investigate the effects of the experimental plants (control (no planting), maize, and tall fescue) and soil amendments (chemical nutrient and compost) on diesel-contaminated soil rhizoremediation and methane production potential. Two kilograms of diesel-contaminated soil were placed in each experimental pot (W 550 mm × L 195 mm × H 150 mm) for the control and tall fescue soil systems, whereas 5 kg were added to the maize soil system pot (W 600 mm × L 400 mm × H 210 mm). The chemical nutrient preparation and compost were added to the diesel-contaminated soil to a final concentration of 80 ml/kg and 100 g/kg, respectively. Then, 4~6 maize seedlings and 20 tall fescue seedlings were planted per pot, respectively. Two pots were prepared per each set of experimental conditions and then cultivated for 95 days at an indoor greenhouse located in the Asan Engineering Building, Ewha Womans University (37°56′65′′ N, 126°94′85′′ E). The average ambient temperature during the experiment period ranged from 16.4 to 31.6°C. All pots were watered 2~3 times a week to keep the surface soil from drying.
Soil Sampling and Pretreatment
Bulk soil sampling was conducted every 1~2 weeks during the experiment and plant roots remained undisturbed during sampling. Bulk soil was sampled from five random points in each pot and mixed homogeneously. Rhizosphere soil sampling was conducted at the end of the pot experiment. Rhizosphere soil firmly attached to each plant root was sampled by manual shaking and mixed homogeneously. Half of each soil sample was freeze-dried for residual TPH concentration analysis and soil DNA extraction (Bondiro Vacuum Freeze-dryer, IlShinBioBase, Korea). The remaining half of the soil samples was spread over a clean vinyl sheet and air-dried in an indoor laboratory for approximately 24 hours. After pretreatment, all soil samples were kept at -4°C until further analyses; soil samples for DNA extraction were stored at -20°C.
One gram of freeze-dried soil sample was placed in a glass test tube, after which 5 ml of hexane-acetone solution (1:1, v/v) was added to serve as an extraction solvent. Test tubes were tightly sealed using screw caps and Teflon tape to prevent solvent volatilization and then vortexed for 30 s. After 30 min of shaking (30°C, 200 rpm) and allowing the mixture to stand undisturbed for 30 min, 1 ml of supernatant was collected for each sample. A gas chromatography system (6980N Network GC System, Agilent Technologies, USA) equipped with a capillary column (L 30 m × ID 0.320 mm × T 0.25 μm; HP-5 GC column, J&W Scientific, Inc., USA) and a flame ionization detector (FID) was used to analyze the residual TPH concentration. The inlet and detector temperatures were 300°C and 320°C, respectively. N2 (99.999%, Dong-A Specialty Gases, Korea) was used as a makeup gas. The oven temperature was maintained at 60°C for the first 3 min, raised to 260°C at a 4°C/min rate, then raised to 310°C at an 84°C/min rate, and finally maintained for 5 min. A TPH standard curve was prepared using serial dilutions (500 to 40,000 ppm) of diesel fuel and FTRPH Calibration/Window Defining Standard (AccuStandard, Inc., USA).
Dehydrogenase Activity Analysis
Dehydrogenase activity was analyzed as described by Bremner and Tabatabai . Briefly, 0.5 g of air-dried soil sample was placed in a glass test tube, and 2 ml of Tris-HCl buffer (pH 7.6) and 1 ml of 1% (w/v) triphenyl tetrazolium chloride solution were added. The reaction mixture was incubated at 37°C in the dark for 24 h. Ten milliliters of ethanol (96%) was added as an extraction solvent, after which the mixture was vortexed for 30 s and centrifuged at 4,000 ×
Potential Methane Emission (PME) Analysis
To estimate the methane emission potential of rhizosphere soil, a modified version of the GHG (greenhouse gas) incubation method was applied . One gram of each air-dried soil sample was placed in a 35-ml glass vial. The moisture content of the soil samples was adjusted to field capacity (-33 kPa) by adding deionized water. The vials were then sealed with butyl stoppers and aluminum caps and incubated at 30°C for 60 days in quadruplicate. To measure accumulated CH4 concentrations, gas samples (100 μl) were collected 30 and 60 days post-incubation using a 300-μl gas-tight syringe (Hamilton, USA). Gas samples were analyzed with a gas chromatography system (7890A GC System, Agilent Technologies) equipped with a capillary column (L 30 m × ID 0.320 mm × T 1.80 μm; DB-624 GC Column, J&W Scientific, Inc., USA) and a flame ionization detector (FID). The inlet, oven, and detector temperatures were 230°C, 100°C, and 230°C, respectively, and N2 (99.999%, Dong-A Specialty Gases, Korea) was used as a makeup gas. A methane standard curve was prepared using serial dilutions (500 to 10,000 ppm) of methane gas (99%; Seoul Specialty Gases Co., Ltd., Korea).
Potential methane emissions were calculated with the following equation:
where, PME is the potential methane emission (μg/g-dry soil), x is the maximum methane concentration of headspace during the 60-day incubation period (ppmv), dry soil is the dry weight of the soil sample in the vial (g), MW is the molecular weight of the methane gas (g/mol), χ is the ratio of the molar mass of C to the molecular weight of the methane gas, P is the atmospheric pressure (atm), R is a gas constant, and VT is the vial headspace volume (ml).
DNA Extraction and Illumina MiSeq
Genomic DNA was extracted from 0.1 g of rhizosphere soil using a Nucleo Spin Soil Kit (Macherey-Nagel GmbH & Co. KG, Germany) and a BeadBeater-1 system (Biospec, USA). DNA extraction was performed following the manufacturer’s instructions. The DNA samples were collected in 50 μl of elution buffer and quantified using a SpectraMax QuickDrop Micro-Volume Spectrophotometer (Molecular Devices, USA). Extracted DNA samples were stored at -20°C until used.
A next-generation sequencing (NGS) approach was used to characterize bacterial community via the Illumina paired-end MiSeq sequencing platform (Macrogen Inc., Korea). The extracted DNA was used as a template for 16S sequencing library preparation, and the overall PCR process was conducted as described in a previous study . Each composite primer was designed based on the 515f and 806r primer sequences, which amplify the V4 region of the microbial 16S ribosomal RNA gene. Operational taxonomic unit (OTU) clustering was performed using the CD-HIT-OTU program . Raw reads with ambiguous bases and reads that didn’t match 515f/806r primers were removed. The median length was calculated for all reads and longer or shorter reads were trimmed through the length filter (200 bp ≤ good sequences ≤ 400 bp). The filtered reads were then clustered into clusters of duplicates if they were aligned at 5’ and shared 100% identity over the full length of shorter sequences, as reads are different in length. Chimeric reads were identified in this step and removed. Singletons were also removed in the OTU clustering process. OTUs were determined at 3% dissimilarity using QIIME software (Macrogen Inc.). The final taxonomy proportions and alpha diversity indices were calculated after normalized read number in each sample.
Functional Gene qPCR
TPH-degrading bacteria and methane-oxidizing bacteria in the rhizosphere soil during rhizoremediation were estimated via qPCR using a CFX96 TouchTM Real-Time PCR Detection system (Bio-Rad Laboratories Inc., USA). Soil DNA samples used for Illumina MiSeq high-throughput sequencing were also analyzed via qPCR. The
The composition of the reaction mixture for quantitative PCR was as follows: 10x PCR buffer with MgCl2 (Genenmed Inc., Korea), 1x; dNTP mixture (Genenmed Inc.), 200 μM; forward primer, 0.2 μM; reverse primer, 0.2 μM; SYBR (Invitrogen, USA), 2x; Rox reference dye (Invitrogen), 2x; Taq polymerase (Genenmed Inc.), 0.025 U/μl. Two microliters of DNA was added as a template and the final volume was adjusted to 25 μl. qPCR was performed in duplicate. Then, 16S rRNA and
One-way and two-way analyses of variance (one-way ANOVA, two-way ANOVA) were conducted to compare the significant differences in the multiple data. The level of significance for different treatments was determined using a Scheffe post-hoc test at a 95% level (
Soil Microbial TPH Remediation Performance and Dehydrogenase Activity
Fig. 1 illustrates the changes in residual TPH concentrations in soil treated with different kinds of plant and soil amendments. The initial soil TPH contamination level was 36,696 ± 2,809 mg TPH/kg soil. In the control soil system, a lag phase was observed during the first 12 days, with no significant change in residual TPH concentration. TPHs then rapidly decreased until day 22, after which the concentration level (14,660~22,119 mg TPH/kg soil) was maintained until day 45. This level tended to gradually decrease after day 45 and the fastest TPH removal rate was observed when compost was added throughout the entire experimental period (Fig. 1A). In contrast, TPHs decreased immediately in soils treated with maize and tall fescue, and no lag phase was observed (Figs. 1B and 1C). In both conditions, the TPH concentration decreased rapidly to 11,438~12,054 and 8,996~10,003 mg TPH/kg soil, respectively, and TPH removal rates in the tall fescue-treated soil continued to decline after day 45.
Time profiles of residual TPH concentration for each soil condition.( A) control (no planting), ( B) maize planting, and ( C) tall fescue planting.
Relative qPCR analysis was performed to investigate
( alkBgene abundance relative to the initial abundance at 0 d. A) control (no planting), ( B) maize planting, and ( C) tall fescue planting.
Fig. 3 illustrates the changes in rhizosphere soil dehydrogenase activity treated with different kinds of plants and soil amendments. In the control soil system treated with the chemical nutrient preparation, dehydrogenase activity rapidly increased to 449 ± 73 μg TPF/(g dry soil/d) during the first 38 days (Fig. 3A), then decreased to 176± 49 μg-TPF/(g dry soil/d) on day 45, after which the activity level remained largely constant until the end of the experiment. In the case of compost addition, dehydrogenase activity increased up to 499 ± 65 μg TPF/(g dry soil/d) during the first 22 days and decreased after day 64. Furthermore, dehydrogenase activities increased up to 220 ± 56 and 296 ± 107 μg TPF/(g dry soil/d) until day 12 when the chemical nutrient preparation was added in maize- and tall fescue-treated soil, respectively. Both activity levels were maintained during the entire experiment. Moreover, in the soil system with maize and compost, dehydrogenase activity increased up to 489 ± 61 μg TPF/(g dry soil/d) on day 12 and showed a consistent increase after day 38. Similarly, when compost was added to the tall fescue soil system, the activity level increased up to 495 ± 117 μg TPF/(g dry soil/d) on day 12 and continued increasing steadily after day 68.
Dehydrogenase activity time profiles in the three studied soil conditions.( A) control (no planting), ( B) maize planting, and ( C) tall fescue planting.
Potential Soil Methane Emission and
pmoA Gene Dynamics
Fig. 4 illustrates the methane emission potential of each soil system treated with different soil amendments at different experimental times. On day 12, the emitted methane level in the chemical nutrient-treated tall fescue system soil (958 ± 186 μg C/g dry soil) was 1.8-fold higher than that of compost-treated soil (528 ± 50 μg C/g dry soil) (Fig. 4C). On day 30, methane emissions in the soil systems were exhibited in the following order: control > tall fescue > maize, and the control soil treated with compost showed its highest methane emission of 1,597 ± 340 μg C/g dry soil (Fig. 4A). The maize soil system treated with compost temporarily showed its highest methane emission of 974 ± 37 μg C/g dry soil on day 45; however, it showed the lowest methane emissions among the soil systems overall (Fig. 4B). Potential methane emissions tended to decrease from day 64 onwards under all conditions examined herein.
Potential methane emission in the three examined soil conditions during the experiment.( A) control (no planting), ( B) maize planting, and ( C) tall fescue planting.
Plant types were found to have a statistically significant effect on potential methane emission except for day 95 (
Absolute qPCR analysis was performed to investigate
( pmoAgene copy numbers in the three examined soil conditions during the experiment. A) control (no planting), ( B) maize planting, ( C) tall fescue planting.
Rhizosphere Bacterial Community Dynamics
Illumina MiSeq sequencing was performed to characterize the rhizosphere bacterial community in the soils treated with different kinds of plant and soil amendments. Table S2 summarizes the alpha diversities calculated from the sequencing data. Under all examined conditions, high bacterial diversities in rhizosphere soil samples were detected by the Shannon index (over 8.00) and inverse Simpson index (over 0.99) (Table S2).
Fig. S2 shows the profiles of bacterial community in each sample; any bacterial species that did not belong to the top 60 species were categorized as “others.”
PCA was also performed to compare the bacterial communities in each soil system (Fig. 6). The bacterial community of the initial contaminated soils (day 0) was different depending on the type of soil amendments, which is likely due to the existence of various exogenous microorganisms in the compost. Significant changes were observed in overall bacterial community as a function of time. Control soil bacterial structures were relatively stable from day 45 until day 95, and that of chemical nutrient-treated soil, especially, showed the least change between the two aforementioned time points. On day 45, the chemical nutrient-treated maize and tall fescue soil systems showed similar bacterial structures, whereas the compost-treated soils in both systems were significantly different from each other. On day 95, the chemical nutrient- and compost-treated soil in the tall fescue system exhibited the highest similarity distances (
Fig. 6. Principal component analysis (PCA) of soil bacterial community after 0 d, 45 d, and 95 d from the start of the experiment.
Effect of Rhizoremediation Factors on TPH Removal Performance and Dehydrogenase Activity
Plants that promote the decomposition of organic contaminants in soil share common characteristics, including extensive and fibrous roots that form an extended rhizosphere . These plants include many common grasses, maize, and legumes (
In the previous study of petroleum contaminant rhizoremediation, dehydrogenase activity was demonstrated to be more relevant in TPH removal efficiency than the TPH-degrading microorganism biomass itself . In this study, the average rate of change in dehydrogenase and the average removal rate of TPH in each sampling time interval showed a moderate positive linear relationship with the Pearson correlation coefficient of 0.324 (
Since microbial communities in the petroleum-contaminated soils have low biodiversity and biomass, it is hard to maintain favorable environmental conditions for the survival of remediation plants . Soil amendments can be applied for the purpose of increasing the rate or extent of biodegradation of PHs, which improves the activity of the soil microorganisms. In this study, the potting soil mixture was contaminated with a high concentration of diesel (30,000 mg diesel/kg soil). As the indigenous microorganisms in the soil mixture may not be capable of degrading the high loads and wide ranges of substrates in diesel, compost and chemical nutrient (control) were added to study the effect of soil amendments on the enhancement of the overall degrading activity of the soil microorganisms. When compost is added to petroleum-contaminated soil, exogenous microorganisms including bacteria and fungi are introduced into the soil ecosystem, which stimulates the degradation of various organic contaminants into less toxic substances. Moreover, high nutrient loads in compost can enhance soil fertility and plant growth, resulting in the removal of organic contaminants in the soil . A previous study reported that compost addition increased diesel removal from soils both with and without ryegrass while the soil with ryegrass showed a much lower level of residual diesel concentration . Likewise, in this study, the TPH removal efficiency and dehydrogenase activity of the compost-amended soil with maize and tall fescue planting were higher than those of other soils.
Effects of Rhizoremediation Factors on Potential Methane Emission
Plants affect soil methane emission by secreting various organic acids as plant root exudation, which can be utilized by microorganisms that participate in the production and elimination of methane . Moreover, many previous studies have reported that rice roots can reduce soil methane emissions in paddy fields. Plant roots enable the ambient oxygen to enter the rhizosphere, thereby changing the soil redox potential . This leads to the retention of a certain portion of the soil-emitted methane, resulting in favorable conditions for methanotrophs . This study found that plant types had statistically significant effects on potential methane emission and the maize planting soil system showed the lowest methane emission among the soil systems (Fig. 4). However, no significant difference in
Many field studies of maize soil (usually conducted in crop rotation systems with legumes due to their having several advantages) demonstrated that the plots showed negligible methane flux, or they acted as a methane sink [33-36]. Meanwhile, the maize rhizosphere soils in the previous study were demonstrated to have completely different microbial community and methanogenic bacterial species compared with those of the rice rhizosphere soils. . Another maize field study with biochar applications showed a significant decrease in the soil of saprotrophic fungi, which were previously reported to produce methane without the involvement of methanogenic archaea [38, 39]. Similarly, in our study, we found that the maize soil showed lower methane emissions especially with compost, and the composition of microbial community significantly altered during the rhizoremediation. Thus, it is assumed that the maize and compost altered the major composition of methanotrophic species (Fig. 7), resulting in less methane emission in the TPH-contaminated environment. However, further testing is needed with greater consideration given to methanogenesis and mcrA gene copy numbers.
Multivariate analysis including 10 major functional species of TPH-degrading bacteria and methylotrophs.PCA biplot represents the bacterial community in different soil systems. Arrows represent projections of the species that are responsible for the differences between groups.
The results in Figs. 4 and 5 confirmed that the addition of compost both increased the potential methane emission and the
Major Functional Bacterial Species During Rhizoremediation
Based on our indoor pot experiment bacterial community analysis, various microorganisms associated with TPH degradation were identified (Fig. S2).
Notably, this study identified various microorganisms related to methane oxidation; however, not all of them were included in the top sixty bacterial community species. For instance, methylotrophs such as
Multivariate analysis including 10 major functional bacterial species was performed and represented as a PCA-biplot of microbial structures of the soil systems (Fig. 7). The 0 d soil systems were clearly characterized with the high abundance of
This study investigated the effects of plants and soil amendments on methane emission characteristics during the rhizoremediation of diesel-contaminated soil. Based on TPH removal efficiency and greenhouse gas emission reduction, maize and tall fescue soil planting was found to be an effective remediation enhancement strategy. Moreover, compost was found to be an effective soil amendment, improving overall remediation efficiencies while also increasing both potential methane emissions and
Supplementary data for this paper are available on-line only at http://jmb.or.kr.
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (NRF-2019R1A2C2006701).
Conflict of Interest
The authors have no financial conflicts of interest to declare.
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